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. 2007 May 1;9(2):479–523. doi: 10.1111/j.1582-4934.2005.tb00376.x

Novel type of interstitial cell (Cajal‐like) in human fallopian tube

LM Popescu 1,3,✉, Sanda M Ciontea 1, D Cretoiu 1,3, ME Hinescu 1,3, E Radu 1,3, N Ionescu 1, M Ceausu 3, Mihaela Gherghiceanu 3, R I Braga 2, Florina Vasilescu 3, L Zagrean 2, Carmen Ardeleanu 3
PMCID: PMC6740321  PMID: 15963270

Abstract

We describe here ‐ presumably for the first time‐a Cajal‐like type of tubal interstitial cells (t‐ICC), resembling the archetypal enteric ICC. t‐ICC were demonstrated in situ and in vitro on fresh preparations (tissue cryosections and primary cell cultures) using methylene‐blue, crystal‐violet, Janus‐Green B or Mito Tracker‐Green FM Probe vital stainings. Also, t‐ICC were identified in fixed specimens by light microscopy (methylene‐blue, Giemsa, trichrome stainings, Gomori silver‐impregnation) or transmission electron microscopy (TEM). The positive diagnosis of t‐ICC was strengthened by immunohistochemistry (IHC; CD117/c‐kit+ and other 14 antigens) and immunofluorescence (IF; CD117/c‐kit+ and other 7 antigens). The spatial density of t‐ICC (ampullar‐segment cryosections) was 100–150 cells/mm2. Non‐conventional light microscopy (NCLM) of Epon semithin‐sections revealed a network‐like distribution of t‐ICC in lammina propria and smooth muscle meshwork. t‐ICC appeared located beneath of epithelium, in a 10–15μ thick ‘belt’, where 18±2% of cells were t‐ICC. In the whole lamina propria, t‐ICC were about 9%, and in muscularis ∼7%. In toto, t‐ICC represent ∼8% of subepithelial cells, as counted by NCLM. In vitro, t‐ICC were 9.9±0.9% of total cell population.

TEM showed that the diagnostic ‘gold standard’ (Huizinga et al., 1997) is fulfilled by ‘our’ t‐ICC. However, we suggest a ‘platinum standard’, adding a new defining criterion ‐ characteristic cytoplasmic processes (number: 1–5; length: tens of μm; thickness: ±0.5μ; aspect: moniliform; braching: dichotomous; organization: network, labyrinthic‐system). Quantitatively, the ultrastructural architecture of t‐ICC is: nucleus, 23.6±3.2% of cell volume, with heterochromatin 49.1±3.8%; mitochondria, 4.8±1.7%; rough and smooth endoplasmic‐reticulum (1.1±0.6%, 1.0±0.2%, respectively); caveolae, 3.4±0.5%. We found more caveolae on the surface of cell processes versus cell body, as confirmed by IF for caveolins. Occasionally, the so‐called ‘Ca2+‐release units’ (subplasmalemmal close associations of caveolae+endoplasmic reticulum±mitochondria) were detected in the dilations of cell processes. Electrophysiological single unit recordings of t‐ICC in primary cultures indicated sustained spontaneous electrical activity (amplitude of field potentials: 57.26±6.56mV).

Besides the CD117/c‐kit marker, t‐ICC expressed variously CD34, caveolins 1&2, α‐SMA, S‐100, vimentin, nestin, desmin, NK‐1. t‐ICC were negative for: CD68, CD1a, CD62P, NSE, GFAP, chromogranin‐A, PGP9.5, but IHC showed the possible existence of (neuro)endocrine cells in tubal interstitium. We call them ‘JF cells’.

In conclusion, the identification of t‐ICC might open the door for understanding some tubal functions, e.g. pace‐making/peristaltism, secretion (auto‐, juxta‐ and/or paracrine), regulation of neurotransmission (nitrergic/purinergic) and intercellular signaling, via the very long processes. Furthermore, t‐ICC might even be uncommitted bipotential progenitor cells.

