Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 2001 May 15;356(Pt 1):191–198. doi: 10.1042/0264-6021:3560191

Activation of store-mediated calcium entry by secretion-like coupling between the inositol 1,4,5-trisphosphate receptor type II and human transient receptor potential (hTrp1) channels in human platelets.

J A Rosado 1, S O Sage 1
PMCID: PMC1221827  PMID: 11336651

Abstract

Physical coupling between inositol 1,4,5-trisphosphate (IP(3)) receptors and transient receptor potential (Trp) channels has been demonstrated in both transfected and normal cells as a candidate mechanism for the activation of store-mediated Ca(2+) entry (SMCE). We have investigated the properties of the coupling between the type II IP(3) receptor and naturally expressed human Trp1 (hTrp1) in human platelets. Treatment with xestospongin C, an inhibitor of IP(3) receptor function, abolished SMCE and coupling between the IP(3) receptor and hTrp1. The coupling was activated by depletion of the intracellular Ca(2+) stores, and was reversed by refilling of the stores. We have also examined the role of actin filaments in the activation and maintenance of the coupling. Stabilization of the cortical actin network with jasplakinolide prevented the coupling, indicating that, as with secretion, the actin filaments at the cell periphery act as a negative clamp which prevents constitutive coupling. In addition, the actin cytoskeleton plays a positive role, since disruption of the actin network inhibited the coupling when the Ca(2+) stores were depleted. These results provide strong evidence for the activation of SMCE by a secretion-like coupling mechanism involving a reversible association between IP(3) receptors and hTrp1 in normal human cells.

