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. 2017 Apr 22;370(1):1–11. doi: 10.1007/s00441-017-2618-8

Cell culture: complications due to mechanical release of ATP and activation of purinoceptors

Geoffrey Burnstock 1,2,✉, Gillian E Knight 1
PMCID: PMC5610203  PMID: 28434079

Abstract

There is abundant evidence that ATP (adenosine 5′-triphosphate) is released from a variety of cultured cells in response to mechanical stimulation. The release mechanism involved appears to be a combination of vesicular exocytosis and connexin and pannexin hemichannels. Purinergic receptors on cultured cells mediate both short-term purinergic signalling of secretion and long-term (trophic) signalling such as proliferation, migration, differentiation and apoptosis. We aim in this review to bring to the attention of non-purinergic researchers using tissue culture that the release of ATP in response to mechanical stress evoked by the unavoidable movement of the cells acting on functional purinergic receptors on the culture cells is likely to complicate the interpretation of their data.

Keywords: P1 receptors, P2 receptors, Purinoceptor, Shear stress, Ectonucleotidases

Introduction

While it was recognised early that ATP (adenosine 5′-triphosphate) is released from damaged or dying cells, it was shown more recently that gentle mechanical perturbation, such as shear stress, membrane stretch and hypo-osmotic cell swelling, leads to release of ATP from most cell types (Bodin and Burnstock 2001; Bodin et al. 1991; Chaudry 1982; Dolovcak et al. 2011; Forrester 1972; Grygorczyk and Guyot 2001; Milner et al. 1990, 1992; Praetorius and Leipziger 2009, 2010; Sperlágh et al. 2007; Wang et al. 1996). In the outstanding review by Lazarowski et al. (2011), it was stated that “P2Y receptor expression-dependent formation of second messengers was noted in cultured cells subjected to mechanical stress, for example medium displacement or cell wash (Filtz et al. 1994; Lazarowski et al. 1995; Parr et al. 1994). A vast number of studies have followed, illustrating that nonlytic release of ATP occurred in practically every cell type subjected to physical stresses, such as flow resulting in shear stress, hydrostatic pressure, osmotic swelling or shrinking, compressive stress, mechanical loading, plasma membrane stretch, hypoxia and cell swelling” performed during routine experimental procedures, such as cell rinsing and medium changes. It is unlikely that ATP release caused by gentle mechanical stimulation arises from cell damage, for example mechanical stimulated ATP release occurs without associated membrane conductive changes (Hamill and Martinac 2001). Many novel assays (or sensors) have been developed to detect ATP release from cells, including luciferin–luciferase bioluminescence and atomic force microscopy (see Dale and Frenguelli 2012; Furuya et al. 2014; Khlyntseva et al. 2009; Praetorius and Leipziger 2009).

The mechanisms responsible for the transport of ATP from cells have been a matter of intense debate. For most cell types, it appears to be a combination of vesicular exocytosis and connexin or pannexin hemichannels (Dahl 2015; Dubyak 2007; Lazarowski et al. 2011; Li et al. 2011; Lohman and Isakson 2014; Novak 2003; Scemes et al. 2009; Spray et al. 2006), although for some cells ATP-binding cassette transporters or maxi ion channels have been claimed (Sabirov and Okada 2005). It has also been proposed that P2X7 receptors may mediate ATP release (Pellegatti et al. 2005; Suadicani et al. 2006). A vesicular nucleotide transporter has been identified (Sawada et al. 2008).

ATP released from cells is rapidly broken down by ectonucleotidases to adenosine (see Cardoso et al. 2015; Yegutkin 2008; Zimmermann 2006) but both ATP and adenosine will have functional effects on the cells via P1, P2X and P2Y receptors (see Corriden and Insel 2010).

Two purinoceptor families were recognised in 1978, namely P1 (adenosine) and P2 (nucleotide) receptors (Burnstock 1978). Purinoceptor subtypes were cloned and characterised in the early 1990s, consisting in 4 P1 G protein-coupled receptor subtypes, 7 P2X ion channel receptor subtypes and 8 P2Y G protein-coupled receptor subtypes (see Burnstock 2007; Ralevic and Burnstock 1998).

Release of ATP from cultured cells in response to mechanical stimulation

A comprehensive summary is shown in Table 1.

Table 1.

ATP release from cultured cells in response to mechanical stimulation

Cell type Stimulus References
Vascular endothelial cells Shear stress Bodin et al. 1991
Li et al. 2015
Milner et al. 1990, 1992
Xiang et al. 2007
Yamamoto et al. 2011
Hypotonic stress Hisadome et al. 2002
Oike et al. 2000
Shinozuka et al. 2001
Mechanical stretch Hamada et al. 1998
Airways
 Lung epithelial cells Stretch Ramsingh et al. 2011
Zhang et al. 2014
Mechanical stress Guyot and Hanrahan 2002
Homolya et al. 2000
Hypotonic stress Okada et al. 2006
Ransford et al. 2009
Seminario-Vidal et al. 2011
 Nasal epithelial cells Mechanical stimulation Watt et al. 1998
 Tracheal epithelial cells Hypotonic stress Kawakami et al. 2004
Eye
 Retinal ganglion cells Swelling Xia et al. 2012
Mechanical stretch Xia et al. 2012
 Retinal pigment cells Hypertonic stress Eldred et al. 2003
Hypotonic stress Mitchell 2001
Reigada and Mitchell 2005
 Retinal glial (Müller) cells Hypo-osmotic swelling Brückner et al. 2012
Voigt et al. 2015
 Lens Hypertonic stress Eldred et al. 2003
 Ciliary epithelial cells Hypotonic stress Li et al. 2010
Mitchell et al. 1998
 Trabecular meshwork cells Mechanical stress Luna et al. 2009
Swelling Li et al. 2011, 2012
 Corneal endothelial cells Mechanical stimulation Gomes et al. 2005
Liver
 Hepatocytes Hypotonic cell swelling Pafundo et al. 2008
 Biliary epithelium (cholangiocytes) Hypotonic cell swelling Roman et al. 1999
Sathe et al. 2011
Shear stress Woo et al. 2008, 2010
Glial cells
 Astrocytes Hypotonic cell swelling Beckel et al. 2014
Darby et al. 2003
Liu et al. 2008
Mechanical stimulation Beckel et al. 2014
Lee et al. 2015
Stout et al. 2002
Zhang et al. 2008
 Astrocytoma cells Hypotonic stress Blum et al. 2010
Joseph et al. 2003
 Microglia Mechanical stimulation Bennett et al. 2008
Bladder urothelial cells Stretch Mansfield and Hughes 2014
Sun and Chai 2002
Sun et al. 2001
Mechanical stress McLatchie and Fry 2015
Hypotonic stimulation Birder et al. 2003
Muscle
 Vascular smooth muscle Mechanical stretch Hamada et al. 1998
 Bronchial smooth muscle Mechanical stretch Takahara et al. 2014
 Cardiomyoctes Mechanical stretch Kim and Woo 2015
Oishi et al. 2012
Swelling Dutta et al. 2004, 2008
Fibroblasts
 L929 fibroblasts Shear stress Grierson and Meldolesi 1995
 Subepithelial fibroblasts Mechanical stimulation Furuya et al. 2005, 2014
Murata et al. 2014
 NIH/3T3 fibroblasts Hypotonic shock Boudreault and Grygorczyk 2002, 2004
 Cardiac fibroblasts Hypotonic stimulation Lu et al. 2012
Bone
 Bone marrow stromal cells Fluid flow (shear stress) Riddle et al. 2007
 Periodontal ligament Mechanical stress Ito et al. 2014
Luckprom et al. 2010, 2011
Wongkhantee et al. 2008
 Osteoblastic cells Mechanical stress Hecht et al. 2013
Romanello et al. 2001, 2005
Shear stress/fluid flow Gardinier et al. 2014
Genetos et al. 2005
Rumney et al. 2012
Xing et al. 2014
 Intervertebral disc annulus cells Vibratory stimulation Yamazaki et al. 2003
 Chondrocytes Hypotonic challenge Rosenthal et al. 2013
Mechanical stress Graff et al. 2000
Kono et al. 2006
Millward-Sadler et al. 2004
 MLO-Y4 osteocytes Mechanical loading by fluid flow Genetos et al. 2007
Focal-force stimulation Wu et al. 2013
Mechanical stimulation Kringelbach et al. 2015
Membrane stretch Thompson et al. 2011
Immune cells
 Jurkat T lymphocytes Hypertonic stress Loomis et al. 2003
Woehrle et al. 2010
Yip et al. 2007
Mechanical stress Loomis et al. 2003
Shockwaves Weihs et al. 2014
Yu et al. 2010
Osmotic stress Corriden et al. 2007
 B lymphoblasts Slow motion Sakowicz-Burkiewicz et al. 2010
 Neutrophils Hypertonic stress Chen et al. 2004, 2015
 Mast cells Hypo-osmotic stress Wang et al. 2013
 Macrophages Hypotonic stress Burow et al. 2015
Tumour cells
 Prostate cancer cells Hypotonic stress Nandigama et al. 2006
Mechanical stress Sauer et al. 2000
 Hepatoma cells Hypotonic stress Dolovcak et al. 2011
Espelt et al. 2013
Feranchak et al. 2010
Wang et al. 1996
 Cholangiocarcinoma Hypotonic cell swelling Gatof et al. 2004
Roman et al. 1999
 Lung epithelial carcinoma (A549) cells Hypotonic shock Seminario-Vidal et al. 2011
Tatur et al. 2008
Shear stress Ramsingh et al. 2011
Stretch Grygorczyk et al. 2013
 Mammary carcinoma (C127) cells Hypotonic challenge Hazama et al. 2000
Sabirov et al. 2001
 Ehrlich ascites tumour cells Mechanical stress Pedersen et al. 1999
 Ovarian carcinoma (SKOV-3) cells Mechanical stimulation Vázquez-Cuevas et al. 2014
 L929 fibrosarcoma cells Hypotonic challenge Islam et al. 2012
Skin
 Adipose tissue-derived stem cells Shock wave treatment Weihs et al. 2014
 Keratinocyte cell lines Air stimulated Denda and Denda 2007
Barr et al. 2013
Mechanical stimulation Burrell et al. 2005
Koizumi et al. 2004
Pancreas
 Acinar cells Mechanical stimulation Haanes et al. 2014
 Duct cells Mechanical & hypotonic stress Kowal et al. 2015
Xenopus oocytes Hypertonic stress Aleu et al. 2003
Stem cells
 Mesenchymal stem cells Shock waves Sun et al. 2013
Weihs et al. 2014
Gut
 Epithelial cell lines Hypotonic challenge Dezaki et al. 2000
van der Wijk et al. 2003
Osmotic cell swelling Tomassen et al. 2004
Salivary glands
 Submandibular gland Mechanical stimulation Ryu et al. 2010
Kidney
 Collecting duct epithelial cells Mechanical stimulation Hovater et al. 2008
 A6 distal nephron epithelial cells Mechanical stretch Ma et al. 2002
Hypotonic treatment Gheorghiu and Van Driessche 2004
Jans et al. 2002
Silva and Garvin 2008
 MDCK cells Pressure pulses Praetorius et al. 2005
Shear stress Rodat-Despoix et al. 2013
 Epithelia from cysts of polycystic kidneys Hypotonic challenge Wilson et al. 1999
Blood cells
 Erythrocytes Hypotonic stretch Locovei et al. 2006
 Platelets Shear stress Mills et al. 1968
 Leukocytes Osmotic stress Corriden et al. 2007
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Purinergic receptor expression in cultured cells