Keywords: interstitial cells of Cajal, uncommitted progenitor cells, CD117/c‐kit, intercellular signaling, caveolae/caveolins, vimentin, calcium release units, uterine tube, oviduct, tubal endocrine cells

References

  • 1. Orci L, Pepper MS, Microscopy: an art Nat Rev Mol Cell Biol. 2002; 3: 133–7. [DOI] [PubMed] [Google Scholar]
  • 2. Cajal SR. Sur les ganglions et plexus nerveux de l'intestin. C.R. Soc Biol (Paris). 1893; 45: 217–23. [Google Scholar]
  • 3. Cajal SR. Les nouvelles idées sur la structure du système nerveux chez l'homme et chez les vertébrés. Paris : C. Reinwald & Cie; 1895. [Google Scholar]
  • 4. Min KW, Seo IS. Interstitial cells of Cajal in the human small intestine: immunochemical and ultrastructural study. Ultrastruct Pathol. 2003; 27: 67–78. [DOI] [PubMed] [Google Scholar]
  • 5. Thuneberg L. One hundred years of interstitial cells of Cajal, Microsc Res Tech. 1999; 47: 223–38. [DOI] [PubMed] [Google Scholar]
  • 6. Vajda J, Feher E. Distribution and fine structure of the interstitial cells of Cajal. Acta Morphol Acad Sci Hung. 1980; 28: 251–8. [PubMed] [Google Scholar]
  • 7. Faussone Pellegrini MS, Cortesini C. Ultrastructural features and localization of the interstitial cells of Cajal in the smooth muscle coat of human esophagus, J Submicrosc Cytol. 1985; 17: 187–97. [PubMed] [Google Scholar]
  • 8. Faussone‐Pellegrini MS, Pantalone D, Cortesini C. Smooth muscle cells, interstitial cells of Cajal and myenteric plexus interrelationships in the human colon. Acta Anat (Basel). 1990; 139: 31–44. [DOI] [PubMed] [Google Scholar]
  • 9. Rumessen JJ, Peters S, Thuneberg L. Light‐and electron microscopical studies of interstitial cells of Cajal (ICC) and muscle cells at the submucosal border of human colon. Lab Invest. 1993; 68: 481–95. [PubMed] [Google Scholar]
  • 10. Rumessen JJ. Identification of interstitial cells of Cajal. Significance for studies of human small intestine and colon. Dan Med Bull. 1994; 41: 275–93. [PubMed] [Google Scholar]
  • 11. Hagger R, Gharaie S, Finlayson C, Kumar D. Distribution of the interstitial cells of Cajal in the human anorectum. J Auton Nerv Syst. 1998; 73: 75–9. [DOI] [PubMed] [Google Scholar]
  • 12. Thuneberg L, Rumessen JJ, Mikkelsen HB, Peters S, Jessen H. Structural aspects of interstital cells of Cajal as intestinal pacemaker cells, In: Huizinga JD, editor. Pacemaker activity and intercellular communication. Boca Ration : CRC Press; 1995. p. 193–222. [Google Scholar]
  • 13. Komuro T, Seki K, Horiguchi K. Ultrastructural characterization of the interstitial cells of Cajal. Arch Histol Cytol. 1999; 62: 295–316. [DOI] [PubMed] [Google Scholar]
  • 14. Faussone Pellegrini MS, Thuneberg L. Guide to the identification of interstitial cells of Cajal. Microsc Res Tech. 1999; 47: 248–66. [DOI] [PubMed] [Google Scholar]
  • 15. Huizinga JD, Thuneberg L, Vanderwinden JM, Rumessen JJ. Interstitial cells of Cajal as targets for pharmacological intervention in gastrointestinal motor disorders. Trends Pharmacol Sci. 1997; 18: 393–403. [DOI] [PubMed] [Google Scholar]
  • 16. Daniel EE, Berezin I, Interstitial cells of Cajal are they major player in control of gastrointestinal motility J Gastrointest Motil. 1992; 4: 1–24. [Google Scholar]
  • 17. Sanders KM. A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterol. 1996; 111: 492–515. [DOI] [PubMed] [Google Scholar]
  • 18. Koh SD, Sanders KM, Ward SM. Spontaneous electrical rhythmicity in cultured interstitial cells of Cajal, isolated from the murine small intestine. J Physiol (Lond). 1998; 513: 203–13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19. Thomsen L, Robinson TL, Lee JCF, Farraway LA, Hughes MJG, Andrews DW, Huizinga JD. Interstitial cells of Cajal generate a rhythmic pacemaker current. Nature Med. 1998; 4: 848–51. [DOI] [PubMed] [Google Scholar]
  • 20. Hirst GD, Ward SM. Interstitial cells: involvement in rhythmicity and neural control of gut smooth muscle. J Physiol. 2003; 550: 337–46. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21. Maeda H, Yamagata A, Nishikawa S, Yoshinaga K, Kobayashi S, Nishi K, Nishikawa SI. Requirement of c‐kit for development of intestinal pacemaker system. Development. 1992; 116: 369–75. [DOI] [PubMed] [Google Scholar]
  • 22. Ward SM, Burns AJ, Torihashi S, Sanders KM. Mutation of the proto‐oncogene c‐kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J Physiol. 1994; 480: 91–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23. Huizinga JD, Thuneberg L, Kluppel M, Malysz J, Mickkelsen HB, Bernstein A. W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature. 1995; 373: 347–9. [DOI] [PubMed] [Google Scholar]
  • 24. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T, Ishiguro S, Kawano K, Hanada N, Kurta A, Takeda M, Muhammad TG, Matsuzawa Y, Kanakura Y, Shinomura Y, Kitamura Y. Gain‐of‐function mutations of c‐kit in human gastrointestinal stromal tumors. Science. 1998; 279: 577–80. [DOI] [PubMed] [Google Scholar]
  • 25. Burton LD, Housley GD, Salih SG, Jaeenwood D. P2X2receptor expression by interstitial cells of Cajal in vas deferens implicated in semen emission. Auton Neurosci Basic Clin. 2000; 84: 147–61. [DOI] [PubMed] [Google Scholar]
  • 26. Sergeant GP, Hollywood MA, McCloskey KD, Thornbury KD, MCHale NG. Specilaized pacemaking cells in the rabbit urethra. J Physiol. 2000; 526: 359–66. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27. Sergeant GP, Hollywood MA, MCCloskey KD, McHale NG, Thornbury KD. Role of IP(3) in modulation of spontaneous activity in pacemaker cells of rabbit urethra. Am J Physiol Cell Physiol. 2001; 280: C1349–56. [DOI] [PubMed] [Google Scholar]
  • 28. Johnston L, Sergeant GP, Hollywood MA, Thornbury KD, McHale NG. Calcium oscillations in interstitial cells of the rabbit urethra. J Physiol. 2005: 566: 449–61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29. McCloskey KD, Gurney AM. Kti positive cells in the guinea‐pig bladder. J Urol. 2002; 168: 832–6. [PubMed] [Google Scholar]
  • 30. Blyweert W, Aa F, Ost D, Stagnaro M, Ridder D, Interstitial cells of the bladder. The missing link BJOK. 2004; 111: 57–60. [DOI] [PubMed] [Google Scholar]
  • 31. Hashitani H, Yanai Y, Suzuki H. Role of interstitial cells and gap junctions in the transmission of spontaneous Ca2+ signals in detrusor smooth muscles of the guinea‐pig urinary bladder. J Physiol. 2004; 559: 567–81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32. Gillespie JI, Markerink‐van Ittersum M, de Vente J. cGMP‐generating cells in the baldder wall: identification of distinct networks of interstitial cells. BJU Int. 2004; 94: 114–24. [DOI] [PubMed] [Google Scholar]
  • 33. Davisdson RA, McCloskey KD. Morphology and localization of interstitial cells in the guinea pig bladder. structural relationships with smooth muscle and neurons. J Urol. 2005; 173: 1385–90. [DOI] [PubMed] [Google Scholar]
  • 34. Pezzone MA, Watkins SC, Alber SM, King WE, de Groat CW, Chancellor MB, Fraser MO. Identification of c‐kit‐pisitive cells in the mouse ureter: the interstitial cells of Cajal of the urinary tract. Am J Renal Physiol. 2003; 284: 925–9. [DOI] [PubMed] [Google Scholar]
  • 35. Metzger R, Schuster T, Till H, Franke FE, Dietz HG. Cajal‐like cells in the uppr urinary tract. comparative study in various species. Pediatr Surg Int. 2005; 21: 169–74. [DOI] [PubMed] [Google Scholar]
  • 36. Duquette RA, Shmygol A, Vaillant C, Mobasheri A, Pope M, Burdyga T, Wray S, Vimentin‐positive, c‐KIT‐negative interstitial cells in human and rat uterus: A role in pacemarking Biol Reprod. 2005; 72: 276–83. [DOI] [PubMed] [Google Scholar]
