Interstitial cells of Cajal: Pathology, injury and repair

Sultan Qaboos University Medical Journal

Volumn 12, Issue 4, 2012, Pages 411-421

  Al Sajee, Dhuha ^a   Huizinga, Jan D ^b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Ageing; C kit; Cajal interstitial cells; Diabetes mellitus; Gastrointestinal stromal tumors; Gastrointestinal tract

Indexed keywords

EID: 84870677547     PISSN: 2075051X     EISSN: 20750528     Source Type: Journal    
DOI: 10.12816/0003165     Document Type: Review

References (56)

1. Kluppel MJ, Huizinga JD, Malysz J, Bernstein A. Developmental origin and kit-dependent development of the interstitial cells of Cajal in the mammalian small intestine. Devel Dynamics 1998; 211:60-71.
2. Komuro T. Comparative morphology of interstitial cells of Cajal: Ultrastructural characterization. Microsc Res Tech 1999; 47:267-85.
3. Ordög T. Interstitial cells of Cajal in diabetic gastroenteropathy. Neurogastroenterol Motil 2008; 20:8-18.
4. Ward SM, Burns AJ, Torihashi S, Sanders KM. Mutation of the protooncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J Physiol (Lond) 1994; 480:91-7.
5. Huizinga JD, Thuneberg L, Kluppel M, Malysz J, Mikkelsen HB, Bernstein A. W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 1995; 373:347-9.
6. Wu JJ, Rothman TP, Gershon MD. Development of the interstitial cells of Cajal: Origin, kit dependence and neuronal and nonneuronal sources of kit ligand. J Neurosci Res 2000; 59:384-401.
7. Horvath VJ, Vittal H, Ordög T. Reduced insulin and IGF-I signaling, not hyperglycemia, underlies the diabetes-associated depletion of interstitial cells of Cajal in the murine stomach. Diabetes 2005; 54:1528-33.
8. Ward SM, Ordög T, Bayguinov JR, Horowitz B, Epperson A, Shen L, et al. Development of interstitial cells of Cajal and pacemaking in mice lacking enteric nerves. Gastroenterology 1999; 117:584-94.
9. Ordög T, Takayama I, Cheung WK, Ward SM, Sanders KM. Remodeling of networks of interstitial cells of Cajal in a murine model of diabetic gastroparesis. Diabetes 2000; 49:1731-9.
10. Huizinga JD, Zarate N, Farrugia G. Physiology, injury, and recovery of interstitial cells of Cajal: Basic and clinical science. Gastroenterology 2009; 137:1548-56.
11. Wang XY, Zarate N, Soderholm JD, Bourgeois JM, Liu LW, Huizinga JD. Ultrastructural injury to interstitial cells of Cajal and communication with mast cells in Crohn's disease. Neurogastroenterol Motil 2007; 19:349-64.
12. Bardsley MR, Horváth VJ, Asuzu DT, Lorincz A, Redelman D, Hayashi Y, et al. Kitlow stem cells cause resistance to Kit/platelet-derived growth factor alpha inhibitors in murine gastrointestinal stromal tumors. Gastroenterology 2010; 139:942-52.
13. 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.
14. Kashyap P, Farrugia G. Diabetic gastroparesis: What we have learned and had to unlearn in the past five years. Gut 2010; 59:1716-26.
15. 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.
16. Zarate N, Wang XY, Tougas G, Anvari M, Birch D, Mearin F, et al. Intramuscular interstitial cells of Cajal associated with mast cells survive nitrergic nerves in achalasia. Neurogastroenterol Motil 2006; 18:556-68.
17. Sanders KM, Zhu MH, Britton FC, Koh SD, Ward SM. Anoctamins and gastrointestinal smooth muscle excitability. Exp Physiol 2012; 97:200-6.
18. Komuro T. Structure and organization of interstitial cells of Cajal in the gastrointestinal tract. J Physiol 2006; 576:653-8.
19. Komuro T, Seki K, Horiguchi K. Ultrastructural characterization of the interstitial cells of Cajal. Arch Histol Cytol 1999; 62:295-316.