A comprehensive summary is shown in Table 2.

Table 2.

Purinergic receptor expression in cultured cells (references in Table 1)

Cell type Receptors expressed
P2X P2Y P1
Vascular endothelial cells P2X4, P2X5, P2X7 P2Y1,2 and 12 A1
Airways
  Lung epithelial cells P2X4, P2X5 P2Y1,2,4,6 and 11 A1, A2A, A2B
  Nasal epithelial cells P2Y2, P2Y6, P2Y11 A2B
  Tracheal epithelial cells P2X4, P2X7 P2Y1, P2Y2 A2B
Eye
  Retinal ganglion cells P2X2-7 A1, A2A, A3
  Retinal pigment cells P2X2, P2X3, P2X7 P2Y2 A1, A2A, A2B, A3
  Retinal glial (Müller) cells P2X7 P2Y1 A1
  Lens P2X1, P2X4 A1
  Ciliary epithelial cells P2X2, P2X3, P2X7 P2Y2 A1, A2A, A2B, A3
  Trabecular meshwork cells P2X1, P2X7 A1
  Corneal endothelial cells P2X4-7 P2Y1,2,4 and 6
Liver
  Hepatocytes P2X4, P2X7 P2Y1,2,4 and 6 A2A, A2B, A3
  Biliary epithelium (cholangiocytes) P2X4 P2Y1,2,4,6,11,12 and 13 A2A
Glial cells
  Astrocytes P2X4, P2X7 P2Y1, P2Y2 A1, A2A, A3
  Astrocytoma cells P2X7 P2Y1, P2Y2 A2A, A2B, A3
  Microglia P2X4, P2X7 P2Y1, P2Y11, P2Y12 A1, A2A, A2B
Bladder urothelial cells P2X2, P2X3, P2X4 P2Y1,2,4 and 6 A1
Muscle
  Vascular smooth muscle P2X1, P2X2, P2X4 P2Y1,2,4 and 6 A2A, A2B, A3
  Bladder smooth muscle P2X1, P2X2 P2Y2, P2Y6 A1, A2A, A2B
  Cardiomyoctes P2X1,3,4,5,6 and 7 P2Y1, P2Y2 A1, A2A, A2B
Fibroblasts
  Fibroblasts P2X7 P2Y2 A2A, A2B
  Cardiac fibroblasts P2X4, P2X7 P2Y2 A1, A2A, A2B, A3
Bone
  Bone marrow stromal cells P2X7 P2Y1,2,6 and 11 A2B
  Periodontal ligament P2Y1,2,4 and 6 A2A
  Osteoblastic cells P2X1-7 P2Y1,2,4,6,12,13 and 14 A2A, A2B
  Intervertebral disc annulus cells P2X4, P2X7
  Chondrocytes P2X1,3,4,5 and 7 P2Y2 A2A, A2B
  MLO-Y4 osteocytes P2X1,2,3,4 and 7 P2Y2,4,12 and 13
Immune cells
  Jurkat T lymphocytes P2X1,4,5 and 7 A1, A2A, A2B, A3
  B lymphoblasts A2A
  Neutrophils P2X1, P2X4, P2X7 P2Y2,4,6 and 11 A1, A2A, A2B, A3
  Mast cells P2X7 P2Y1, P2Y2 A2A, A2B, A3
  Macrophages P2X7 P2Y2, P2Y6 A2A, A2B
Tumour cells
  Prostate cancer cells P2X4-7 P2Y1,2,6 and 11 A1, A2A, A2B, A3
  Hepatoma cells P2Y1,2,4,6 and 13 A2A, A2B, A3
  Cholangiocarcinoma P2Y2
  Lung epithelial carcinoma (A549) cells P2X4-7 P2Y2, P2Y4, P2Y6 A2A, A2B, A3
  Mammary carcinoma cells P2X7 P2Y1 A1, A2A, A3
  Ehrlich ascites tumour cells P2Y1, P2Y2
  Ovarian carcinoma (SKOV-3) cells P2X7 P2Y2, P2Y6
  L929 fibrosarcoma cells P2X7
Skin
  Keratinocyte cell lines P2X2,3,5 and 7 P2Y1,2,4,6 and 11
Pancreas
  Acinar cells P2X12,3,4,6 and 7 P2Y1,2,4,11,12,13 and 14 A1, A2A, A2B
  Duct cells P2X1,2,4,5,6 and 7 P2Y1,2,4,6,11,12,13 and 14 A1, A2A, A2B, A3
Xenopus oocytes P2X4 P2Y2-like Atypical A1
Stem cells
  Mesenchymal stem cells P2X4,5,6 and 7 P2Y1,2,4,11,13 and 14 A1, A2A, A2B
Gut
  Epithelial cell lines P2X7 P2Y2, P2Y6 A2A, A2B
Salivary glands
  Submandibular gland P2X1-7 P2Y1, P2Y2
Kidney
  Collecting duct epithelial cells P2X4, P2X5, P2X6 P2Y1,2,4 and 6 A1, A2A, A2B, A3
  A6 distal nephron epithelial cells P2X4 P2Y1, P2Y2 A1, A2
  MDCK cells P2X7 P2Y1,2,6 and 11 A1
  Epithelia from cysts of polycystic kidneys P2X4, P2X5 P2Y1, P2Y2, P2Y6
Blood cells
  Erythrocytes P2X1, P2X4, P2X7 P2Y1, P2Y2 A2B
  Platelets P2X1 P2Y1, P2Y12, P2Y14 A2A, A2B
  Leukocytes P2X4, P2X7 P2Y2, P2Y6 A1, A2A, A2B, A3
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When cells are cultured, they de-differentiate, which is associated with changes in receptor expression. If the cell density is high, the cells usually re-differentiate and this again is associated with changes in receptor expression (see, e.g., Chamley et al. 1974). Upregulation of P2Y2 receptors in rat salivary gland cells during short-term culture has also been reported (Turner et al. 1997).

Function of purinergic receptors on cultured cells in response to released ATP

A comprehensive review of the functional expression of P2 receptors on a wide range of cell types is available (Burnstock and Knight 2004). Some examples follow. ATP released from retinal epithelial cells acts via P2 receptors to increase the rate of fluid transport or decrease phagocytosis (Mitchell 2001) and regulate neural retinal progenitor cell proliferation (Pearson et al. 2005). ATP released by osteoblasts inhibits bone mineralisation (Orriss et al. 2013). Stretch-released ATP from fibroblasts results in cell proliferation (Wang et al. 2005). ATP released from astrocytes mediates glial calcium waves (Guthrie et al. 1999). ATP released from endothelial cells by shear stress acts on endothelial P2 receptors to release nitric oxide resulting in vasodilatation (Burnstock and Ralevic 2014).