  • 37. Ciontea MS, Radu E, Regalia T, Ceafalan L, Cretoiu D, Gherghiceanu M, Braga RI, Malincenco M, Zagrean L, Hinescu ME, Popescu LM. C‐kit immunopositive interstitial cells (Cajal‐type) in human myometrium. J Cell Mol Med. 2005; 9: 407–20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38. Pucovsky V, Moss RF, Bolton TB. Non‐contractile cells with thin processes resembling interstitial cells of Cajal found in the wall of guinea‐pig mesenteric arteries. J Physiol. 2003; 552: 119–33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39. Harhun MI, Gordienko DV, Povstyan OV, Moss RF, Bolton TB. Function of interstitial cells of Cajal in the rabbit protal vein. Circ Res. 2004; 95: 619–26. [DOI] [PubMed] [Google Scholar]
  • 40. Harhun MI, Pucovsky V, Povstyan OV, Gordienko DV, Bolton TB. Interstitial cells in the vasculatre. J Cell Mol Med. 2005; 9: 232–43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41. McCloskey KD, Hollywood MA, Thornbury KD, Ward SM, McHale NG. Kit‐like immunopositive cells in sheep mesenteric lymphatic vessels. Cell Tissue Res. 2002; 310: 77–84. [DOI] [PubMed] [Google Scholar]
  • 42. Exintaris B, Klemm MF, Lang RJ. Spontaneous slow wave and contractile activity of the guinea pig prostate. J Urol. 2002; 168: 315–22. [PubMed] [Google Scholar]
  • 43. van den Aa F, Roskams T, Blyweert W, de Ridder D, Interstitial cells in the human prostate: a new therapeutic target Prostate. 2003; 56: 250–5. [DOI] [PubMed] [Google Scholar]
  • 44. Hashitani H, Suzuki H. Identification of interstitial cells of Cajal in corporal tissues of the guinea‐pig penis. Br J Pharmacol. 2004; 141: 199–204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45. Popescu LM, Andrei F, Hinescu ME. Snapshots of mammary gland interstitial cells: methylene blue vital staining and c‐kit immunopositivity. J Cell Mol Med. 2005; 9: 476–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46. Popescu LM, Hinescu ME, Ionescu N, Ciontea MS, Cretoiu D, Ardeleanu C. Interstitial cells of Cajal in pancreas. J Cell Mol Med. 2005; 9: 169–90. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47. Hendrickson MR, Kempson RL. Normal histology, of the uterus and fallopian tubes In: Sternberg SS, editor. Histology for pathologists, 2nd edition Philadelphia : Lippincott‐Raven; 1997. p. 879–928. [Google Scholar]
  • 48. Hunt JL, Lynn AA. Histologic features of surgically removed fallopian tubes. Arch Pathol Lab Med. 2002; 126: 951–5. [DOI] [PubMed] [Google Scholar]
  • 49. Hunter RH, Have the Fallopian tubes a vital role in promoting fertility Acta Obstet Gynecol Scand. 1998; 77: 475–86. [PubMed] [Google Scholar]
  • 50. Leese HJ, Tay JI, Reischl J, Downing SJ. Formation of Fallopian tubal fluid: role of a neglected epithelium. Reproduction. 2001; 121: 339–46. [DOI] [PubMed] [Google Scholar]
  • 51. Arbab F, Goldsby J, Matijevic‐Aleksic N, Huang G, Ruan KH, Huang JC. Prostacyclin is an autocrine regulaor in the contraction of oviductal smooth muscle. Hum Reprod. 2002; 17: 3053–9. [DOI] [PubMed] [Google Scholar]
  • 52. Morimoto T, Head JR, MacDonald PC, Casey ML. Thrombospondin‐1 expression in human myometrium before and during pregnancy, before and during labor, and in human myometrial cells in culture. Biol Reprod. 1998; 59: 862–70. [DOI] [PubMed] [Google Scholar]
  • 53. Niculescu I. An atlas concerning morphological apects of visceral nerve endings. 1st ed Bucharest : Editura Medicla; 1958. [Google Scholar]
  • 54. Yack JE. Janus Green B as a rapid, vital stain for pheripheral nerves and chordotonal organs in insects. J Neurosci Methods. 1993; 49: 17–22. [DOI] [PubMed] [Google Scholar]