Full Text

The Full Text of this article is available as a PDF (281.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berridge M. J. Capacitative calcium entry. Biochem J. 1995 Nov 15;312(Pt 1):1–11. doi: 10.1042/bj3120001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bird G. S., Putney J. W., Jr Inhibition of thapsigargin-induced calcium entry by microinjected guanine nucleotide analogues. Evidence for the involvement of a small G-protein in capacitative calcium entry. J Biol Chem. 1993 Oct 15;268(29):21486–21488. [PubMed] [Google Scholar]
  3. Birnbaumer L., Boulay G., Brown D., Jiang M., Dietrich A., Mikoshiba K., Zhu X., Qin N. Mechanism of capacitative Ca2+ entry (CCE): interaction between IP3 receptor and TRP links the internal calcium storage compartment to plasma membrane CCE channels. Recent Prog Horm Res. 2000;55:127–162. [PubMed] [Google Scholar]
  4. Birnbaumer L., Zhu X., Jiang M., Boulay G., Peyton M., Vannier B., Brown D., Platano D., Sadeghi H., Stefani E. On the molecular basis and regulation of cellular capacitative calcium entry: roles for Trp proteins. Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15195–15202. doi: 10.1073/pnas.93.26.15195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boulay G., Brown D. M., Qin N., Jiang M., Dietrich A., Zhu M. X., Chen Z., Birnbaumer M., Mikoshiba K., Birnbaumer L. Modulation of Ca(2+) entry by polypeptides of the inositol 1,4, 5-trisphosphate receptor (IP3R) that bind transient receptor potential (TRP): evidence for roles of TRP and IP3R in store depletion-activated Ca(2+) entry. Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):14955–14960. doi: 10.1073/pnas.96.26.14955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cooper J. A. Effects of cytochalasin and phalloidin on actin. J Cell Biol. 1987 Oct;105(4):1473–1478. doi: 10.1083/jcb.105.4.1473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. El-Daher S. S., Patel Y., Siddiqua A., Hassock S., Edmunds S., Maddison B., Patel G., Goulding D., Lupu F., Wojcikiewicz R. J. Distinct localization and function of (1,4,5)IP(3) receptor subtypes and the (1,3,4,5)IP(4) receptor GAP1(IP4BP) in highly purified human platelet membranes. Blood. 2000 Jun 1;95(11):3412–3422. [PubMed] [Google Scholar]
  8. Fasolato C., Hoth M., Penner R. A GTP-dependent step in the activation mechanism of capacitative calcium influx. J Biol Chem. 1993 Oct 5;268(28):20737–20740. [PubMed] [Google Scholar]
  9. Gafni J., Munsch J. A., Lam T. H., Catlin M. C., Costa L. G., Molinski T. F., Pessah I. N. Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor. Neuron. 1997 Sep;19(3):723–733. doi: 10.1016/s0896-6273(00)80384-0. [DOI] [PubMed] [Google Scholar]
  10. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  11. Hartwig J. H. Mechanisms of actin rearrangements mediating platelet activation. J Cell Biol. 1992 Sep;118(6):1421–1442. doi: 10.1083/jcb.118.6.1421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jenner S., Farndale R. W., Sage S. O. The effect of calcium-store depletion and refilling with various bivalent cations on tyrosine phosphorylation and Mn2+ entry in fura-2-loaded human platelets. Biochem J. 1994 Oct 15;303(Pt 2):337–339. doi: 10.1042/bj3030337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kiselyov K., Mignery G. A., Zhu M. X., Muallem S. The N-terminal domain of the IP3 receptor gates store-operated hTrp3 channels. Mol Cell. 1999 Sep;4(3):423–429. doi: 10.1016/s1097-2765(00)80344-5. [DOI] [PubMed] [Google Scholar]
  14. Kiselyov K., Xu X., Mozhayeva G., Kuo T., Pessah I., Mignery G., Zhu X., Birnbaumer L., Muallem S. Functional interaction between InsP3 receptors and store-operated Htrp3 channels. Nature. 1998 Dec 3;396(6710):478–482. doi: 10.1038/24890. [DOI] [PubMed] [Google Scholar]
  15. Liu X., Wang W., Singh B. B., Lockwich T., Jadlowiec J., O'Connell B., Wellner R., Zhu M. X., Ambudkar I. S. Trp1, a candidate protein for the store-operated Ca(2+) influx mechanism in salivary gland cells. J Biol Chem. 2000 Feb 4;275(5):3403–3411. doi: 10.1074/jbc.275.5.3403. [DOI] [PubMed] [Google Scholar]
  16. Lockwich T. P., Liu X., Singh B. B., Jadlowiec J., Weiland S., Ambudkar I. S. Assembly of Trp1 in a signaling complex associated with caveolin-scaffolding lipid raft domains. J Biol Chem. 2000 Apr 21;275(16):11934–11942. doi: 10.1074/jbc.275.16.11934. [DOI] [PubMed] [Google Scholar]
  17. Ma H. T., Patterson R. L., van Rossum D. B., Birnbaumer L., Mikoshiba K., Gill D. L. Requirement of the inositol trisphosphate receptor for activation of store-operated Ca2+ channels. Science. 2000 Mar 3;287(5458):1647–1651. doi: 10.1126/science.287.5458.1647. [DOI] [PubMed] [Google Scholar]
  18. Muallem S., Kwiatkowska K., Xu X., Yin H. L. Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol. 1995 Feb;128(4):589–598. doi: 10.1083/jcb.128.4.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Parekh A. B., Penner R. Store depletion and calcium influx. Physiol Rev. 1997 Oct;77(4):901–930. doi: 10.1152/physrev.1997.77.4.901. [DOI] [PubMed] [Google Scholar]
  20. Patterson R. L., van Rossum D. B., Gill D. L. Store-operated Ca2+ entry: evidence for a secretion-like coupling model. Cell. 1999 Aug 20;98(4):487–499. doi: 10.1016/s0092-8674(00)81977-7. [DOI] [PubMed] [Google Scholar]
  21. Putney J. W., Jr, McKay R. R. Capacitative calcium entry channels. Bioessays. 1999 Jan;21(1):38–46. doi: 10.1002/(SICI)1521-1878(199901)21:1<38::AID-BIES5>3.0.CO;2-S. [DOI] [PubMed] [Google Scholar]
  22. Putney J. W., Jr TRP, inositol 1,4,5-trisphosphate receptors, and capacitative calcium entry. Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):14669–14671. doi: 10.1073/pnas.96.26.14669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Quinton T. M., Dean W. L. Multiple inositol 1,4,5-trisphosphate receptor isoforms are present in platelets. Biochem Biophys Res Commun. 1996 Jul 25;224(3):740–746. doi: 10.1006/bbrc.1996.1093. [DOI] [PubMed] [Google Scholar]
  24. Rosado J. A., Jenner S., Sage S. O. A role for the actin cytoskeleton in the initiation and maintenance of store-mediated calcium entry in human platelets. Evidence for conformational coupling. J Biol Chem. 2000 Mar 17;275(11):7527–7533. doi: 10.1074/jbc.275.11.7527. [DOI] [PubMed] [Google Scholar]
  25. Rosado J. A., Sage S. O. Coupling between inositol 1,4,5-trisphosphate receptors and human transient receptor potential channel 1 when intracellular Ca2+ stores are depleted. Biochem J. 2000 Sep 15;350(Pt 3):631–635. [PMC free article] [PubMed] [Google Scholar]
  26. Rosado J. A., Sage S. O. Farnesylcysteine analogues inhibit store-regulated Ca2+ entry in human platelets: evidence for involvement of small GTP-binding proteins and actin cytoskeleton. Biochem J. 2000 Apr 1;347(Pt 1):183–192. [PMC free article] [PubMed] [Google Scholar]
  27. Valentijn K., Valentijn J. A., Jamieson J. D. Role of actin in regulated exocytosis and compensatory membrane retrieval: insights from an old acquaintance. Biochem Biophys Res Commun. 1999 Dec 29;266(3):652–661. doi: 10.1006/bbrc.1999.1883. [DOI] [PubMed] [Google Scholar]
  28. Yao Y., Ferrer-Montiel A. V., Montal M., Tsien R. Y. Activation of store-operated Ca2+ current in Xenopus oocytes requires SNAP-25 but not a diffusible messenger. Cell. 1999 Aug 20;98(4):475–485. doi: 10.1016/s0092-8674(00)81976-5. [DOI] [PubMed] [Google Scholar]
  29. Zhu X., Jiang M., Peyton M., Boulay G., Hurst R., Stefani E., Birnbaumer L. trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry. Cell. 1996 May 31;85(5):661–671. doi: 10.1016/s0092-8674(00)81233-7. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES