Interstitial cells in the primate gastrointestinal tract

Cell and Tissue Research

Volumn 350, Issue 2, 2012, Pages 199-213

  Blair, Peter J ^a   Bayguinov, Yulia ^a   Sanders, Kenton M ^a   Ward, Sean M ^a  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

ANO1; Histamine; ICC; Mast cells; PDGFRa+ cells; TMEM16A

Indexed keywords

ANTIBODY; HISTAMINE ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL SUBPOPULATION; COLON; CONFOCAL MICROSCOPY; FEMALE; FROZEN SECTION; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRACT; HAPLORHINI; IMAGE RECONSTRUCTION; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELL OF CAJAL; LAMINA PROPRIA; LOWER ESOPHAGUS SPHINCTER; MALE; MAST CELL; MORPHOLOGY; MYENTERIC PLEXUS; NONHUMAN; PRIMATE; PRIORITY JOURNAL; RODENT; SMALL INTESTINE; SMOOTH MUSCLE FIBER; SPINDLE CELL; STOMACH; THREE DIMENSIONAL IMAGING;

ANIMALS; FEMALE; GASTROINTESTINAL TRACT; HUMANS; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELLS OF CAJAL; MACACA FASCICULARIS; MALE;

MACACA FASCICULARIS; PRIMATES; RODENTIA;

EID: 84871241376     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-012-1468-7     Document Type: Article

References (60)