  • 55. Keij JF, Bell‐Prince C, Steinkamp JA. Staining of mitochondrial membranes with 10‐nonyl acridine orange, MitoFluor Green, and Mito Trcker Green is affected by mitochondrial membrane potential altering drugs. Cytometry. 2000; 39: 203–10. [DOI] [PubMed] [Google Scholar]
  • 56. Vanden Berghe P, Hennig GW, Smith TK. Characteristics of intermittent mitochondrial transport in guinea pig enteric nerve fibers. Am J Physiol Gastrointest Liver Physiol. 2004; 286: G671–82. [DOI] [PubMed] [Google Scholar]
  • 57. Bancroft JD, Gamble M, editors. Theory and practice of histological techniques. 5th ed London : Churchill Livingstone; 2002. [Google Scholar]
  • 58. Weibel ER. Practical methods for biological morphometry. Stereological methods. London : Academic Press; 1979. [Google Scholar]
  • 59. Hsu SM, Raine L, Fanger H. Use of avidin‐biotin‐peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unalbeled antibody (PAP) procedures. J Histochem Cytochem. 1981; 29: 577–80. [DOI] [PubMed] [Google Scholar]
  • 60. Bussolati G, Gugliotta P. Nonspecific staining of mast cells by avidin‐biotin‐peroxidase complexes (ABC). J Histochem Cytochem. 1983; 31: 1419–21. [DOI] [PubMed] [Google Scholar]
  • 61. Alberti E, Mikkelsen HB, Larsen JO, Jimmenez M. Motility patterns and distribution of interstitial cells of Cajal and nitergic neurons in the proximal, mid‐ and distal‐colon of the rat. Neurogastroenterol Motil. 2005; 17: 133–47. [DOI] [PubMed] [Google Scholar]
  • 62. Lazarow A, Cooperstein SJ. Studies on the enzymatic basis for the Janus green B staining reaction. J Histochem Cytochem. 1953; 1: 234–41. [DOI] [PubMed] [Google Scholar]
  • 63. Rumessen JJ, Vanderwinden JM. Interstitial cells in the musculature of the gastrointestinal tract: Cajal and beyond. Int Rev Cytol. 2003; 229: 115–208. [DOI] [PubMed] [Google Scholar]
  • 64. Huizinga JD, Faussone‐Pellegrini MS. About the presence of interstitial cells of Cajal outside the musculature of the gastrointestinal tract. J Cell Mol Med. 2005; 9: 468–73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65. Popescu LM, Diculescu I, Zelck U, Ionescu N. Ultrastructural distribution of calcium in smooth muscle cells of guinea‐pig taenia coli. A correlated electron microscopic and quantitative study. Cell Tissue Res. 1974; 154: 357–78. [DOI] [PubMed] [Google Scholar]
  • 66. Brinsfield TH, Fisher M, Hawk HW. Ultrastructure of endometrial stromal cells in the ewe during the estrous cycle and early pregnancy. J Anim Sci. 1974; 39: 565–74. [DOI] [PubMed] [Google Scholar]
  • 67. Popescu LM. A conceptual model of the excitation‐contraction coupling in smooth muscle: the possible role of the surface microvesicles. Studia Biophys. 1974; 44: 141–53. [Google Scholar]
  • 68. Moore ED, Voigt T, Kobayashi YM, Isenberg G, Fay FS, Gallitelli MF, Frnzini‐Armstrong C. Oranization of Ca2+ release units in excitable smooth muscle of the guinea‐pig urinary bladder. Biophys J. 2004; 87: 1836–47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69. Schurch W, Seemayer TA, Gabbiani G. Myofibroblast In: Sternberg SS, editor. Histology for pathologists, 2ndedition Philadelphia : Lippincott‐Raven; 1997. p. 129–65. [Google Scholar]
  • 70. Wheaton K, Sampsel K, Biosvert FM, Davy A, Robbins S, Riabowol K. Loss of functional caveolae during senescence of human fibroblasts. J Cell Physiol. 2001; 187: 226–35. [DOI] [PubMed] [Google Scholar]
  • 71. Capozza F, Cohen AW, Chenug MW, Sotgia F, Schubert W, Battista M, Lee H, Franke PG, Lisanti MP. Muscile‐specific interaction of caveloin isoforms: differential complex formation between caveolins in fibroblastic vs. muscle cells. Am J Physiol Cell Physiol. 2005; 288: C677–91. [DOI] [PubMed] [Google Scholar]