Mechanically-induced Ca2+ waves have been observed in a variety of cells, including chondrocytes (D’Andrea and Vittur 1996), airways epithelial cells (Boitano et al. 1994; Hansen et al. 1993; Sanderson et al. 1990), glial cells, including Müller cells (Charles et al. 1991, 1992, 1993; Newman 2001), keratinocytes (Koizumi et al. 2004), endothelial cells (Demer et al. 1993), T cells (Wang et al. 2014), mast cells (Osipchuk and Cahalan 1992) and others (see Leybaert and Sanderson 2012). It is likely that they are due to the activation of purinergic receptors by ATP released from the mechanically stimulated cells, mainly via P2Y1 and P2Y4 receptors (Frame and de Feijter 1997; Gallagher and Salter 2003; Stamatakis and Mantzaris 2006). Calcium waves are a dynamic intracellular signalling mechanism that allows spatiotemporal information to be rapidly propagated in tissues. ATP released at sites of cell stress signals danger to the immune system.

Conclusion: need for re-interpretation of data derived from cell culture experiments

Release of ATP from cultured cells is unavoidable, due to gentle mechanical stimulation. The released ATP acts on purinoceptors expressed by these cells, which mediate both secretion and trophic events, such as cell proliferation, differentiation, death and migration. These events mean that interpreting results from experiments based on tissue culture need to take into account the effects of released ATP and its actions on purinoceptors.

Compliance with ethical standards

Declarations

The authors declare that they have no conflict of interest.

