Late embryonic and postnatal development of interstitial cells of cajal in mouse esophagus: Distribution, proliferation and kit dependence

Cells Tissues Organs

Volumn 196, Issue 2, 2012, Pages 175-188

  He, Xiao ^a   Yang, Wen Cui ^a   Wen, Xiang Yin ^a   Tang, Di ^a   Xiao, Lan ^a   Han, Juan ^b   Yu, Bin ^a   Zhang, Wei ^a   Mei, Feng ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b People's Liberation Army Hospital   (China)

Author keywords

Bromodeoxyuridine; Esophageal model; Interstitial cells of Cajal; Ki67; Kit; Postnatal development; Proliferation

Indexed keywords

BROXURIDINE; IMATINIB; STEM CELL FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; COLONY FORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ESOPHAGUS; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELL OF CAJAL; MOUSE; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; SMOOTH MUSCLE FIBER; SPINDLE CELL;

ANIMALS; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; ESOPHAGUS; HUMANS; INTERSTITIAL CELLS OF CAJAL; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; PROTO-ONCOGENE PROTEINS C-KIT; SIGNAL TRANSDUCTION;

MUS;

EID: 84863526662     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000332381     Document Type: Article

References (61)

1. Beckett, E.A., S. Ro, Y. Bayguinov, K.M. Sanders, S.M. Ward (2007) Kit signaling is essential for development and maintenance of interstitial cells of Cajal and electrical rhythmicity in the embryonic gastrointestinal tract. Dev Dyn 236: 60-72. (Pubitemid 46095079)
2. Berezin, I., E.E. Daniel, J.D. Huizinga (1994) Ultrastructure of interstitial cells of Cajal in the canine distal esophagus. Can J Physiol Pharmacol 72: 1049-1059. (Pubitemid 24364489)
3. Burns, A.J., T.M. Herbert, S.M. Ward, K.M. Sanders (1997) Interstitial cells of Cajal in the guinea-pig gastrointestinal tract as revealed by c-Kit immunohistochemistry. Cell Tissue Res 290: 11-20. (Pubitemid 27460120)
4. Daniel, E.E., V. Posey-Daniel (1984) Neuromuscular structures in opossum esophagus: role of interstitial cells of Cajal. Am J Physiol 246: G305-G315. (Pubitemid 14121789)
5. Farre, R., X.Y. Wang, E. Vidal, A. Domenech, M. Pumarola, P. Clave, J.D. Huizinga, M. Jimenez (2007) Interstitial cells of Cajal and neuromuscular transmission in the rat lower oesophageal sphincter. Neurogastroenterol Motil 19: 484-496. (Pubitemid 46905391)
6. Faussone-Pellegrini, M.S., C. Cortesini (1985) Ultrastructural features and localization of the interstitial cells of Cajal in the smooth muscle coat of human esophagus. J Submicrosc Cytol 17: 187-197. (Pubitemid 15101753)
7. Faussone-Pellegrini, M.S., D. Pantalone, C. Cortesini (1990) Smooth muscle cells, interstitial cells of Cajal and myenteric plexus interrelationships in the human colon. Acta Anat (Basel) 139: 31-44. (Pubitemid 20330946)
8. Fox, E.A., R.J. Phillips, M.S. Byerly, E.A. Baronowsky, M.M. Chi, T.L. Powley (2002) Selective loss of vagal intramuscular mechanoreceptors in mice mutant for steel factor, the c-Kit receptor ligand. Anat Embryol (Berl) 205: 325-342. (Pubitemid 34824174)
9. Gomez-Pinilla, P.J., S.J. Gibbons, M.R. Bardsley, A. Lorincz, M.J. Pozo, P.J. Pasricha (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.
10. Han, J., W.H. Shen, Y.Z. Jiang, B. Yu, Y.T. He, N. Li, F. Mei (2010a) Distribution, development and proliferation of interstitial cells of Cajal in murine colon: an immunohistochemical study from neonatal to adult life. Histochem Cell Biol 133: 163-175.