  • 72. Schurch W, Seemayer TA, Gabbiani G. The myofibroblast: a quarter century after its discovery. Am J Surg Pathol. 1998; 22: 141–7. [DOI] [PubMed] [Google Scholar]
  • 73. Eyden B. The myofibroblast: an assessment of controversial issues and a definition useful in diagnosis and research. Ultrastruct Pathol. 2001; 25: 39–50. [DOI] [PubMed] [Google Scholar]
  • 74. Powell DW, Miffin RC, Valentich JD, Crowe SE, Saada JI, West AB. Myofibroblasts. I. Paracrine cells important in health and disease. Am J Physiol. 1999; 277: C1–9. [DOI] [PubMed] [Google Scholar]
  • 75. Walter I. Myofibroblasts in the mucosal layer of the uterine tube. Ital J Anat Embryol. 1998; 103: 259–66. [PubMed] [Google Scholar]
  • 76. Lee H, Doughlas‐Jones AG, Morgan JM, Jasani B. The effect of fixation and processing on the sensitivity of oestrogen receptor assay by immunohistochemistry in breast carcinoma. J Clin Pathol. 2002; 55: 236–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77. Torihashi S, Horisawa M, Watanabe Y. c‐Kit immunoreactive intersitial cells in the human gastrointestinal tract. J Auton Nerv Syst. 1999; 75: 38–85. [DOI] [PubMed] [Google Scholar]
  • 78. Cho WJ, Daniel EF. Proteins of interstitial cells of Cajal and intestinal smooth muscle, colocalized with caveolin‐1. Am J Physiol Gastrointest Liver Physiol. 2005; 288: G571–85. [DOI] [PubMed] [Google Scholar]
  • 79. Puxeddu I, Piliponsky AM, Bachelet I, Levi‐Schaffer F. Mast cells in allergy and beyond. Int J Boiochem Cell Biol. 2003; 35: 1601–7. [DOI] [PubMed] [Google Scholar]
  • 80. Vanderwinden JM, Rumessen JJ, de Laet MH, Vanderhaeghen JJ, Schiffmann SN. CD34+ cells in human intestine are fibroblasts adjacent to, but distinct from, interstitial cells of Cajal. Lab Invest. 1999; 79: 59–65. [PubMed] [Google Scholar]
  • 81. Fina L, Molgaard HW, Robertson D, Bradley NJ, Monaghan P, Delia D, Sutherland DR, Baker MA, Greaves MF. Expression of the CD34 gene in vascular endothelial cells. Blood. 1990; 75: 2417–26. [PubMed] [Google Scholar]
  • 82. Tsujimura T, Makiishi‐Shimobayashi C, Lundkvist J, Lendahl U, Nakasho K, Sugihara A, Iwasaki T, Mano M, Yamada N, Yamashita K, Toyosaka A, Terada N. Expression of the inermediate filament nestin in gastrointestinal stromal tumors and interstitial cells of Cajal, Am J Pathol. 2001; 158: 817–23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 83. Torihashi S, Ward SM, Sanders KM. Development of c‐kit‐positive cells and the onset of electrical rhythmicity in murine small intestine. Gastroenterology. 1997; 112: 144–55. [DOI] [PubMed] [Google Scholar]
  • 84. Grinder JR. Focus on “molecular markers expressed in cultured and freshly isolated interstitial cells of Cajal”. Am J Physiol Cell Physiol. 2000; 279: C284–5. [DOI] [PubMed] [Google Scholar]
  • 85. Vento P, Soinila S. Quantitative comparison of growth‐associated protein GAP‐43, neuron specific enolase and protein gene product 9.5 as neuronal markers in mature human intestine. J Histochem Cytochem. 1999; 47: 1405–15. [DOI] [PubMed] [Google Scholar]
  • 86. An S, Zenisek D. Regulation of exocytosis in neurons and neuroendocrine cells. Curr Opin Neurobiol. 2004; 14: 522–30. [DOI] [PubMed] [Google Scholar]
  • 87. Dursun P, Salman MC, Taskiran C, Usubutun A, Ayhan A. Primary neuroendocrine carcinoma of the fallopian tube: a case report. Am J Obstet Gynecol. 2004; 190: 568–71. [DOI] [PubMed] [Google Scholar]
  • 88. Kuriyanma H, Kitamura K, Itoh T, Inou R. Physiological features of visceral smooth muscle cells, with special reference to receptors and ion channels. Physiol Rev. 1998; 78: 811–920. [DOI] [PubMed] [Google Scholar]
  • 89. Vanderwinden JM, Gillard K, de Laet MH, Messam CA, Schiffmann SN. Distribution of the intermediate filament nestin in the muscularis propria of the human gastrointestinal tract. Cell Tissue Res. 2002; 309: 261–8. [DOI] [PubMed] [Google Scholar]
