Regulation of interstitial cells of Cajal in the mouse gastric body by neuronal nitric oxide

Neurogastroenterology and Motility

Volumn 19, Issue 7, 2007, Pages 585-595

  Choi, K M ^a   Gibbons, S J ^a   Roeder, J L ^a   Lurken, M S ^a   Zhu, J ^a   Wouters, M M ^a   Miller, S M ^a   Szurszewski, J H ^a   Farrugia, G ^a  

^a MAYO CLINIC   (United States)

Author keywords

Gastrointestinal tract; Stomach; Survival

Indexed keywords

N ACETYL S NITROSOPENICILLAMINE; N(G) NITROARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; STEM CELL FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL CULTURE; CELL SURVIVAL; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELL OF CAJAL; LASER MICROSCOPY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE; STOMACH; THREE DIMENSIONAL IMAGING;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; ENTERIC NERVOUS SYSTEM; ENZYME INHIBITORS; FEMALE; IMMUNOHISTOCHEMISTRY; INTESTINE, SMALL; MICE; MICE, INBRED STRAINS; MICE, MUTANT STRAINS; MUSCLE, SMOOTH; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE I; NITROARGININE; ORGAN CULTURE TECHNIQUES; PROTO-ONCOGENE PROTEINS C-KIT; S-NITROSO-N-ACETYLPENICILLAMINE; STOMACH;

EID: 34250862734     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2007.00936.x     Document Type: Article

References (56)