1. Albertí E, Mikkelsen HB, Wang XY, Díaz M, Larsen JO, Huizinga JD, Jiménez M (2007) Pacemaker activity and inhibitory neurotransmission in the colon of Ws/Ws mutant rats. Am J Physiol Gastrointest Liver Physiol 292:G1499-G1510
2. Aranishi H, Kunisawa Y, Komuro T (2009) Characterization of interstitial cells of Cajal in the subserosal layer of the guinea-pig colon. Cell Tissue Res 335:323-329
3. Beckett EA, Horiguchi K, Khoyi M, Sanders KM, Ward SM (2002) Loss of enteric motor neurotransmission in the gastric fundus of Sl/Sl(d) mice. J Physiol 543:871-887
4. Bernardini N, Segnani C, Ippolito C, De Giorgio R, Colucci R, Faussone-Pellegrini MS, Chiarugi M, Campani D, Castagna M, Mattii L, Blandizzi C, Dolfi A (2012) Immunohistochemical analysis of myenteric ganglia and interstitial cells of Cajal in ulcerative colitis. J Cell Mol Med 16:318-327
5. Burns AJ, Lomax AE, Torihashi S, Sanders KM, Ward SM (1996) Interstitial cells of Cajal mediate inhibitory neurotransmission in the stomach. Proc Natl Acad Sci USA 93:12008-12013
6. Burns AJ, Herbert TM, Ward SM, Sanders KM (1997) Interstitial cells of Cajal in the guinea-pig gastrointestinal tract as revealed by c-Kit immunohistochemistry. Cell Tissue Res 290:11-20
7. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, Pfeffer U, Ravazzolo R, Zegarra-Moran O, Galietta LJ (2008) TMEM16A, a membrane protein associated with calciumdependent chloride channel activity. Science 322:590-594
8. Chen H, Ordög T, Chen J, Young DL, Bardsley MR, Redelman D, Ward SM, Sanders KM (2007) Differential gene expression in functional classes of interstitial cells of Cajal in murine small intestine. Physiol Genom 31:492-509
9. Cobine CA, Hennig GW, Bayguinov YR, Hatton WJ, Ward SM, Keef KD (2010) Interstitial cells of Cajal in the cynomolgus monkey rectoanal region and their relationship to sympathetic and nitrergic nerves. Am J Physiol Gastrointest Liver Physiol 298:G643-G656
10. Cobine CA, Hennig GW, Kurahashi M, Sanders KM, Ward SM, Keef KD (2011) Relationship between interstitial cells of Cajal, fibroblast-like cells and inhibitory motor nerves in the internal anal sphincter. Cell Tissue Res 344:17-30
11. Dickens EJ, Hirst GD, Tomita T (1999) Identification of rhythmically active cells in guinea-pig stomach. J Physiol 514(Pt 2):515-531
12. Dickens EJ, Edwards FR, Hirst GD (2001) Selective knockout of intramuscular interstitial cells reveals their role in the generation of slow waves in mouse stomach. J Physiol 531:827-833
13. Espinosa I, Lee CH, Kim MK, Rouse BT, Subramanian S, Montgomery K, Varma S, Corless CL, Heinrich MC, Smith KS, Wang Z, Rubin B, Nielsen TO, Seitz RS, Ross DT, West RB, Cleary ML, van de Rijn M (2008) A novel monoclonal antibody against DOG1 is a sensitive and specific marker for gastrointestinal stromal tumors. Am J Surg Pathol 32:210-218
14. Fox EA, Phillips RJ, Martinson FA, Baronowsky EA, Powley TL (2001) C-Kit mutant mice have a selective loss of vagal intramuscular mechanoreceptors in the forestomach. Anat Embryol (Berl) 204:11-26
15. Gomez-Pinilla PJ, Gibbons SJ, Bardsley MR, Lorincz A, Pozo MJ, Pasricha PJ, Van de Rijn M, West RB, Sarr MG, Kendrick ML, Cima RR, Dozois EJ, Larson DW, Ordog T, Farrugia G (2009) Ano1 is a selective marker of interstitial cells of Cajal in the human and mouse gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 296:G1370-G1381
16. Grützkau A, Smorodchenko A, Lippert U, Kirchhof L, Artuc M, Henz BM (2004) LAMP-1 and LAMP-2, but not LAMP-3, are reliable markers for activation-induced secretion of human mast cells. Cytometry A 61:62-68
17. Hagger R, Gharaie S, Finlayson C, Kumar D (1998) Regional and transmural density of interstitial cells of Cajal in human colon and rectum. Am J Physiol 275:G1309-G1316
18. Horiguchi K, Semple GS, Sanders KM, Ward SM (2001) Distribution of pacemaker function through the tunica muscularis of the canine gastric antrum. J Physiol 537:237-250
19. Huizinga JD, Thuneberg L, Kluppel M, Malysz J, Mikkelsen HB, Bernstein A (1995) W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 373:347-349
20. Hwang SJ, Blair PJ, Britton FC, O'Driscoll KE, Hennig G, Bayguinov YR, Rock JR, Harfe BD, Sanders KM, Ward SM (2009) Expression of anoctamin 1/TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles. J Physiol 587:4887-4904
21. Ibba Manneschi L, Pacini S, Corsani L, Bechi P, Faussone-Pellegrini MS (2004) Interstitital cells of Cajal in the human stomach: distribution and relationship with enteric innervation. Histol Histopathol 19:1153-1164
22. Iino S, Horiguchi K, Nojyo Y (2008) Interstitial cells of Cajal are innervated by nitrergic nerves and express nitric oxide-sensitive guanylate cyclase in the guinea-pig gastrointestinal tract. Neuroscience 152:437-448
23. Iino S, Horiguchi K, Horiguchi S, Nojyo Y (2009) c-Kit-negative fibroblast-like cells express platelet-derived growth factor receptor alpha in the murine gastrointestinal musculature. Histochem Cell Biol 131:691-702
24. Johansson O, Virtanen M, Hilliges M, Yang Q (1994) Histamine immunohistochemistry is superior to the conventional heparin-based routine staining methodology for investigations of human skin mast cells. Histochem J 26:424-430
25. Kinoshita K, Horiguchi K, Fujisawa M, Kobirumaki F, Yamato S, Hori M, Ozaki H (2007) Possible involvement of muscularis resident macrophages in impairment of interstitial cells of Cajal and myenteric nerve systems in rat models of TNBS-induced colitis. Histochem Cell Biol 127:41-53
26. Komuro T, Seki K, Horiguchi K (1999) Ultrastructural characterization of the interstitial cells of Cajal. Arch Histol Cytol 62:295-316