  • 90. Ortiz‐Hidalgo C, de Leon B, Albores‐Saavedra J. Stromal tumor of the gallbladder with phenotype of interstitial cells of Cajal: a previously unrecognized neoplasm.. Am J Surg. Pathol, 2000; 24: 1420–3. [DOI] [PubMed] [Google Scholar]
  • 91. Sakurai S, Fukasawa T, Chong JM, Tanaka A, Fukayama M. Embryonic form of smooth muscle myosin heavy chain (SMemb/MHC‐B) in gastrointestinal stromal tumor and interstitial cells of Cajal. Am J Pathol. 1999; 154: 23–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 92. Raff M, Adult stem cell plasticity: fact or artifact Annu Rev Cell Dev Biol. 2003; 19: 1–22. [DOI] [PubMed] [Google Scholar]
  • 93. Epperson A, Hatton WJ, Callaghan B, Doherty P, Walker RL, Sanders KM, Ward SM, Horowitz B. Molecular markers expressed in cultured and freshly isolated interstitial cells of Cajal. Am J Physiol Cell Physiol. 2000; 279: C529–39. [DOI] [PubMed] [Google Scholar]
  • 94. Li CX, Liu BH, Tong WD, Zhang LY, Jiang YP. Dissociation, culture and morphologic changes of interstitial cells of Cajal in vitro. World J Gastroenterol. 2005; 22: 2838–40. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 95. Torihashi S, Ward SM, Nishikawa S, Nishi K, Kobayashi S, Sanders KM. c‐kit‐dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract. Cell Tissue Res. 1995; 280: 97–111. [DOI] [PubMed] [Google Scholar]
  • 96. Tong WD, Liu BH, Zhang LY, Xiong RP, Liu P, Zhang SB. Expression of c‐kit messenger ribonucleic acid and c‐kit protein in sigmoid colon of patients with slow transit constipation. Int J Colorectal Dis. 2005; 20: 363–7. [DOI] [PubMed] [Google Scholar]
  • 97. Isozaki K, Terris B, Belghiti J, Schiffmann S, Hirota S, Vanderwinden JM. Germline‐activating mutation in the kinase domain of KIT gene in familial gastrointestinal stromal tumors. Am J Pathol. 2000; 157: 1581–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98. Torihashi S, Nishi K, Tokutomi Y, Nishi T, Ward S, Sanders KM. Blockade of kit signaling induces transdifferentiation of interstitial cells of Cajal to a smooth muscle phenotype. Gastroenterology. 1999; 117: 140–8. [DOI] [PubMed] [Google Scholar]
  • 99. Sarlomo‐Rikala M, Kovatich AJ, Barusevicius A, Miettinen M. CD117: a sensitiver marker for gastrointestinal stromal tumors that is more specific than CD34.. Mod. Pathol. 1998, 11: 728–34. [PubMed] [Google Scholar]
  • 100. Dhimes P, Lopez‐Carreira M, Ortega‐Serrano MP, Garcia‐Munoz H, Martinez‐Gonzalez MA, Ballestin C. Gastrointestinal autonomic nerve tumours and their separation from other gastrointestinal stromal tumours: an ultrastructural and immunohistochemical study of seven cases. Virchows Arch. 1995; 426: 27–35. [DOI] [PubMed] [Google Scholar]
  • 101. Yamazaki K, Eyden BP. Ultrastructural and immunohistochemical studies of stromal cells in lamina propria of human fallopian tube ampullar mucosa: the recognition of ‘CD34 positive reticular network’ and its putative function for immune surveillance. J Submicrosc Cytol Pathol. 1995; 28: 325–37. [PubMed] [Google Scholar]
  • 102. Sircar K, Hewlett BR, Huizinga JD, Chorneyko K, Berezin I, Riddell RH. Interstitial cells of Cajal as precursors of gastrointestinal stromal tumors. Am J Surg Pathol. 1999; 23: 377–89. [DOI] [PubMed] [Google Scholar]
  • 103. Piaseczna PA, Rolle U, Solari V, Puri P, Interstitial cells of Cajal in the Human normal urinary bladder and in the bladder of patients with megacystis‐microcolon intestinal hypoperistalsis syndrome. BJU Int. 2004; 94: 143–6. [DOI] [PubMed] [Google Scholar]
  • 104. Bucala R, Spiegel LA., Chesney J, Hogan M, Cerami A. Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Mol Med. 1994; 1: 71–81. [PMC free article] [PubMed] [Google Scholar]