11. Han, J., Y.P. Zhou, Y.Z. Jiang, Y.T. He, F. Mei (2010b) Postnatal development of interstitial cells of Cajal in mouse colon in response to Kit signal blockade with imatinib (Glivec). Acta Histochem 112: 215-221.
12. Horiguchi, K., G.S. Semple, K.M. Sanders, S.M. Ward (2001) Distribution of pacemaker function through the tunica muscularis of the canine gastric antrum. J Physiol 537: 237-250. (Pubitemid 33076970)
13. Horisawa, M., Y. Watanabe, S. Torihashi (1998) Distribution of c-Kit immunopositive cells in normal human colon and in Hirsch-sprung's disease. J Pediatr Surg 33: 1209-1214. (Pubitemid 28384802)
14. Horvath, V.J., H. Vittal, A. Lorincz, H. Chen, G. Meida-Porada, D. Redelman, T. Ordog (2006) Reduced stem cell factor links smooth myopathy and loss of interstitial cells of Cajal in murine diabetic gastroparesis. Gastroenterology 130: 759-770. (Pubitemid 43374526)
15. Huizinga, J.D., D.E. Reed, I. Berezin, X.Y. Wang, D.T. Valdez, L.W. Liu, N.E. Diamant (2008) Survival dependency of intramuscular ICC on vagal afferent nerves in the cat esophagus. Am J Physiol Regul Integr Comp Physiol 294: R302-R310. (Pubitemid 351213734)
16. Huizinga, J.D., L. Thuneberg, M. Kluppel, J. Malysz, H.B. Mikkelsen, A. Bernstein (1995) W/Kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 373: 347-349.
17. Huizinga, J.D., E.J. White (2008) Progenitor cells of interstitial cells of Cajal: on the road to tissue repair. Gastroenterology 134: 1252-1254. (Pubitemid 351452017)
18. Kallmunzer, B., B. Sorensen, W.L. Neuhuber, J. Worl (2008) Enteric co-innervation of striated muscle fibres in human oesophagus. Neurogastroenterol.Motil 20: 597-610. (Pubitemid 351678615)
19. Katori, Y., B.H. Cho, C.H. Song, M. Fujimiya, G. Murakami, T. Kawase (2010) Smooth-tostriated muscle transition in human esophagus: an immunohistochemical study using fetal and adult materials. Ann Anat 192 : 33-41
20. Kluppel, M., J.D. Huizinga, J. Malysz, A. Bernstein (1998) Developmental origin and Kitdependent development of the interstitial cells of Cajal in the mammalian small intestine. Dev Dyn 211: 60-71. (Pubitemid 28035812)
21. Lecoin, L., G. Gabella, N. Le Douarin (1996) Origin of the c-kit-positive interstitial cells in the avian bowel. Development 122: 725-733. (Pubitemid 26095978)
22. Lin, L., L.M. Xu, W. Zhang, Y.B. Ge, Y.R. Tang, H.J. Zhang, X.L. Li, J.D. Chen (2010) Roles of stem cell factor on the depletion of interstitial cells of Cajal in the colon of diabetic mice. Am J Physiol Gastrointest Liver Physiol 298 : G241-G247.
23. Liu, L.W., J.D. Huizinga (1994) Canine colonic circular muscle generates action potentials without the pacemaker component. Can J Physiol Pharmaco l 72 : 70-81. (Pubitemid 24131038)
24. Lorincz, A., D. Redelman, V.J. Horvath, M.R. Bardsley, H. Chen, T. Ordog (2008) Progenitors of interstitial cells of Cajal in the postnatal murine stomach. Gastroenterology 134: 1083-1093. (Pubitemid 351451982)
25. Maeda, H., A. Yamagata, S. Nishikawa, K. Yoshinaga, S. Kobayashi, K. Nishi, S. Nishikawa (1992) Requirement of c-kit for development of intestinal pacemaker system. Development 116: 369-375.
26. Mei, F., S. Guo, Y.T. He, J. Zhu, D.S. Zhou, J.Q. Niu, H.Z. Wang, Y.P. Tian (2009a) Apoptosis of interstitial cells of Cajal, smooth muscle cells, and enteric neurons induced by intestinal ischemia and reperfusion injury in adult guinea pigs. Virchows Arch 454: 401-409.
27. Mei, F., J. Han, Y. Huang, Z.Y. Jiang, C.J. Xiong, D.S. Zhou (2009b) Plasticity of interstitial cells of Cajal: a study in the small intestine of adult guinea pigs. Anat Rec (Hoboken) 292: 985-993.