27. Kurahashi M, Niwa Y, Cheng J, Ohsaki Y, Fujita A, Goto H, Fujimoto T, Torihashi S (2008) Platelet-derived growth factor signals play critical roles in differentiation of longitudinal smooth muscle cells in mouse embryonic gut. Neurogastroenterol Motil 20:521-531
28. Kurahashi M, Zheng H, Dwyer L, Ward SM, Don Koh S, Sanders KM (2011) A functional role for the 'fibroblast-like cells' in gastrointestinal smooth muscles. J Physiol 589:697-710
29. Kurahashi M, Nakano Y, Hennig GW, Ward SM, Sanders KM (2012) Platelet derived growth factor receptor a-positive cells in the tunica muscularis of human colon. J Cell Mol Med
30. Liu YA, Chung YC, Pan ST, Hou YC, Peng SJ, Pasricha PJ, Tang SC (2012) 3-D illustration of network orientations of interstitial cells of Cajal subgroups in human colon as revealed by deep-tissue imaging with optical clearing. Am J Physiol Gastrointest Liver Physiol 302:G1099-G1110
31. Maeda H, Yamagata A, Nishikawa S, Yoshinaga K, Kobayashi S, Nishi K (1992) Requirement of c-kit for development of intestinal pacemaker system. Development 116:369-375
32. McCloskey KD, Gurney AM (2002) Kit positive cells in the guinea pig bladder. J Urol 168:832-836
33. McHale NG, Hollywood MA, Sergeant GP, Shafei M, Thornbury KT, Ward SM (2006) Organization and function of ICC in the urinary tract. J Physiol 576:689-694
34. Mikkelsen HB (2010) Interstitial cells of Cajal, macrophages and mast cells in the gut musculature: morphology, distribution, spatial and possible functional interactions. J Cell Mol Med 14:818-832
35. Nissinen MJ, Panula P (1995) Developmental patterns of histamine-like immunoreactivity in themouse. J HistochemCytochem43:211-227
36. Ordog T, Ward SM, Sanders KM (1999) Interstitial cells of cajal generate electrical slow waves in the murine stomach. J Physiol 518(Pt 1):257-269
37. Pezzone MA, Watkins SC, Alber SM, King WE, de Groat WC, Chancellor MB, Fraser MO (2003) Identification of c-kitpositive cells in the mouse ureter: the interstitial cells of Cajal of the urinary tract. Am J Physiol Ren Physiol 284:F925-F929
38. Rhee PL, Lee JY, Son HJ, Kim JJ, Rhee JC, Kim S, Koh SD, Hwang SJ, Sanders KM, Ward SM (2011) Analysis of pacemaker activity in the human stomach. J Physiol 589:6105-6118
39. Rumessen JJ (1994) Identification of interstitial cells of Cajal. Significance for studies of human small intestine and colon. Dan Med Bull 41:275-293
40. Sanders KM (1996) A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 111:492-515
41. Sanders KM, Stevens R, Burke E, Ward SW (1990) Slow waves actively propagate at submucosal surface of circular layer in canine colon. Am J Physiol 259:G258-G263
42. Schroeder BC, Cheng T, Jan YN, Jan LY (2008) Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134:1019-1029
43. Sergeant GP, Thornbury KD, McHale NG, Hollywood MA (2006) Interstitial cells of Cajal in the urethra. J Cell Mol Med 10:280-291
44. Silverman AJ, Sutherland AK, Wilhelm M, Silver R (2000) Mast cells migrate from blood to brain. J Neurosci 20:401-408
45. Song G, David G, Hirst S, Sanders KM, Ward SM (2005) Regional variation in ICC distribution, pacemaking activity and neural responses in the longitudinal muscle of the murine stomach. J Physiol 564:523-540
46. Strege PR, Ou Y, Sha L, Rich A, Gibbons SJ, Szurszewski JH, Sarr MG, Farrugia G (2003) Sodium current in human intestinal interstitial cells of Cajal. Am J Physiol Gastrointest Liver Physiol 285: G1111-G1121
47. Thuneberg L (1982) Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol 71:1-130
48. Torihashi S, Ward SM, Nishikawa S, Nishi K, Kobayashi S, Sanders KM (1995) c-kit-dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract. Cell Tissue Res 280:97-111
49. Torihashi S, Ward SM, Sanders KM (1997) Development of c-Kitpositive cells and the onset of electrical rhythmicity in murine small intestine. Gastroenterology 112:144-155
50. Vanderwinden JM (1999) Role of Interstitial Cells of Cajal and their relationship with the enteric nervous system. Eur J Morphol 37:250-256
51. Vanderwinden JM, Liu H, Menu R, Conreur JL, De Laet MH, Vanderhaeghen JJ (1996) The pathology of infantile hypertrophic pyloric stenosis after healing. J Pediatr Surg 31:1530-1534
52. Ward SM, Burns AJ, Torihashi S, Sanders KM (1994) Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J Physiol 480(Pt 1):91-97
53. Ward SM, Burns AJ, Torihashi S, Harney SC, Sanders KM (1995) Impaired development of interstitial cells and intestinal electrical rhythmicity in steel mutants. Am J Physiol 269:C1577-C1585
54. Ward SM, Morris G, Reese L, Wang XY, Sanders KM (1998) Interstitial cells of Cajal mediate enteric inhibitory neurotransmission in the lower esophageal and pyloric sphincters. Gastroenterology 115:314-329
55. Ward SM, Beckett EA, Wang X, Baker F, Khoyi M, Sanders KM (2000) Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motor neurons. J Neurosci 20:1393-1403
56. Won KJ, Sanders KM, Ward SM (2005) Interstitial cells of Cajal mediate mechanosensitive responses in the stomach. Proc Natl Acad Sci USA 102:14913-14918
57. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, Raouf R, Shin YK, Oh U (2008) TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:1210-1215
58. Yun HY, Sung R, Kim YC, Choi W, Kim HS, Kim H, Lee GJ, You RY, Park SM, Yun SJ, Kim MJ, Kim WS, Song YJ, Xu WX, Lee SJ (2010) Regional Distribution of Interstitial Cells of Cajal (ICC) in Human Stomach. Korean J Physiol Pharmacol 14:317-324
59. Zhu MH, Kim TW, Ro S, Yan W, Ward SM, Koh SD, Sanders KM (2009) A Ca(2+)-activated Cl(-) conductance in interstitial cells of Cajal linked to slow wave currents and pacemaker activity. J Physiol 587:4905-4918
60. Zhu MH, Sung IK, Zheng H, Sung TS, Britton FC, O'Driscoll K, Koh SD, Sanders KM (2011) Muscarinic activation of Ca2 + -activated Cl-current in interstitial cells of Cajal. J Physiol 589:4565-4582