  • 105. Young HM. Embryological origin of interstitial cells of Cajal. Microsc Res Tech. 1999; 47: 303–8. [DOI] [PubMed] [Google Scholar]
  • 106. Neijssen J, Herberts C, Drijfhout JW, Reits E, Janssen L, Neefjes J. Cross‐presentation by intercellular peptide transfer through gap junctions. Nature. 2005; 434: 83–8. [DOI] [PubMed] [Google Scholar]
  • 107. Ward SM, Ordog T, Koh SD, Baker SA, Jun JY, Amberg G, Monaghan K, Sanders KM. Pacemaking in interstitial cells of Cajal depends upon calcium handling by endoplasmic reticulum and mitochondria. J Physiol. 2000; 525: 355–61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 108. Yoneda S, Takano H, Takaki M, Suzuki H. Properties of Spontaneously active cells distributed in the submucosal layer of mouse proximal colon. J Physiol. 2002; 542: 887–97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 109. Hanani M, Farrugia G, Komuro T. Intercellular coupling of interstitial cells of Cajal in the digestive tract. Int Rev Cytol. 2005; 242: 249–82. [DOI] [PubMed] [Google Scholar]
  • 110. Daniel EE, Willis A, Cho WJ, Boddy G. Comparisons of neural and pcing activities in intestinal segments from W/W++ and W/W(V) mice. Neurogastroenterol Motil. 2005; 17: 355–65. [DOI] [PubMed] [Google Scholar]
  • 111. Jankovic SM, Protic BA, Jankovic SV. Contractile effect of acetylcholine on isolated ampullar segment of Fallopian tubes. Pharmacol Res. 2004; 49: 31–5. [DOI] [PubMed] [Google Scholar]
  • 112. Samuelson UE, Wiklund NP, Gustafsson LE. Endogenous purines may modulate adrenergic neurotransmission in the human fallopian tube. Neurosci Lett. 1988; 85: 51–5. [DOI] [PubMed] [Google Scholar]
  • 113. Ziganshin Au, Vafina Z., Fatkullin IF. Pharmacological characterization of P2‐receptors in human fallopian tubes. Bull Exp Biol Med. 2004; 137: 242–5. [DOI] [PubMed] [Google Scholar]
  • 114. Ekerhovd E, Brannstrom M, Alexandersson M, Norstrom A Evidence for nitric oxide mediation of contractile activity in isolated strips of the human Fallopian tube. Hum Reprod. 1997; 12: 301–5. [DOI] [PubMed] [Google Scholar]
  • 115. Ekerhovd E, Norstrom A. Involvement of a nitric oxide‐cycle guanosine monophosphate pathyway in control of fallopian tube contractility. Gynecol Endocrinol. 2004; 19: 239–46. [DOI] [PubMed] [Google Scholar]
  • 116. Briton‐Jones C, Hung Lok I, Yuen PM, Chiu TTY, Cheung LP, Haines C, Regulation of human ovidectin mRNA expressin in vivo. Fertil Steril. 2001; 75: 942–6. [DOI] [PubMed] [Google Scholar]
  • 117. Streuli C. Extracellular matrix remodelling and cellular differentiation. Curr Opin Cell Biol. 1999; 11: 634–40. [DOI] [PubMed] [Google Scholar]
  • 118. Tomasek JT, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechanoregulation of connective tissue remodelling. Nat Rev Mol Cell Biol. 2002; 3: 349–63. [DOI] [PubMed] [Google Scholar]
  • 119. Demouillere A, Darby IA, Gabbiani G. Normal and pathologic soft tissue remodeling: role of the myofibroblast, with special emphasis on liver and kidney fibrosis. Lab Invest. 2003; 83: 1689–707. [DOI] [PubMed] [Google Scholar]
  • 120. Sartore S, Chiavegato A, Faffin E, Franch R, Puato M, Ausoni S, Pauletto P. Contribution of adventitial fibroblasts to neointima formation and vascular remodeling. From innocent bystander to active participant. Circ ResK. 2001; 89: 1111–21. [DOI] [PubMed] [Google Scholar]
  • 121. Watrelot A, Hamilton J, Crudzinskas JG. Advances in the assessment of the uterus and fallopian tube function. Best Pract Res Clin Obst Cynaecol. 2003; 17: 187–209. [DOI] [PubMed] [Google Scholar]
  • 122. Talevi R, Gualtieri R. In vivo versus in vitro fertilization Eur J Obst Gynecol Reprod Biol. 2004; 115S: S68–S71. [DOI] [PubMed] [Google Scholar]

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