20. Yuzawa S, Opatowsky Y, Zhang Z, Mandiyan V, Lax I, Schlessinger J. Structural basis for activation of the receptor tyrosine kinase KIT by stem cell factor. Cell 2007; 130:323-4.
21. Liu H, Chen X, Focia PJ, He X. Structural basis for stem cell factor-KIT signaling and activation of class III receptor tyrosine kinases. EMBO J 2007; 26:891-901.
22. You M, Yu DH, Feng GS. She-2 tyroisne phosphatase functions as a negative regulator of the interferon stimulated Jak//STAT pathway. Mol Cell Biol 1999; 19:2416-24.
23. Hwang SJ, Blair PJ, Britton FC, O'Driscoll KE, Hennig G, Bayguinov YR, et al. Expression of anoctamin 1/ TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles. J Physiol 2009; 587:4887-904.
24. Robinson TL, Sincar K, Hewlett BR, Chornevko K, Riddell RH, Huizinga JD. Gastrointestinal stromal tumors may originate from a subset of CD34-positive interstitial cells of Cajal. Am J Pathol 2000; 156:1157-63.
25. Lornicz A, Redelman D, Horvath VJ, Bardsley MR, Chen H, Ordög T. Progenitors of interstitial cells of Cajal in postnatal murine stomach. Gastroenterology 2008; 1053:1083-93.
26. Vanderwinden JM, Rumessen JJ, De Laet MH, Vanderhaeghen JJ, Schiffmann SN. CD34 immunoreactivity and interstitial cells of Cajal in the human and mouse gastrointestinal tract. Cell Tissue Res 2000; 302:145-53.
27. Yu B, Han J, He YT, Guo S, Li SF, Mei F. Immunohistochemical study of CD44 immunopositive cells in the muscular layers of the gastrointestinal tract in adult guinea pigs and mice. Acta Histochem 2009; 111:382-90.
28. Sanders KM, Ordög T, Koh SD, Torihashi S, Ward SM. Development and plasticity of interstitial cells of Cajal. Neurogastroenterol Motil 1999; 11:311-38.
29. Young HM. Embryological origin of interstitial cells of Cajal. Microsc Res Tech 1999; 47:303-8.
30. de Paulis A, Minopoli G, Arbustini E, de Crescenzo G, Dal Piaz F, Pucci P, et al. Stem cell factor is localized in, released from, and cleaved by human mast cells. J Immunol 1999; 163:2799-808.
31. Faussone-Pellegrini MS. Cytodifferentiation of the interstitial cells of Cajal related to the myenteric plexus of mouse intestinal muscle coat. An E.M. study from foetal to adult life. Anat Embryol (Berl) 1985; 171:163-9.
32. Wang XY, Huizinga J, Diamond J, Liu L. Loss of intramuscular and submuscular ICC and associated enteric nerves is related to decreased gastric emptying in streptozotocin-induced diabetes. Neurogastroenterol Motil 2009; 21:1095-e92.
33. Horiguchi K, Komuro T. Ultrastructural observations of fibroblast-like cells forming gap junctions in the W/W (nu) mouse small intestine. J Auton Nerv Syst 2000; 80:142-7.
34. Lammers WJ, Al-Bloushi HM, Al-Eisaei SA, AlDhaheri FA, Stephen B, John R, et al. Slow wave propagation and plasticity of interstitial cells of Cajal in the small intestine of diabetic rats. Exp Physiol 2011; 96:1039-48.
35. Lin L, Xu LM, Zhang W, Ge YB, Tang YR, Zhang HJ, et al. 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 2010; 298:G241-7.
36. Gomez-Pinilla PJ, Gibbons SJ, Sarr MG, Kendrick ML, Shen KR, Cima RR, et al. Changes in interstitial cells of Cajal with age in the human stomach and colon. Neurogastroenterol Motil 2011; 23:36-44.
37. Choi KM, Gibbons SJ, Nguyen TV, Stoltz GJ, Lurken MS, Ordög T, et al. Heme oxygenase-1 protects interstitial cells of Cajal from oxidative stress and reverses diabetic gastroparesis. Gastroenterology 2008; 135:2055-64.
38. Grover M, Farrugia G, Lurken MS, Bernard CE, Faussone-Pellegrini MS, Smyrk TC, et al. NIDDK Gastroparesis Clinical Research Consortium: Cellular changes in diabetic and idiopathic gastroparesis. Gastroenterology 2011; 140:1575-85.