1. Der-Silaphet T, Malysz J, Hagel S, Larry Arsenault A, Huizinga JD. Interstitial cells of cajal direct normal propulsive contractile activity in the mouse small intestine. Gastroenterology 1998 114 : 724 36.
2. 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 (Pt 1 91 7.
3. 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.
4. Farrugia G, Lei S, Lin X et al. A major role for carbon monoxide as an endogenous hyperpolarizing factor in the gastrointestinal tract. Proc Natl Acad Sci U S A 2003 100 : 8567 70.
5. Strege PR, Ou Y, Sha L et al. Sodium current in human intestinal interstitial cells of Cajal. Am J Physiol Gastrointest Liver Physiol 2003 285 : G1111 21.
6. Won KJ, Sanders KM, Ward SM. Interstitial cells of Cajal mediate mechanosensitive responses in the stomach. Proc Natl Acad Sci U S A 2005 102 : 14913 8.
7. Burns AJ, Lomax AE, Torihashi S, Sanders KM, Ward SM. Interstitial cells of Cajal mediate inhibitory neurotransmission in the stomach. Proc Natl Acad Sci U S A 1996 93 : 12008 13.
8. He CL, Burgart L, Wang L et al. Decreased interstitial cell of cajal volume in patients with slow-transit constipation. Gastroenterology 2000 118 : 14 21.
9. Lyford GL, He CL, Soffer E et al. Pan-colonic decrease in interstitial cells of Cajal in patients with slow transit constipation. Gut 2002 51 : 496 501.
10. Kenny SE, Vanderwinden JM, Rintala RJ et al. Delayed maturation of the interstitial cells of Cajal: a new diagnosis for transient neonatal pseudoobstruction. Report of two cases. J Pediatr Surg 1998 33 : 94 8.
11. Vanderwinden JM, Rumessen JJ. Interstitial cells of Cajal in human gut and gastrointestinal disease. Microsc Res Tech 1999 47 : 344 60.
12. Feldstein AE, Miller SM, El-Youssef M et al. Chronic intestinal pseudoobstruction associated with altered interstitial cells of cajal networks. J Pediatr Gastroenterol Nutr 2003 36 : 492 7.
13. He CL, Soffer EE, Ferris CD, Walsh RM, Szurszewski JH, Farrugia G. Loss of interstitial cells of cajal and inhibitory innervation in insulin-dependent diabetes. Gastroenterology 2001 121 : 427 34.
14. Burns AJ, Herbert TM, Ward SM, Sanders KM. Interstitial cells of Cajal in the guinea-pig gastrointestinal tract as revealed by c-Kit immunohistochemistry. Cell Tissue Res 1997 290 : 11 20.
15. Rich A, Miller SM, Gibbons SJ, Malysz J, Szurszewski JH, Farrugia G. Local presentation of Steel factor increases expression of c-kit immunoreactive interstitial cells of Cajal in culture. Am J Physiol Gastrointest Liver Physiol 2003 284 : G313 20.
16. Maeda H, Yamagata A, Nishikawa S, Yoshinaga K, Kobayashi S, Nishi K. Requirement of c-kit for development of intestinal pacemaker system. Development 1992 116 : 369 75.
17. 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.
18. Daniel EE, Posey-Daniel V. Neuromuscular structures in opossum esophagus: role of interstitial cells of Cajal. Am J Physiol 1984 246 : G305 15.
19. Horisawa M, Watanabe Y, Torihashi S. Distribution of c-Kit immunopositive cells in normal human colon and in Hirschsprung's disease. J Pediatr Surg 1998 33 : 1209 14.
20. Wedel T, Spiegler J, Soellner S et al. Enteric nerves and interstitial cells of Cajal are altered in patients with slow-transit constipation and megacolon. Gastroenterology 2002 123 : 1459 67.
21. Vanderwinden JM, Liu H, Menu R, Conreur JL, De Laet MH, Vanderhaeghen JJ. The pathology of infantile hypertrophic pyloric stenosis after healing. J Pediatr Surg 1996 31 : 1530 4.
22. Watkins CC, Sawa A, Jaffrey S et al. Insulin restores neuronal nitric oxide synthase expression and function that is lost in diabetic gastropathy. J Clin Invest 2000 106 : 373 84.
23. Ordog 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.
24. Stark ME, Szurszewski JH. Role of nitric oxide in gastrointestinal and hepatic function and disease. Gastroenterology 1992 103 : 1928 49.
25. Kroncke KD, Fehsel K, Kolb-Bachofen V. Nitric oxide: cytotoxicity versus cytoprotection - how, why, when, and where Nitric Oxide 1997 1 : 107 20.
26. Stamler JS. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 1994 78 : 931 6.
27. Andoh T, Lee SY, Chiueh CC. Preconditioning regulation of bcl-2 and p66shc by human NOS1 enhances tolerance to oxidative stress. FASEB J 2000 14 : 2144 6.
28. Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 1993 75 : 1273 86.
29. Choi KM, Gibbons SJ, Lurken MS et al. Loss of neuronal nitric oxide synthase results in altered volume and distribution of interstitial cells of Cajal in mouse stomach. Neurogastroenterol Motil 2005 17 : 612, A33.
30. Mashimo H, Kjellin A, Goyal RK. Gastric stasis in neuronal nitric oxide synthase-deficient knockout mice. Gastroenterology 2000 119 : 766 73.