28. Mei, F., J. Zhu, S. Guo, D.S. Zhou, J. Han, B. Yu, S.F. Li, Z.Y. Jiang, C.J. Xiong (2009c) An agedependent proliferation is involved in the postnatal development of interstitial cells of Cajal in the small intestine of mice. Histochem Cell Biol 131: 43-53.
29. Mikkelsen, H.B., J. Malysz, J.D. Huizinga, L. Thuneberg (1998) Action potential generation, Kit receptor immunohistochemistry and morphology of steel-Dickie (Sl/Sld) mutant mouse small intestine. Neurogastroenterol Motil 10: 11-26. (Pubitemid 28056788)
30. Nakagawa, T., H. Misawa, Y. Nakajima, M. Takaki (2005) Absence of peristalsis in the ileum of W/W(V) mutant mice that are selectively deficient in myenteric interstitial cells of Cajal. J Smooth Muscle Res 41: 141-151. (Pubitemid 41373394)
31. Nakama, A., S. Hirota, T. Okazaki, K. Nagano, S. Kawano, M. Hori, Y. Kitamura (1998) Disturbed pyloric motility in Ws/Ws mutant rats due to deficiency of c-kit-expressing interstitial cells of Cajal. Pathol Int 48 : 843-849. (Pubitemid 28512073)
32. Ohta, Y., K. Ichimura (2000) Proliferation markers, proliferating cell nuclear antigen, Ki67, 5-bromo-2-deoxyuridine, and cyclin D1 in mouse olfactory epithelium. Ann Otol Rhinol Laryngol 109: 1046-1048.
33. Ordog, T., S.M. Ward, K.M. Sanders (1999) Interstitial cells of Cajal generate electrical slow waves in the murine stomach. J Physiol 518: 257-269. (Pubitemid 29332970)
34. Patapoutian, A., B.J. Wold, R.A. Wagner (1995) Evidence for developmentally programmed transdifferentiation in mouse esophageal muscle. Science 270 : 1818-1821. (Pubitemid 26007228)
35. Radenkovic, G., I. Ilic, D. Zivanovic, S. Vlajkovic, V. Petrovic, O. Mitrovic (2010) C-kit-immunopositive interstitial cells of Cajal in human embryonal and fetal oesophagus. Cell Tissue Res 340: 427-436.
36. Rishniw, M., P.J. Fisher, R.M. Doran, S.P. Bliss, M.I. Kotlikoff (2009) Striated myogenesis and peristalsis in the fetal murine esophagus occur without cell migration or interstitial cells of Cajal. Cells Tissues Organs 189: 410-419.
37. Rishniw, M., P.W. Fisher, R.M. Doran, E. Meadows, W.H. Klein, M.I. Kotlikoff (2007) Smooth muscle persists in the muscularis externa of developing and adult mouse esophagus. J Muscle Res Cell Motil 28: 153-165. (Pubitemid 47434729)
38. Rishniw, M., H.B. Xin, K.Y. Deng, M.I. Kotlikoff (2003) Skeletal myogenesis in the mouse esophagus does not occur through transdifferentiation. Genesis 36: 81-82. (Pubitemid 36818666)
39. Rumessen, J.J., A. Kerchove, S. Mignon, F. Bernex, J.P. Timmermans, S.N. Schiffmann, J.J. Panthier, J.M. Vanderwinden (2001) Interstitial cells of Cajal in the striated musculature of the mouse esophagus. Cell Tissue Res 306: 1-14. (Pubitemid 32905593)
40. Rumessen, J.J., L. Thuneberg (1996) Pacemaker cells in the gastrointestinal tract: interstitial cells of Cajal. Scand J Gastroenterol 216(suppl): 82-94. (Pubitemid 26130549)
41. Sanders, K.M. (1996) A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 111: 492-515. (Pubitemid 26256739)
42. Sanders, K.M., S.M. Ward (2007) Kit mutants and gastrointestinal physiology. J Physiol 578: 33-42. (Pubitemid 44971108)
43. Sang, Q., H.M. Young (1997) Development of nicotinic receptor clusters and innervation accompanying the change in muscle phenotype in the mouse esophagus. J Comp Neurol 386: 119-136. (Pubitemid 27392146)
44. Serio, R., C. Barajas-Lopez, E.E. Daniel, I. Berezin, J.D. Huizinga (1991) Slow-wave activity in colon: role of network of submucosal interstitial cells of Cajal. Am J Physiol 260: G636-G645.