39. Faussone-Pellegrini MS, Grover M, Pasricha P, Bernard C, Lurken M, Smyrk T, Parkman H, et al. Ultrastructural differences between diabetic and idiopathic gastroparesis: The NIDDK gastroparesis clinical research consortium (GpCRC). J Cell Mol Med 2012; 16:1573-81.
40. Wang XY, Berezin I, Mikkelsen HB, Der T, Bercik P, Collins SM, et al. Pathology of interstitial cells of Cajal in relation to inflammation revealed by ultrastructure but not immunohistochemistry. Am J Pathol 2002; 160:1529-40.
41. Chang IY, Glasgow NJ, Takayama I, Horiguchi K, Sanders KM, Ward SM. Loss of interstitial cells of Cajal and development of electrical dysfunction in murine small bowel obstruction. J Physiol 2001; 536:555-68.
42. Mikkelsen HB. ICC, macrophages and mast cells in the gut musculature: Morphology, distribution, spatial and possible functional interaction. J Cell Mol Med 2010; 14:818-32.
43. Yanagida H, Yanase H, Sanders KM, Ward SM. Intestinal surgical resection disrupts electrical rhythmicity, neural responses, and interstitial cell networks. Gastroenterology 2004; 127:1748-59.
44. Asuzu DT, Hayashi Y, Bardsley MR, Farrugia G, Ordög T. Persistent β-catenin activation underlies senescence of interstitial cell of Cajal (ICC) stem cells in naturally aging mice. Gastroenterology 2011; 140:S-139.
45. Kindblom LG, Remotti HE, Alsenborg F, MeisKindblom JM. Gastrointestinal pacemaker cell tumor (GIPACT): Gastrointestinal stromal tumors show phenotypic characteristics of the interstitial cells of Cajal. Am J Pathol 1998; 152:1259-69.
46. Izbeki F, Asuzu DT, Lorincz A, Bardsley MR, Popko LN, Choi KM, et al. Loss of Kitlow progenitors, reduced stem cell factor, and high oxidative stress underlie gastric dysfunction in progeric mice. J Physiol 2010; 15:3101-17.
47. Kuro-o M. Klotho and the aging process. Korean J Intern Med 2011; 26:113-22.
48. Katoh M. WNT signaling in stem cell biology and regenerative medicine. Curr Drug Targets 2008; 9:565-70.
49. Gibbons SJ, De Giorgio R, Pellegrini MS, GarrityPark MM, Miller SM, Schmalz PF, et al. Apoptotic cell death of human interstitial cells of Cajal. Neurogastroenterol Motil 2009; 21:85-93.
50. Sircar K, Hewlett BR, Huizinga JD, Chornevok K, Berezin I, Riddell RH. Interstitial cells of Cajal as precursors of gastrointestinal stromal tumors. Am J Surg Path 1999; 23:377-89.
51. Wong NA. Gastrointestinal stromal tumours-an update for histopathologists. Histopathology 2011; 59:807-21.
52. Mazur MT, Clark HB: Gatric Stroma Tumors: Reappraisal of histogenesis. Am J Surg Pathol 1983; 7:507-19.
53. Kitamura Y. Gastrointestinal stromal tumors: Past, present, and future. J Gastroenterol 2008, 43:499-508.
54. West RB, Corless CL, Chen X, Rubin BP, Subramanian S, Montgomery K, et al. The novel marker, DOG1, is expressed ubiquitously in gastrointestinal stromal tumors irrespective of KIT or PDGFRA mutation status. Am J Pathol 2004; 165:107-13.
55. Rossi G, Valli R, Bertolini F, Marchioni A, Cavazza A, Mucciarini C, et al. PDGFR expression in differential diagnosis between KIT-negative gastrointestinal stromal tumours and other primary soft-tissue tumours of the gastrointestinal tract. Histopathology 2005; 46:522-31.
56. Asuzu DT, McGehee CD, Hayashi Y, Bardsley MR, Grzenda AL, Lomberk GA, et al. Epigenetic control of Kit expression in murine Kitlow interstitial cell of Cajal (ICC) stem cells and gastrointestinal stromal tumors (GIST). Gastroenterology 2011; 140:S119-120.