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Aleu J, Martín-Satué M, Navarro P, Pérez de Lara I, Bahima L, Marsal J, Solsona C. Release of ATP induced by hypertonic solutions in Xenopus oocytes. J Physiol. 2003;547:209–219. doi: 10.1113/jphysiol.2002.029660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barr TP, Albrecht PJ, Hou Q, Mongin AA, Strichartz GR, Rice FL. Air-stimulated ATP release from keratinocytes occurs through connexin hemichannels. PLoS ONE. 2013;8:e56744. doi: 10.1371/journal.pone.0056744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beckel JM, Argall AJ, Lim JC, Xia J, Lu W, Coffey EE, Macarak EJ, Shahidullah M, Delamere NA, Zode GS, Sheffield VC, Shestopalov VI, Laties AM, Mitchell CH. Mechanosensitive release of adenosine 5′-triphosphate through pannexin channels and mechanosensitive upregulation of pannexin channels in optic nerve head astrocytes: a mechanism for purinergic involvement in chronic strain. Glia. 2014;62:1486–1501. doi: 10.1002/glia.22695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bennett MR, Buljan V, Farnell L, Gibson WG. Purinergic junctional transmission and propagation of calcium waves in cultured spinal cord microglial networks. Purinergic Signal. 2008;4:47–59. doi: 10.1007/s11302-007-9076-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Birder LA, Barrick SR, Roppolo JR, Kanai AJ, de Groat WC, Kiss S, Buffington CA. Feline interstitial cystitis results in mechanical hypersensitivity and altered ATP release from bladder urothelium. Am J Physiol Renal Physiol. 2003;285:F423–F429. doi: 10.1152/ajprenal.00056.2003. [DOI] [PubMed] [Google Scholar]
  6. Blum AE, Walsh BC, Dubyak GR. Extracellular osmolarity modulates G protein-coupled receptor-dependent ATP release from 1321N1 astrocytoma cells. Am J Physiol Cell Physiol. 2010;298:C386–C396. doi: 10.1152/ajpcell.00430.2009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bodin P, Burnstock G. Purinergic signalling: ATP release. Neurochem Res. 2001;26:959–969. doi: 10.1023/a:1012388618693. [DOI] [PubMed] [Google Scholar]
  8. Bodin P, Bailey DJ, Burnstock G. Increased flow-induced ATP release from isolated vascular endothelial cells but not smooth muscle cells. Br J Pharmacol. 1991;103:1203–1205. doi: 10.1111/j.1476-5381.1991.tb12324.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Boitano S, Sanderson MJ, Dirksen ER. A role for Ca2+-conducting ion channels in mechanically-induced signal transduction of airway epithelial cells. J Cell Sci. 1994;107:3037–3044. doi: 10.1242/jcs.107.11.3037. [DOI] [PubMed] [Google Scholar]
  10. Boudreault F, Grygorczyk R. Cell swelling-induced ATP release and gadolinium-sensitive channels. Am J Physiol Cell Physiol. 2002;282:C219–C226. doi: 10.1152/ajpcell.00317.2001. [DOI] [PubMed] [Google Scholar]
  11. Boudreault F, Grygorczyk R. Cell swelling-induced ATP release is tightly dependent on intracellular calcium elevations. J Physiol. 2004;561:499–513. doi: 10.1113/jphysiol.2004.072306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Brückner E, Grosche A, Pannicke T, Wiedemann P, Reichenbach A, Bringmann A. Mechanisms of VEGF- and glutamate-induced inhibition of osmotic swelling of murine retinal glial (Müller) cells: indications for the involvement of vesicular glutamate release and connexin-mediated ATP release. Neurochem Res. 2012;37:268–278. doi: 10.1007/s11064-011-0606-z. [DOI] [PubMed] [Google Scholar]
  13. Burnstock G. A basis for distinguishing two types of purinergic receptor. In: Straub RW, Bolis L, editors. Cell membrane receptors for drugs and hormones: a multidisciplinary approach. New York: Raven; 1978. pp. 107–118. [Google Scholar]
  14. Burnstock G. Purine and pyrimidine receptors. Cell Mol Life Sci. 2007;64:1471–1483. doi: 10.1007/s00018-007-6497-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Burnstock G, Knight GE. Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol. 2004;240:31–304. doi: 10.1016/S0074-7696(04)40002-3. [DOI] [PubMed] [Google Scholar]
  16. Burnstock G, Ralevic V. Purinergic signalling and blood vessels in health and disease. Pharmacol Rev. 2014;66:102–192. doi: 10.1124/pr.113.008029. [DOI] [PubMed] [Google Scholar]
  17. Burow P, Klapperstück M, Markwardt F. Activation of ATP secretion via volume-regulated anion channels by sphingosine-1-phosphate in RAW macrophages. Pflugers Arch. 2015;467:1215–1226. doi: 10.1007/s00424-014-1561-8. [DOI] [PubMed] [Google Scholar]
  18. Burrell HE, Wlodarski B, Foster BJ, Buckley KA, Sharpe GR, Quayle JM, Simpson AW, Gallagher JA. Human keratinocytes release ATP and utilize three mechanisms for nucleotide interconversion at the cell surface. J Biol Chem. 2005;280:29667–29676. doi: 10.1074/jbc.M505381200. [DOI] [PubMed] [Google Scholar]
  19. Cardoso AM, Schetinger MRC, Correia-de-Sá P, Sévigny J. Impact of ectonucleotidases in autonomic nervous functions. Auton Neurosci. 2015;191:25–38. doi: 10.1016/j.autneu.2015.04.014. [DOI] [PubMed] [Google Scholar]
  20. Chamley JH, Campbell GR, Burnstock G. Dedifferentiation, redifferentiation and bundle formation of smooth muscle cells in tissue culture: the influence of cell number and nerve fibres. J Embryol Exp Cell Morphol. 1974;32:297–323. [PubMed] [Google Scholar]
  21. Charles AC, Merrill JE, Dirksen ER, Sanderson MJ. Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron. 1991;6:983–992. doi: 10.1016/0896-6273(91)90238-u. [DOI] [PubMed] [Google Scholar]
  22. Charles AC, Naus CC, Zhu D, Kidder GM, Dirksen ER, Sanderson MJ. Intercellular calcium signaling via gap junctions in glioma cells. J Cell Biol. 1992;118:195–201. doi: 10.1083/jcb.118.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Charles AC, Dirksen ER, Merrill JE, Sanderson MJ. Mechanisms of intercellular calcium signaling in glial cells studied with dantrolene and thapsigargin. Glia. 1993;7:134–145. doi: 10.1002/glia.440070203. [DOI] [PubMed] [Google Scholar]
  24. Chaudry IH. Does ATP cross the cell plasma membrane. Yale J Biol Med. 1982;55:1–10. [PMC free article] [PubMed] [Google Scholar]
  25. Chen Y, Shukla A, Namiki S, Insel PA, Junger WG. A putative osmoreceptor system that controls neutrophil function through the release of ATP, its conversion to adenosine, and activation of A2 adenosine and P2 receptors. J Leukoc Biol. 2004;76:245–253. doi: 10.1189/jlb.0204066. [DOI] [PubMed] [Google Scholar]
  26. Chen Y, Bao Y, Zhang J, Woehrle T, Sumi Y, Ledderose S, Li X, Ledderose C, Junger WG. Inhibition of neutrophils by hypertonic saline involves pannexin-1, CD39, CD73, and other sctonucleotidases. Shock. 2015;44:221–227. doi: 10.1097/SHK.0000000000000402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Corriden R, Insel PA. Basal release of ATP: an autocrine-paracrine mechanism for cell regulation. Sci Signal. 2010;3:re1. doi: 10.1126/scisignal.3104re1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Corriden R, Insel PA, Junger WG. A novel method using fluorescence microscopy for real-time assessment of ATP release from individual cells. Am J Physiol Cell Physiol. 2007;293:C1420–C1425. doi: 10.1152/ajpcell.00271.2007. [DOI] [PubMed] [Google Scholar]
  29. Dahl G. ATP release through pannexon channels. Philos Trans R Soc Lond B. 2015;370:20140191. doi: 10.1098/rstb.2014.0191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Dale N, Frenguelli BG. Measurement of purine release with microelectrode biosensors. Purinergic Signal. 2012;8:27–40. doi: 10.1007/s11302-011-9273-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. D’Andrea P, Vittur F. Ca2+ oscillations and intercellular Ca2+ waves in ATP-stimulated articular chondrocytes. J Bone Miner Res. 1996;11:946–954. doi: 10.1002/jbmr.5650110711. [DOI] [PubMed] [Google Scholar]
  32. Darby M, Kuzmiski JB, Panenka W, Feighan D, MacVicar BA. ATP released from astrocytes during swelling activates chloride channels. J Neurophysiol. 2003;89:1870–1877. doi: 10.1152/jn.00510.2002. [DOI] [PubMed] [Google Scholar]
  33. Demer LL, Wortham CM, Dirksen ER, Sanderson MJ. Mechanical stimulation induces intercellular calcium signaling in bovine aortic endothelial cells. Am J Physiol. 1993;264:H2094–H2102. doi: 10.1152/ajpheart.1993.264.6.H2094. [DOI] [PubMed] [Google Scholar]
  34. Denda M, Denda S. Air-exposed keratinocytes exhibited intracellular calcium oscillation. Skin Res Technol. 2007;13:195–201. doi: 10.1111/j.1600-0846.2007.00210.x. [DOI] [PubMed] [Google Scholar]
  35. Dezaki K, Tsumura T, Maeno E, Okada Y. Receptor-mediated facilitation of cell volume regulation by swelling-induced ATP release in human epithelial cells. Jpn J Physiol. 2000;50:235–241. doi: 10.2170/jjphysiol.50.235. [DOI] [PubMed] [Google Scholar]
  36. Dolovcak S, Waldrop SL, Xiao F, Kilic G. Evidence for sustained ATP release from liver cells that is not mediated by vesicular exocytosis. Purinergic Signal. 2011;7:435–446. doi: 10.1007/s11302-011-9240-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Dubyak GR. ATP release mechanisms. In: Burnstock G, Arnett TR, editors. Nucleotides and regulation of bone cell function. Boca Raton: Taylor & Francis; 2007. pp. 99–158. [Google Scholar]