45. Shimojima, N., T. Nakaki, Y. Morikawa, K. Hoshino, M. Kitajima (2005) Imatinib blocks spontaneous mechanical activities in the adult mouse small intestine: possible inhibition of c-Kit signaling. Pharmacology 74: 95-99. (Pubitemid 40827591)
46. Sperelakis, N., E.E. Daniel (2004) Activation of intestinal smooth muscle cells by interstitial cells of Cajal in simulation studies. Am J Physiol Gastrointest Liver Physiol 286 : G234-G243. (Pubitemid 38134034)
47. Stratton, C.J., Y. Bayguinov, K.M. Sanders, S.M. Ward (2000) Ultrastructural analysis of the transdifferentiation of smooth muscle to skeletal muscle in the murine esophagus. Cell Tissue Res 301: 283-298. (Pubitemid 30601561)
48. Tharayil, V.S., M.M. Wouters, J.E. Stanich, et al. (2010) Lack of serotonin 5-HT2B receptor alters proliferation and network volume of interstitial cells of Cajal in vivo. Neurogastroenterol Motil 22: 462-410.
49. Thuneberg, L. (1999) One hundred years of interstitial cells of Cajal. Microsc Res Tech 47: 223-238.
50. Torihashi, S., M. Horisawa, Y. Watanabe (1999a) c-Kit immunoreactive interstitial cells in the human gastrointestinal tract. J Auton Nerv Syst 75: 38-50. (Pubitemid 29034710)
51. Torihashi, S., K. Nishi, Y. Tokutomi, T. Nishi, S. Ward, K.M. Sanders (1999b) Blockade of kit signaling induces transdifferentiation of interstitial cells of Cajal to a smooth muscle phenotype. Gastroenterology 117: 140-148. (Pubitemid 29297630)
52. Torihashi, S., S.M. Ward, K.M. Sanders (1997) Development of c-Kit-positive cells and the onset of electrical rhythmicity in murine small intestine. Gastroenterology 112: 144-155. (Pubitemid 27008996)
53. Ward, S.M., A.J. Burns, S. Torihashi, S.C. Harney, K.M. Sanders (1995) Impaired development of interstitial cells and intestinal electrical rhythmicity in steel mutants. Am J Physiol 269: C1577-C1585.
54. Ward, S.M., A.J. Burns, S. Torihashi, K.M. Sanders (1994) Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J Physiol 480: 91-97. (Pubitemid 24310002)
55. Ward, S.M., G. Morris, L. Reese, X.Y. Wang, K.M. Sanders (1998) Interstitial cells of Cajal mediate enteric inhibitory neurotransmission in the lower esophageal and pyloric sphincters. Gastroenterology 115: 314-329. (Pubitemid 28363424)
56. Ward, S.M., K.M. Sanders (2001) Physiology and pathophysiology of the interstitial cell of Cajal: from bench to bedside. I. Functional development and plasticity of interstitial cells of Cajal networks. Am J Physiol Gastrointest Liver Physiol 281: G602-G611.
57. Wong, W.C., S.H. Tan, T.Y. Yick, E.A. Ling (1990) Ultrastructure of interstitial cells of Cajal at the gastro-oesophageal junction of the monkey (Macaca fascicularis). Acta Anat (Basel) 138: 318-326. (Pubitemid 20251616)
58. Wu, J.J., T.P. Rothman, M.D. Gershon (2000) Development of the interstitial cell of Cajal: origin, kit dependence and neuronal and nonneuronal sources of kit ligand. J Neurosci Res 59: 384-401. (Pubitemid 30107979)
59. Young, H.M. (1999) Embryological origin of interstitial cells of Cajal. Microsc Res Tech 47: 303-308.
60. Young, H.M., D. Ciampoli, B.R. Southwell, D.F. Newgreen (1996) Origin of interstitial cells of Cajal in the mouse intestine. Dev Biol 180: 97-107. (Pubitemid 26426161)
61. Zhou, D.S., J. Desaki, T. Komuro (1996) Neuromuscular junctions of longitudinal and circular muscle fibers of the guinea-pig esophagus and their relation to myenteric plexus. J Auton Nerv Syst 58: 63-68. (Pubitemid 26148600)