31. Gibbons SJ, Rich A, Distad MA et al. Kit/stem cell factor receptor-induced phosphatidylinositol 3′-kinase signalling is not required for normal development and function of interstitial cells of Cajal in mouse gastrointestinal tract. Neurogastroenterol Motil 2003 15 : 643 53.
32. Sasaki S, Siragy HM, Gildea JJ, Felder RA, Carey RM. Production and role of extracellular guanosine cyclic-3′,5′-monophosphate in sodium uptake in human proximal tubule cells. Hypertension 2004 43 : 286 91.
33. Matsuda NM, Miller SM, Sha L, Farrugia G, Szurszewski JH. Mediators of non-adrenergic non-cholinergic inhibitory neurotransmission in porcine jejunum. Neurogastroenterol Motil 2004 16 : 605 12.
34. Zyromski NJ, Duenes JA, Kendrick ML, Balsiger BM, Farrugia G, Sarr MG. Mechanism mediating nitric oxide-induced inhibition in human jejunal longitudinal smooth muscle. Surgery 2001 130 : 489 96.
35. Miller SM, Farrugia G, Schmalz PF, Ermilov LG, Maines MD, Szurszewski JH. Heme oxygenase 2 is present in interstitial cell networks of the mouse small intestine. Gastroenterology 1998 114 : 239 44.
36. Linden DR, Couvrette JM, Ciolino A et al. Indiscriminate loss of myenteric neurones in the TNBS-inflamed guinea-pig distal colon. Neurogastroenterol Motil 2005 17 : 751 60.
37. Seki K, Komuro T. Distribution of interstitial cells of Cajal and gap junction protein, Cx 43 in the stomach of wild-type and W/Wv mutant mice. Anat Embryol (Berl) 2002 206 : 57 65.
38. Ordog T, Baldo M, Danko R, Sanders KM. Plasticity of electrical pacemaking by interstitial cells of Cajal and gastric dysrhythmias in W/W mutant mice. Gastroenterology 2002 123 : 2028 40.
39. Song G, David G, Hirst S, Sanders KM, Ward SM. Regional variation in ICC distribution, pacemaking activity and neural responses in the longitudinal muscle of the murine stomach. J Physiol 2005 564 : 523 40.
40. Mashimo H, Goyal RK. Lessons from genetically engineered animal models. IV. Nitric oxide synthase gene knockout mice. Am J Physiol 1999 277 : G745 50.
41. Bernex F, De Sepulveda P, Kress C, Elbaz C, Delouis C, Panthier JJ. Spatial and temporal patterns of c-kit-expressing cells in WlacZ/+ and WlacZ/WlacZ mouse embryos. Development 1996 122 : 3023 33.
42. Ward SM, Ordog T, Bayguinov JR et al. Development of interstitial cells of Cajal and pacemaking in mice lacking enteric nerves. Gastroenterology 1999 117 : 584 94.
43. Horvath VJ, Vittal H, Ordog 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.
44. Nemeth L, Puri P. Three-dimensional morphology of c-Kit-positive cellular network and nitrergic innervation in the human gut. Arch Pathol Lab Med 2001 125 : 899 904.
45. Wang XY, Sanders KM, Ward SM. Intimate relationship between interstitial cells of cajal and enteric nerves in the guinea-pig small intestine. Cell Tissue Res 1999 295 : 247 56.
46. Iwasaki H, Kajimura M, Osawa S et al. A deficiency of gastric interstitial cells of Cajal accompanied by decreased expression of neuronal nitric oxide synthase and substance P in patients with type 2 diabetes mellitus. J Gastroenterol 2006 41 : 1076 87.
47. Wu JJ, Rothman TP, Gershon MD. Development of the interstitial cell of Cajal: origin, kit dependence and neuronal and nonneuronal sources of kit ligand. J Neurosci Res 2000 59 : 384 401.
48. Hagl CI, Holland-Cunz S, Schafer KH. What do knockout models teach us about the enteric nervous system Eur J Pediatr Surg 2003 13 : 170 5.
49. 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.
50. Papapetropoulos A, Garcia-Cardena G, Madri JA, Sessa WC. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 1997 100 : 3131 9.
51. Contestabile A, Ciani E. Role of nitric oxide in the regulation of neuronal proliferation, survival and differentiation. Neurochem Int 2004 45 : 903 14.
52. Tuteja N, Chandra M, Tuteja R, Misra MK. Nitric oxide as a unique bioactive signaling messenger in physiology and pathophysiology. J Biomed Biotechnol 2004 2004 : 227 37.
53. Boerth NJ, Dey NB, Cornwell TL, Lincoln TM. Cyclic GMP-dependent protein kinase regulates vascular smooth muscle cell phenotype. J Vasc Res 1997 34 : 245 59.
54. Pervin S, Singh R, Hernandez E, Wu G, Chaudhuri G. Nitric oxide in physiologic concentrations targets the translational machinery to increase the proliferation of human breast cancer cells: involvement of mammalian target of rapamycin/eIF4E pathway. Cancer Res 2007 67 : 289 99.
55. Mejia-Garcia TA, Paes-de-Carvalho R. Nitric oxide regulates cell survival in purified cultures of avian retinal neurons: involvement of multiple transduction pathways. J Neurochem 2007 100 : 382 94.
56. Cooke JP. The pivotal role of nitric oxide for vascular health. Can J Cardiol 2004 20 (Suppl B 7B 15B.