  38. Dutta AK, Sabirov RZ, Uramoto H, Okada Y. Role of ATP-conductive anion channel in ATP release from neonatal rat cardiomyocytes in ischaemic or hypoxic conditions. J Physiol. 2004;559:799–812. doi: 10.1113/jphysiol.2004.069245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Dutta AK, Korchev YE, Shevchuk AI, Hayashi S, Okada Y, Sabirov RZ. Spatial distribution of maxi-anion channel on cardiomyocytes detected by smart-patch technique. Biophys J. 2008;94:1646–1655. doi: 10.1529/biophysj.107.117820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Eldred JA, Sanderson J, Wormstone M, Reddan JR, Duncan G. Stress-induced ATP release from and growth modulation of human lens and retinal pigment epithelial cells. Biochem Soc Trans. 2003;31:1213–1215. doi: 10.1042/bst0311213. [DOI] [PubMed] [Google Scholar]
  41. Espelt MV, de Tezanos PF, Alvarez CL, Alberti GS, Incicco J, Leal Denis MF, Davio C, Schwarzbaum PJ. On the role of ATP release, ectoATPase activity, and extracellular ADP in the regulatory volume decrease of Huh-7 human hepatoma cells. Am J Physiol Cell Physiol. 2013;304:C1013–C1026. doi: 10.1152/ajpcell.00254.2012. [DOI] [PubMed] [Google Scholar]
  42. Feranchak AP, Lewis MA, Kresge C, Sathe M, Bugde A, Luby-Phelps K, Antich PP, Fitz JG. Initiation of purinergic signaling by exocytosis of ATP-containing vesicles in liver epithelium. J Biol Chem. 2010;285:8138–8147. doi: 10.1074/jbc.M109.065482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Filtz TM, Li Q, Boyer JL, Nicholas RA, Harden TK. Expression of a cloned P2Y purinergic receptor that couples to phospholipase C. Mol Pharmacol. 1994;46:8–14. [PubMed] [Google Scholar]
  44. Forrester T. A quantitative estimation of adenosine triphosphate released from human forearm muscle during sustained exercise. J Physiol. 1972;221:25P–26P. [PubMed] [Google Scholar]
  45. Frame MK, de Feijter AW. Propagation of mechanically induced intercellular calcium waves via gap junctions and ATP receptors in rat liver epithelial cells. Exp Cell Res. 1997;230:197–207. doi: 10.1006/excr.1996.3409. [DOI] [PubMed] [Google Scholar]
  46. Furuya K, Sokabe M, Furuya S. Characteristics of subepithelial fibroblasts as a mechano-sensor in the intestine: cell-shape-dependent ATP release and P2Y1 signaling. J Cell Sci. 2005;118:3289–3304. doi: 10.1242/jcs.02453. [DOI] [PubMed] [Google Scholar]
  47. Furuya K, Sokabe M, Grygorczyk R. Real-time luminescence imaging of cellular ATP release. Methods. 2014;66:330–344. doi: 10.1016/j.ymeth.2013.08.007. [DOI] [PubMed] [Google Scholar]
  48. Gallagher CJ, Salter MW. Differential properties of astrocyte calcium waves mediated by P2Y1 and P2Y2 receptors. J Neurosci. 2003;23:6728–6739. doi: 10.1523/JNEUROSCI.23-17-06728.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Gardinier JD, Gangadharan V, Wang L, Duncan RL. Hydraulic pressure during fluid flow regulates purinergic signaling and cytoskeleton organization of osteoblasts. Cell Mol Bioeng. 2014;7:266–277. doi: 10.1007/s12195-014-0329-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Gatof D, Kilic G, Fitz JG. Vesicular exocytosis contributes to volume-sensitive ATP release in biliary cells. Am J Physiol Gastrointest Liver Physiol. 2004;286:G538–G546. doi: 10.1152/ajpgi.00355.2003. [DOI] [PubMed] [Google Scholar]
  51. Genetos DC, Geist DJ, Liu D, Donahue HJ, Duncan RL. Fluid shear-induced ATP secretion mediates prostaglandin release in MC3T3-E1 osteoblasts. J Bone Miner Res. 2005;20:41–49. doi: 10.1359/JBMR.041009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Genetos DC, Kephart CJ, Zhang Y, Yellowley CE, Donahue HJ. Oscillating fluid flow activation of gap junction hemichannels induces ATP release from MLO-Y4 osteocytes. J Cell Physiol. 2007;212:207–214. doi: 10.1002/jcp.21021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Gheorghiu M, Van Driessche W. Modeling of basolateral ATP release induced by hypotonic treatment in A6 cells. Eur Biophys J. 2004;33:412–420. doi: 10.1007/s00249-003-0375-y. [DOI] [PubMed] [Google Scholar]
  54. Gomes P, Srinivas SP, Van DW, Vereecke J, Himpens B. ATP release through connexin hemichannels in corneal endothelial cells. Invest Ophthalmol Vis Sci. 2005;46:1208–1218. doi: 10.1167/iovs.04-1181. [DOI] [PubMed] [Google Scholar]
  55. Graff RD, Lazarowski ER, Banes AJ, Lee GM. ATP release by mechanically loaded porcine chondrons in pellet culture. Arthritis Rheum. 2000;43:1571–1579. doi: 10.1002/1529-0131(200007)43:7<1571::AID-ANR22>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
  56. Grierson JP, Meldolesi J. Shear stress-induced [Ca2+]i transients and oscillations in mouse fibroblasts are mediated by endogenously released ATP. J Biol Chem. 1995;270:4451–4456. doi: 10.1074/jbc.270.9.4451. [DOI] [PubMed] [Google Scholar]
  57. Grygorczyk R, Guyot A. Osmotic swelling-induced ATP release: a new role for tyrosine and Rho-kinases? J Physiol. 2001;532:582. doi: 10.1111/j.1469-7793.2001.0582e.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Grygorczyk R, Furuya K, Sokabe M. Imaging and characterization of stretch-induced ATP release from alveolar A549 cells. J Physiol. 2013;591:1195–1215. doi: 10.1113/jphysiol.2012.244145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Guthrie PB, Knappenberger J, Segal M, Bennett MV, Charles AC, Kater SB. ATP released from astrocytes mediates glial calcium waves. J Neurosci. 1999;19:520–528. doi: 10.1523/JNEUROSCI.19-02-00520.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Guyot A, Hanrahan JW. ATP release from human airway epithelial cells studied using a capillary cell culture system. J Physiol. 2002;545:199–206. doi: 10.1113/jphysiol.2002.030148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Haanes KA, Kowal JM, Arpino G, Lange SC, Moriyama Y, Pedersen PA, Novak I. Role of vesicular nucleotide transporter VNUT (SLC17A9) in release of ATP from AR42J cells and mouse pancreatic acinar cells. Purinergic Signal. 2014;10:431–440. doi: 10.1007/s11302-014-9406-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Hamada K, Takuwa N, Yokoyama K, Takuwa Y. Stretch activates Jun N-terminal kinase/stress-activated protein kinase in vascular smooth muscle cells through mechanisms involving autocrine ATP stimulation of purinoceptors. J Biol Chem. 1998;273:6334–6340. doi: 10.1074/jbc.273.11.6334. [DOI] [PubMed] [Google Scholar]
  63. Hamill OP, Martinac B. Molecular basis of mechanotransduction in living cells. Physiol Rev. 2001;81:685–740. doi: 10.1152/physrev.2001.81.2.685. [DOI] [PubMed] [Google Scholar]
  64. Hansen M, Boitano S, Dirksen ER, Sanderson MJ. Intercellular calcium signaling induced by extracellular adenosine 5′-triphosphate and mechanical stimulation in airway epithelial cells. J Cell Sci. 1993;106:995–1004. doi: 10.1242/jcs.106.4.995. [DOI] [PubMed] [Google Scholar]
  65. Hazama A, Fan HT, Abdullaev I, Maeno E, Tanaka S, Ando AY, Okada Y. Swelling-activated, cystic fibrosis transmembrane conductance regulator-augmented ATP release and Cl− conductances in murine C127 cells. J Physiol. 2000;523:1–11. doi: 10.1111/j.1469-7793.2000.t01-6-00001.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Hecht E, Liedert A, Ignatius A, Mizaikoff B, Kranz C. Local detection of mechanically induced ATP release from bone cells with ATP microbiosensors. Biosens Bioelectron. 2013;44:27–33. doi: 10.1016/j.bios.2013.01.008. [DOI] [PubMed] [Google Scholar]
  67. Hisadome K, Koyama T, Kimura C, Droogmans G, Ito Y, Oike M. Volume-regulated anion channels serve as an auto/paracrine nucleotide release pathway in aortic endothelial cells. J Gen Physiol. 2002;119:511–520. doi: 10.1085/jgp.20028540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Homolya L, Steinberg TH, Boucher RC. Cell to cell communication in response to mechanical stress via bilateral release of ATP and UTP in polarized epithelia. J Cell Biol. 2000;150:1349–1360. doi: 10.1083/jcb.150.6.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Hovater MB, Olteanu D, Hanson EL, Cheng NL, Siroky B, Fintha A, Komlosi P, Liu W, Satlin LM, Bell PD, Yoder BK, Schwiebert EM. Loss of apical monocilia on collecting duct principal cells impairs ATP secretion across the apical cell surface and ATP-dependent and flow-induced calcium signals. Purinergic Signal. 2008;4:155–170. doi: 10.1007/s11302-007-9072-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Islam M, Uramoto H, Okada T, Sabirov RZ, Okada Y. Maxi-anion channel and pannexin 1 hemichannel constitute separate pathways for swelling-induced ATP release in murine L929 fibrosarcoma cells. Am J Physiol Cell Physiol. 2012;303:C924–C935. doi: 10.1152/ajpcell.00459.2011. [DOI] [PubMed] [Google Scholar]
  71. Ito M, Arakawa T, Okayama M, Shitara A, Mizoguchi I, Takuma T. Gravity loading induces adenosine triphosphate release and phosphorylation of extracellular signal-regulated kinases in human periodontal ligament cells. J Investig Clin Dent. 2014;5:266–274. doi: 10.1111/jicd.12049. [DOI] [PubMed] [Google Scholar]
  72. Jans D, Srinivas SP, Waelkens E, Segal A, Lariviere E, Simaels J, Van Driessche W. Hypotonic treatment evokes biphasic ATP release across the basolateral membrane of cultured renal epithelia (A6) J Physiol. 2002;545:543–555. doi: 10.1113/jphysiol.2002.026641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Joseph SM, Buchakjian MR, Dubyak GR. Colocalization of ATP release sites and ecto-ATPase activity at the extracellular surface of human astrocytes. J Biol Chem. 2003;278:23331–23342. doi: 10.1074/jbc.M302680200. [DOI] [PubMed] [Google Scholar]
  74. Kawakami M, Nagira T, Hayashi T, Shimamoto C, Kubota T, Mori H, Yoshida H, Nakahari T. Hypo-osmotic potentiation of acetylcholine-stimulated ciliary beat frequency through ATP release in rat tracheal ciliary cells. Exp Physiol. 2004;89:739–751. doi: 10.1113/expphysiol.2004.028670. [DOI] [PubMed] [Google Scholar]
  75. Khlyntseva SV, Bazel YR, Vishnikin AB, Andruch V. Methods for the determination of adenosine triphosphate and other adenine nucleotides. J Anal Chem. 2009;64:657–673. [Google Scholar]
  76. Kim JC, Woo SH. Shear stress induces a longitudinal Ca2+ wave via autocrine activation of P2Y 1 purinergic signalling in rat atrial myocytes. J Physiol. 2015;593:5091–5109. doi: 10.1113/JP271016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Koizumi S, Fujishita K, Inoue K, Shigemoto-Mogami Y, Tsuda M, Inoue K. Ca2+ waves in keratinocytes are transmitted to sensory neurons: the involvement of extracellular ATP and P2Y2 receptor activation. Biochem J. 2004;380:329–338. doi: 10.1042/BJ20031089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Kono T, Nishikori T, Kataoka H, Uchio Y, Ochi M, Enomoto K. Spontaneous oscillation and mechanically induced calcium waves in chondrocytes. Cell Biochem Funct. 2006;24:103–111. doi: 10.1002/cbf.1304. [DOI] [PubMed] [Google Scholar]
  79. Kowal JM, Yegutkin GG, Novak I. ATP release, generation and hydrolysis in exocrine pancreatic duct cells. Purinergic Signal. 2015;11:533–550. doi: 10.1007/s11302-015-9472-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Kringelbach TM, Aslan D, Novak I, Ellegaard M, Syberg S, Andersen CKB, Kristiansen KA, Vang O, Schwarz P, Jørgensen NR. Fine-tuned ATP signals are acute mediators in osteocyte mechanotransduction. Cell Signal. 2015;27:2401–2409. doi: 10.1016/j.cellsig.2015.08.016. [DOI] [PubMed] [Google Scholar]
  81. Lazarowski ER, Watt WC, Stutts MJ, Boucher RC, Harden TK. Pharmacological selectivity of the cloned human P2U-purinoceptor: potent activation by diadenosine tetraphosphate. Br J Pharmacol. 1995;116:1619–1627. doi: 10.1111/j.1476-5381.1995.tb16382.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Lazarowski ER, Sesma JI, Seminario-Vidal L, Kreda SM. Molecular mechanisms of purine and pyrimidine nucleotide release. Adv Pharmacol. 2011;61:221–261. doi: 10.1016/B978-0-12-385526-8.00008-4. [DOI] [PubMed] [Google Scholar]
  83. Lee J, Chun YE, Han KS, Lee J, Woo DH, Lee CJ. Ca2+ Entry is required for mechanical stimulation-induced ATP release from astrocyte. Exp Neurobiol. 2015;24:17–23. doi: 10.5607/en.2015.24.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Leybaert L, Sanderson MJ. Intercellular Ca2+ waves: mechanisms and function. Physiol Rev. 2012;92:1359–1392. doi: 10.1152/physrev.00029.2011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Li A, Leung CT, Peterson-Yantorno K, Mitchell CH, Civan MM. Pathways for ATP release by bovine ciliary epithelial cells, the initial step in purinergic regulation of aqueous humor inflow. Am J Physiol Cell Physiol. 2010;299:C1308–C1317. doi: 10.1152/ajpcell.00333.2010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Li A, Banerjee J, Leung CT, Peterson-Yantorno K, Stamer WD, Civan MM. Mechanisms of ATP release, the enabling step in purinergic dynamics. Cell Physiol Biochem. 2011;28:1135–1144. doi: 10.1159/000335865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Li A, Leung CT, Peterson-Yantorno K, Stamer WD, Mitchell CH, Civan MM. Mechanisms of ATP release by human trabecular meshwork cells, the enabling step in purinergic regulation of aqueous humor outflow. J Cell Physiol. 2012;227:172–182. doi: 10.1002/jcp.22715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Li LF, Xiang C, Qin KR. Modeling of TRPV4-C1-mediated calcium signaling in vascular endothelial cells induced by fluid shear stress and ATP. Biomech Model Mechanobiol. 2015;14:979–993. doi: 10.1007/s10237-015-0647-3. [DOI] [PubMed] [Google Scholar]
  89. Liu HT, Toychiev AH, Takahashi N, Sabirov RZ, Okada Y. Maxi-anion channel as a candidate pathway for osmosensitive ATP release from mouse astrocytes in primary culture. Cell Res. 2008;18:558–565. doi: 10.1038/cr.2008.49. [DOI] [PubMed] [Google Scholar]
  90. Locovei S, Bao L, Dahl G. Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci U S A. 2006;103:7655–7659. doi: 10.1073/pnas.0601037103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Lohman AW, Isakson BE. Differentiating connexin hemichannels and pannexin channels in cellular ATP release. FEBS Lett. 2014;588:1379–1388. doi: 10.1016/j.febslet.2014.02.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Loomis WH, Namiki S, Ostrom RS, Insel PA, Junger WG. Hypertonic stress increases T cell interleukin-2 expression through a mechanism that involves ATP release, P2 receptor, and p38 MAPK activation. J Biol Chem. 2003;278:4590–4596. doi: 10.1074/jbc.M207868200. [DOI] [PubMed] [Google Scholar]
  93. Lu D, Soleymani S, Madakshire R, Insel PA. ATP released from cardiac fibroblasts via connexin hemichannels activates profibrotic P2Y2 receptors. FASEB J. 2012;26:2580–2591. doi: 10.1096/fj.12-204677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Luckprom P, Wongkhantee S, Yongchaitrakul T, Pavasant P. Adenosine triphosphate stimulates RANKL expression through P2Y1 receptor-cyclo-oxygenase-dependent pathway in human periodontal ligament cells. J Periodontal Res. 2010;45:404–411. doi: 10.1111/j.1600-0765.2009.01256.x. [DOI] [PubMed] [Google Scholar]
  95. Luckprom P, Kanjanamekanant K, Pavasant P. Role of connexin43 hemichannels in mechanical stress-induced ATP release in human periodontal ligament cells. J Periodontal Res. 2011;46:607–615. doi: 10.1111/j.1600-0765.2011.01379.x. [DOI] [PubMed] [Google Scholar]
  96. Luna C, Li G, Qiu J, Challa P, Epstein DL, Gonzalez P. Extracellular release of ATP mediated by cyclic mechanical stress leads to mobilization of AA in trabecular meshwork cells. Invest Ophthalmol Vis Sci. 2009;50:5805–5810. doi: 10.1167/iovs.09-3796. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Ma HP, Li L, Zhou ZH, Eaton DC, Warnock DG. ATP masks stretch activation of epithelial sodium channels in A6 distal nephron cells. Am J Physiol Renal Physiol. 2002;282:F501–F505. doi: 10.1152/ajprenal.00147.2001. [DOI] [PubMed] [Google Scholar]
  98. Mansfield KJ, Hughes JR. P2Y receptor modulation of ATP release in the urothelium. Biomed Res Int. 2014;2014:830374. doi: 10.1155/2014/830374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. McLatchie LM, Fry CH. ATP release from freshly isolated guinea-pig bladder urothelial cells: a quantification and study of the mechanisms involved. BJU Int. 2015;115:987–993. doi: 10.1111/bju.12954. [DOI] [PubMed] [Google Scholar]
  100. Mills DC, Robb IA, Roberts GC. The release of nucleotides, 5-hydroxytryptamine and enzymes from human blood platelets during aggregation. J Physiol. 1968;195:715–729. doi: 10.1113/jphysiol.1968.sp008484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Millward-Sadler SJ, Wright MO, Flatman PW, Salter DM. ATP in the mechanotransduction pathway of normal human chondrocytes. Biorheology. 2004;41:567–575. [PubMed] [Google Scholar]
  102. Milner P, Bodin P, Loesch A, Burnstock G. Rapid release of endothelin and ATP from isolated aortic endothelial cells exposed to increased flow. Biochem Biophys Res Commun. 1990;170:649–656. doi: 10.1016/0006-291x(90)92141-l. [DOI] [PubMed] [Google Scholar]
  103. Milner P, Bodin P, Loesch A, Burnstock G. Increased shear stress leads to differential release of endothelin and ATP from isolated endothelial cells from 4- and 12-month-old male rabbit aorta. J Vasc Res. 1992;29:420–425. doi: 10.1159/000158960. [DOI] [PubMed] [Google Scholar]
  104. Mitchell CH. Release of ATP by a human retinal pigment epithelial cell line: potential for autocrine stimulation through subretinal space. J Physiol. 2001;534:193–202. doi: 10.1111/j.1469-7793.2001.00193.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. Mitchell CH, Carre DA, McGlinn AM, Stone RA, Civan MM. A release mechanism for stored ATP in ocular ciliary epithelial cells. Proc Natl Acad Sci U S A. 1998;95:7174–7178. doi: 10.1073/pnas.95.12.7174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Murata N, Ito S, Furuya K, Takahara N, Naruse K, Aso H, Kondo M, Sokabe M, Hasegawa Y. Ca2+ influx and ATP release mediated by mechanical stretch in human lung fibroblasts. Biochem Biophys Res Commun. 2014;453:101–105. doi: 10.1016/j.bbrc.2014.09.063. [DOI] [PubMed] [Google Scholar]
  107. Nandigama R, Padmasekar M, Wartenberg M, Sauer H. Feed forward cycle of hypotonic stress-induced ATP release, purinergic receptor activation, and growth stimulation of prostate cancer cells. J Biol Chem. 2006;281:5686–5693. doi: 10.1074/jbc.M510452200. [DOI] [PubMed] [Google Scholar]
  108. Newman EA. Calcium signaling in retinal glial cells and its effect on neuronal activity. Prog Brain Res. 2001;132:241–254. doi: 10.1016/S0079-6123(01)32080-0. [DOI] [PubMed] [Google Scholar]
  109. Novak I. ATP as a signaling molecule: the exocrine focus. News Physiol Sci. 2003;18:12–17. doi: 10.1152/nips.01409.2002. [DOI] [PubMed] [Google Scholar]
  110. Oike M, Kimura C, Koyama T, Yoshikawa M, Ito Y. Hypotonic stress-induced dual Ca2+ responses in bovine aortic endothelial cells. Am J Physiol Heart Circ Physiol. 2000;279:H630–H638. doi: 10.1152/ajpheart.2000.279.2.H630. [DOI] [PubMed] [Google Scholar]
  111. Oishi S, Sasano T, Tateishi Y, Tamura N, Isobe M, Furukawa T. Stretch of atrial myocytes stimulates recruitment of macrophages via ATP released through gap-junction channels. J Pharmacol Sci. 2012;120:296–304. doi: 10.1254/jphs.12202fp. [DOI] [PubMed] [Google Scholar]
  112. Okada SF, Nicholas RA, Kreda SM, Lazarowski ER, Boucher RC. Physiological regulation of ATP release at the apical surface of human airway epithelia. J Biol Chem. 2006;281:22992–23002. doi: 10.1074/jbc.M603019200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. Orriss IR, Key ML, Hajjawi MO, Arnett TR. Extracellular ATP released by osteoblasts is a key local inhibitor of bone mineralisation. PLoS ONE. 2013;8:e69057. doi: 10.1371/journal.pone.0069057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Osipchuk Y, Cahalan M. Cell-to-cell spread of calcium signals mediated by ATP receptors in mast cells. Nature. 1992;359:241–244. doi: 10.1038/359241a0. [DOI] [PubMed] [Google Scholar]
  115. Pafundo DE, Chara O, Faillace MP, Krumschnabel G, Schwarzbaum PJ. Kinetics of ATP release and cell volume regulation of hyposmotically challenged goldfish hepatocytes. Am J Phys Regul Integr Comp Phys. 2008;294:R220–R233. doi: 10.1152/ajpregu.00522.2007. [DOI] [PubMed] [Google Scholar]
  116. Parr CE, Sullivan DM, Paradiso AM, Lazarowski ER, Burch LH, Olsen JC, Erb L, Weisman GA, Boucher RC, Turner JT. Cloning and expression of a human P2U nucleotide receptor, a target for cystic fibrosis pharmacotherapy. Proc Natl Acad Sci U S A. 1994;91:3275–3279. doi: 10.1073/pnas.91.8.3275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Pearson RA, Dale N, Llaudet E, Mobbs P. ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron. 2005;46:731–744. doi: 10.1016/j.neuron.2005.04.024. [DOI] [PubMed] [Google Scholar]
  118. Pedersen S, Pedersen SF, Nilius B, Lambert IH, Hoffmann EK. Mechanical stress induces release of ATP from Ehrlich ascites tumor cells. Biochim Biophys Acta. 1999;1416:271–284. doi: 10.1016/s0005-2736(98)00228-4. [DOI] [PubMed] [Google Scholar]
  119. Pellegatti P, Falzoni S, Pinton P, Rizzuto R, Di VF. A novel recombinant plasma membrane-targeted luciferase reveals a new pathway for ATP secretion. Mol Biol Cell. 2005;16:3659–3665. doi: 10.1091/mbc.E05-03-0222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Praetorius HA, Leipziger J. ATP release from non-excitable cells. Purinergic Signal. 2009;5:433–446. doi: 10.1007/s11302-009-9146-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Praetorius HA, Leipziger J. Intrarenal purinergic signaling in the control of renal tubular transport. Annu Rev Physiol. 2010;72:377–393. doi: 10.1146/annurev-physiol-021909-135825. [DOI] [PubMed] [Google Scholar]
  122. Praetorius HA, Frøkiaer J, Leipziger J. Transepithelial pressure pulses induce nucleotide release in polarized MDCK cells. Am J Physiol Renal Physiol. 2005;288:F133–F141. doi: 10.1152/ajprenal.00238.2004. [DOI] [PubMed] [Google Scholar]
  123. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev. 1998;50:413–492. [PubMed] [Google Scholar]
  124. Ramsingh R, Grygorczyk A, Solecki A, Cherkaoui LS, Berthiaume Y, Grygorczyk R. Cell deformation at the air-liquid interface induces Ca2+-dependent ATP release from lung epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2011;300:L587–L595. doi: 10.1152/ajplung.00345.2010. [DOI] [PubMed] [Google Scholar]
  125. Ransford GA, Fregien N, Qiu F, Dahl G, Conner GE, Salathe M. Pannexin 1 contributes to ATP release in airway epithelia. Am J Respir Cell Mol Biol. 2009;41:525–534. doi: 10.1165/rcmb.2008-0367OC. [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. Reigada D, Mitchell CH. Release of ATP from retinal pigment epithelial cells involves both CFTR and vesicular transport. Am J Physiol Cell Physiol. 2005;288:C132–C140. doi: 10.1152/ajpcell.00201.2004. [DOI] [PubMed] [Google Scholar]
  127. Riddle RC, Taylor AF, Rogers JR, Donahue HJ. ATP release mediates fluid flow-induced proliferation of human bone marrow stromal cells. J Bone Miner Res. 2007;22:589–600. doi: 10.1359/jbmr.070113. [DOI] [PubMed] [Google Scholar]
  128. Rodat-Despoix L, Hao J, Dandonneau M, Delmas P. Shear stress-induced Ca2+ mobilization in MDCK cells is ATP dependent, no matter the primary cilium. Cell Calcium. 2013;53:327–337. doi: 10.1016/j.ceca.2013.02.002. [DOI] [PubMed] [Google Scholar]
  129. Roman RM, Feranchak AP, Salter KD, Wang Y, Fitz JG. Endogenous ATP release regulates Cl− secretion in cultured human and rat biliary epithelial cells. Am J Physiol. 1999;276:G1391–G1400. doi: 10.1152/ajpgi.1999.276.6.G1391. [DOI] [PubMed] [Google Scholar]
  130. Romanello M, Pani B, Bicego M, D’Andrea P. Mechanically induced ATP release from human osteoblastic cells. Biochem Biophys Res Commun. 2001;289:1275–1281. doi: 10.1006/bbrc.2001.6124. [DOI] [PubMed] [Google Scholar]
  131. Romanello M, Codognotto A, Bicego M, Pines A, Tell G, D’Andrea P. Autocrine/paracrine stimulation of purinergic receptors in osteoblasts: contribution of vesicular ATP release. Biochem Biophys Res Commun. 2005;331:1429–1438. doi: 10.1016/j.bbrc.2005.03.246. [DOI] [PubMed] [Google Scholar]
  132. Rosenthal AK, Gohr CM, Mitton-Fitzgerald E, Lutz MK, Dubyak GR, Ryan LM. The progressive ankylosis gene product ANK regulates extracellular ATP levels in primary articular chondrocytes. Arthritis Res Ther. 2013;15:R154. doi: 10.1186/ar4337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  133. Rumney RM, Sunters A, Reilly GC, Gartland A. Application of multiple forms of mechanical loading to human osteoblasts reveals increased ATP release in response to fluid flow in 3D cultures and differential regulation of immediate early genes. J Biomech. 2012;45:549–554. doi: 10.1016/j.jbiomech.2011.11.036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Ryu SY, Peixoto PM, Won JH, Yule DI, Kinnally KW. Extracellular ATP and P2Y2 receptors mediate intercellular Ca2+ waves induced by mechanical stimulation in submandibular gland cells: role of mitochondrial regulation of store operated Ca2+ entry. Cell Calcium. 2010;47:65–76. doi: 10.1016/j.ceca.2009.11.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  135. Sabirov R, Okada Y. ATP release via anion channels. Purinergic Signal. 2005;1:311–328. doi: 10.1007/s11302-005-1557-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. Sabirov RZ, Dutta AK, Okada Y. Volume-dependent ATP-conductive large-conductance anion channel as a pathway for swelling-induced ATP release. J Gen Physiol. 2001;118:251–266. doi: 10.1085/jgp.118.3.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Sakowicz-Burkiewicz M, Kocbuch K, Grden M, Szutowicz A, Pawelczyk T. Adenosine 5′-triphosphate is the predominant source of peripheral adenosine in human B lymphoblasts. J Physiol Pharmacol. 2010;61:491–499. [PubMed] [Google Scholar]
  138. Sanderson MJ, Charles AC, Dirksen ER. Mechanical stimulation and intercellular communication increases intracellular Ca2+ in epithelial cells. Cell Regul. 1990;1:585–596. doi: 10.1091/mbc.1.8.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  139. Sathe MN, Woo K, Kresge C, Bugde A, Luby-Phelps K, Lewis MA, Feranchak AP. Regulation of purinergic signaling in biliary epithelial cells by exocytosis of SLC17A9-dependent ATP-enriched vesicles. J Biol Chem. 2011;286:25363–25376. doi: 10.1074/jbc.M111.232868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  140. Sauer H, Hescheler J, Wartenberg M. Mechanical strain-induced Ca2+ waves are propagated via ATP release and purinergic receptor activation. Am J Physiol Cell Physiol. 2000;279:C295–C307. doi: 10.1152/ajpcell.2000.279.2.C295. [DOI] [PubMed] [Google Scholar]
  141. Sawada K, Echigo N, Juge N, Miyaji T, Otsuka M, Omote H, Yamamoto A, Moriyama Y. Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci U S A. 2008;105:5683–5686. doi: 10.1073/pnas.0800141105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Scemes E, Spray DC, Meda P. Connexins, pannexins, innexins: novel roles of “hemi-channels”. Pflugers Arch. 2009;457:1207–1226. doi: 10.1007/s00424-008-0591-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. Seminario-Vidal L, Okada SF, Sesma JI, Kreda SM, van Heusden CA, Zhu Y, Jones LC, O’Neal WK, Penuela S, Laird DW, Boucher RC, Lazarowski ER. Rho signaling regulates pannexin 1-mediated ATP release from airway epithelia. J Biol Chem. 2011;286:26277–26286. doi: 10.1074/jbc.M111.260562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  144. Shinozuka K, Tanaka N, Kawasaki K, Mizuno H, Kubota Y, Nakamura K, Hashimoto M, Kunitomo M. Participation of ATP in cell volume regulation in the endothelium after hypotonic stress. Clin Exp Pharmacol Physiol. 2001;28:799–803. doi: 10.1046/j.1440-1681.2001.03525.x. [DOI] [PubMed] [Google Scholar]
  145. Silva GB, Garvin JL. TRPV4 mediates hypotonicity-induced ATP release by the thick ascending limb. Am J Physiol Renal Physiol. 2008;295:F1090–F1095. doi: 10.1152/ajprenal.90365.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. Sperlágh B, Heinrich A, Csölle C. P2 receptor-mediated modulation of neurotransmitter release-an update. Purinergic Signal. 2007;3:269–284. doi: 10.1007/s11302-007-9080-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  147. Spray DC, Ye ZC, Ransom BR. Functional connexin “hemichannels”: a critical appraisal. Glia. 2006;54:758–773. doi: 10.1002/glia.20429. [DOI] [PubMed] [Google Scholar]
  148. Stamatakis M, Mantzaris NV. Modeling of ATP-mediated signal transduction and wave propagation in astrocytic cellular networks. J Theor Biol. 2006;241:649–668. doi: 10.1016/j.jtbi.2006.01.002. [DOI] [PubMed] [Google Scholar]
  149. Stout CE, Costantin JL, Naus CC, Charles AC. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem. 2002;277:10482–10488. doi: 10.1074/jbc.M109902200. [DOI] [PubMed] [Google Scholar]
  150. Suadicani SO, Brosnan CF, Scemes E. P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J Neurosci. 2006;26:1378–1385. doi: 10.1523/JNEUROSCI.3902-05.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  151. Sun Y, Chai TC. Effects of dimethyl sulphoxide and heparin on stretch-activated ATP release by bladder urothelial cells from patients with interstitial cystitis. BJU Int. 2002;90:381–385. doi: 10.1046/j.1464-410x.2002.02912.x. [DOI] [PubMed] [Google Scholar]
  152. Sun Y, Keay S, De Deyne PG, Chai TC. Augmented stretch activated adenosine triphosphate release from bladder uroepithelial cells in patients with interstitial cystitis. J Urol. 2001;166:1951–1956. [PubMed] [Google Scholar]
  153. Sun D, Junger WG, Yuan C, Zhang W, Bao Y, Qin D, Wang C, Tan L, Qi B, Zhu D, Zhang X, Yu T. Shockwaves induce osteogenic differentiation of human mesenchymal stem cells through ATP release and activation of P2X7 receptors. Stem Cells. 2013;31:1170–1180. doi: 10.1002/stem.1356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  154. Takahara N, Ito S, Furuya K, Naruse K, Aso H, Kondo M, Sokabe M, Hasegawa Y. Real-time imaging of ATP release induced by mechanical stretch in human airway smooth muscle cells. Am J Respir Cell Mol Biol. 2014;51:772–782. doi: 10.1165/rcmb.2014-0008OC. [DOI] [PubMed] [Google Scholar]
  155. Tatur S, Kreda S, Lazarowski E, Grygorczyk R. Calcium-dependent release of adenosine and uridine nucleotides from A549 cells. Purinergic Signal. 2008;4:139–146. doi: 10.1007/s11302-007-9059-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  156. Thompson WR, Majid AS, Czymmek KJ, Ruff AL, García J, Duncan RL, Farach-Carson MC. Association of the α2δ1 subunit with Cav3.2 enhances membrane expression and regulates mechanically induced ATP release in MLO-Y4 osteocytes. J Bone Miner Res. 2011;26:2125–2139. doi: 10.1002/jbmr.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  157. Tomassen SFB, van der Wijk T, De Jonge HR, Tilly BC. Activation of phospholipase D by osmotic cell swelling. FEBS Lett. 2004;566:287–290. doi: 10.1016/j.febslet.2004.04.063. [DOI] [PubMed] [Google Scholar]
  158. Turner JT, Weisman GA, Camden JM. Upregulation of P2Y2 nucleotide receptors in rat salivary gland cells during short-term culture. Am J Physiol. 1997;273:C1100–C1107. doi: 10.1152/ajpcell.1997.273.3.C1100. [DOI] [PubMed] [Google Scholar]
  159. van der Wijk T, Tomassen SF, Houtsmuller AB, De Jonge HR, Tilly BC. Increased vesicle recycling in response to osmotic cell swelling. Cause and consequence of hypotonicity-provoked ATP release. J Biol Chem. 2003;278:40020–40025. doi: 10.1074/jbc.M307603200. [DOI] [PubMed] [Google Scholar]
  160. Vázquez-Cuevas FG, Martínez-Ramírez AS, Robles-Martínez L, Garay E, García-Carrancá A, Pérez-Montiel D, Castañeda-García C, Arellano RO. Paracrine stimulation of P2X7 receptor by ATP activates a proliferative pathway in ovarian carcinoma cells. J Cell Biochem. 2014;115:1955–1966. doi: 10.1002/jcb.24867. [DOI] [PubMed] [Google Scholar]
  161. Voigt J, Grosche A, Vogler S, Pannicke T, Hollborn M, Kohen L, Wiedemann P, Reichenbach A, Bringmann A. Nonvesicular release of ATP from rat retinal glial (Müller) cells is differentially mediated in response to osmotic stress and glutamate. Neurochem Res. 2015;40:651–660. doi: 10.1007/s11064-014-1511-z. [DOI] [PubMed] [Google Scholar]
  162. Wang Y, Roman R, Lidofsky SD, Fitz JG. Autocrine signaling through ATP release represents a novel mechanism for cell volume regulation. Proc Natl Acad Sci U S A. 1996;93:12020–12025. doi: 10.1073/pnas.93.21.12020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  163. Wang JG, Miyazu M, Xiang P, Li SN, Sokabe M, Naruse K. Stretch-induced cell proliferation is mediated by FAK-MAPK pathway. Life Sci. 2005;76:2817–2825. doi: 10.1016/j.lfs.2004.10.050. [DOI] [PubMed] [Google Scholar]
  164. Wang L, Sikora J, Hu L, Shen X, Grygorczyk R, Schwarz W (2013) ATP release from mast cells by physical stimulation: a putative early step in activation of acupuncture points. Evid Based Complement Alternat Med 350949 [DOI] [PMC free article] [PubMed]
  165. Wang CM, Ploia C, Anselmi F, Sarukhan A, Viola A. Adenosine triphosphate acts as a paracrine signaling molecule to reduce the motility of T cells. EMBO J. 2014;33:1354–1364. doi: 10.15252/embj.201386666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  166. Watt WC, Lazarowski ER, Boucher RC. Cystic fibrosis transmembrane regulator-independent release of ATP. Its implications for the regulation of P2Y2 receptors in airway epithelia. J Biol Chem. 1998;273:14053–14058. doi: 10.1074/jbc.273.22.14053. [DOI] [PubMed] [Google Scholar]
  167. Weihs AM, Fuchs C, Teuschl AH, Hartinger J, Slezak P, Mittermayr R, Redl H, Junger WG, Sitte HH, Runzler D. Shock wave treatment enhances cell proliferation and improves wound healing by ATP release-coupled extracellular signal-regulated kinase (ERK) activation. J Biol Chem. 2014;289:27090–27104. doi: 10.1074/jbc.M114.580936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  168. Wilson PD, Hovater JS, Casey CC, Fortenberry JA, Schwiebert EM. ATP release mechanisms in primary cultures of epithelia derived from the cysts of polycystic kidneys. J Am Soc Nephrol. 1999;10:218–229. doi: 10.1681/ASN.V102218. [DOI] [PubMed] [Google Scholar]
  169. Woehrle T, Yip L, Manohar M, Sumi Y, Yao Y, Chen Y, Junger WG. Hypertonic stress regulates T cell function via pannexin-1 hemichannels and P2X receptors. J Leukoc Biol. 2010;88:1181–1189. doi: 10.1189/jlb.0410211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  170. Wongkhantee S, Yongchaitrakul T, Pavasant P. Mechanical stress induces osteopontin via ATP/P2Y1 in periodontal cells. J Dent Res. 2008;87:564–568. doi: 10.1177/154405910808700601. [DOI] [PubMed] [Google Scholar]
  171. Woo K, Dutta AK, Patel V, Kresge C, Feranchak AP. Fluid flow induces mechanosensitive ATP release, calcium signalling and Cl-transport in biliary epithelial cells through a PKCζ-dependent pathway. J Physiol. 2008;586:2779–2798. doi: 10.1113/jphysiol.2008.153015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  172. Woo K, Sathe M, Kresge C, Esser V, Ueno Y, Venter J, Glaser SS, Alpini G, Feranchak AP. Adenosine triphosphate release and purinergic (P2) receptor-mediated secretion in small and large mouse cholangiocytes. Hepatology. 2010;52:1819–1828. doi: 10.1002/hep.23883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  173. Wu D, Schaffler MB, Weinbaum S, Spray DC. Matrix-dependent adhesion mediates network responses to physiological stimulation of the osteocyte cell process. Proc Natl Acad Sci U S A. 2013;110:12096–12101. doi: 10.1073/pnas.1310003110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  174. Xia J, Lim JC, Lu W, Beckel JM, Macarak EJ, Laties AM, Mitchell CH. Neurons respond directly to mechanical deformation with pannexin-mediated ATP release and autostimulation of P2X7 receptors. J Physiol. 2012;590:2285–2304. doi: 10.1113/jphysiol.2012.227983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  175. Xiang C, Cao L, Qin K, Xu Z, Chen BM (2007) A modified dynamic model for shear stress induced ATP release from vascular endothelial cells. In: Li K, Fei M, Irwin GW, Ma S (eds) Bio-inspired computational intelligence and applications: international conference on Life System Modeling and Simulation, LSMS 2007, Shanghai, China, September 14–17, 2007. Proceedings, pp. 462–472
  176. Xing Y, Gu Y, Bresnahan JJ, Paul EM, Donahue HJ, You J (2014) The roles of P2Y2 purinergic receptors in osteoblasts and mechanotransduction. PLoS ONE 9 [DOI] [PMC free article] [PubMed]
  177. Yamamoto K, Furuya K, Nakamura M, Kobatake E, Sokabe M, Ando J. Visualization of flow-induced ATP release and triggering of Ca2+ waves at caveolae in vascular endothelial cells. J Cell Sci. 2011;124:3477–3483. doi: 10.1242/jcs.087221. [DOI] [PubMed] [Google Scholar]
  178. Yamazaki S, Weinhold PS, Graff RD, Tsuzaki M, Kawakami M, Minchew JT, Banes AJ. Annulus cells release ATP in response to vibratory loading in vitro. J Cell Biochem. 2003;90:812–818. doi: 10.1002/jcb.10681. [DOI] [PubMed] [Google Scholar]
  179. Yegutkin GG. Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim Biophys Acta. 2008;1783:673–694. doi: 10.1016/j.bbamcr.2008.01.024. [DOI] [PubMed] [Google Scholar]
  180. Yip L, Cheung CW, Corriden R, Chen Y, Insel PA, Junger WG. Hypertonic stress regulates T-cell function by the opposing actions of extracellular adenosine triphosphate and adenosine. Shock. 2007;27:242–250. doi: 10.1097/01.shk.0000245014.96419.3a. [DOI] [PubMed] [Google Scholar]
  181. Yu T, Junger WG, Yuan C, Jin A, Zhao Y, Zheng X, Zeng Y, Liu J. Shockwaves increase T-cell proliferation and IL-2 expression through ATP release, P2X7 receptors, and FAK activation. Am J Physiol Cell Physiol. 2010;298:C457–C464. doi: 10.1152/ajpcell.00342.2009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  182. Zhang Y, Phillips GJ, Li Q, Yeung ES. Imaging localized astrocyte ATP release with firefly luciferase beads attached to the cell surface. Anal Chem. 2008;80:9316–9325. doi: 10.1021/ac801701w. [DOI] [PubMed] [Google Scholar]
  183. Zhang T, Liu C, Zhou X, Kolosov VP, Perelman JM. Effects of ATP release on mucin5AC secretion in airway epithelial cells by mechanical stretching. Ann Clin Lab Sci. 2014;44:425–430. [PubMed] [Google Scholar]
  184. Zimmermann H (2006) Ectonucleotidases in the nervous system. Novartis Foundation Symposium 276 Purinergic Signalling in Neuron-Glial Interactions. Wiley, Chichester, pp 113–128 [PubMed]

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