Impaired heme oxygenase-1 induction in the gastric antrum induces disruption of the interstitial cells of Cajal network in a rat model of streptozotocin-induced diabetes

Neurogastroenterology and Motility

Volumn 25, Issue 7, 2013, Pages

  Mogami, S ^a,b   Suzuki, H ^a   Tsugawa, H ^a   Fukuhara, S ^a   Hibi, T ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b TSUMURA AND CO   (Japan)

Author keywords

Diabetes; M2 macrophage; Oxidative stress

Indexed keywords

HEME OXYGENASE 1; PROTOPORPHYRIN COBALT; STEM CELL FACTOR RECEPTOR; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DISRUPTION; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME INDUCTION; FEMALE; GENE MUTATION; IMMUNOFLUORESCENCE; INTERSTITIAL CELL OF CAJAL; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STOMACH ANTRUM; STREPTOZOCIN DIABETES; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HEME OXYGENASE (DECYCLIZING); INTERSTITIAL CELLS OF CAJAL; PYLORIC ANTRUM; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STREPTOZOCIN; UP-REGULATION;

EID: 84879136541     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12122     Document Type: Article

References (24)

1. 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.
2. Choi KM, Gibbons SJ, Nguyen TV et al. Heme oxygenase-1 protects interstitial cells of Cajal from oxidative stress and reverses diabetic gastroparesis. Gastroenterology 2008; 135: 2055-64, 2064, e2051-2052.
3. Wang XY, Huizinga JD, Diamond J, Liu LW. Loss of intramuscular and submuscular interstitial cells of Cajal and associated enteric nerves is related to decreased gastric emptying in streptozotocin-induced diabetes. Neurogastroenterol Motil 2009; 21: 1095, e1092.
4. 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.
5. 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.
6. Suzuki S, Suzuki H, Horiguchi K et al. Delayed gastric emptying and disruption of the interstitial cells of Cajal network after gastric ischaemia and reperfusion. Neurogastroenterol Motil 2010; 22: 585-593, e126.
7. 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.
8. Ward SM, Harney SC, Bayguinov JR, McLaren GJ, Sanders KM. Development of electrical rhythmicity in the murine gastrointestinal tract is specifically encoded in the tunica muscularis. J Physiol 1997; 505(Pt 1): 241-58.
9. Sanders KM. A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 1996; 111: 492-515.
10. 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.
11. Ward SM, Beckett EA, Wang X, Baker F, Khoyi M, Sanders KM. Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motor neurons. J Neurosci 2000; 20: 1393-403.
12. Mitsui R, Komuro T. Distribution and ultrastructure of interstitial cells of Cajal in the gastric antrum of wild-type and Ws/Ws rats. Anat Embryol (Berl) 2003; 206: 453-60.
13. Faussone-Pellegrini MS. Relationships between neurokinin receptor-expressing interstitial cells of Cajal and tachykininergic nerves in the gut. J Cell Mol Med 2006; 10: 20-32.
14. Abraham NG, Asija A, Drummond G, Peterson S. Heme oxygenase -1 gene therapy: recent advances and therapeutic applications. Curr Gene Ther 2007; 7: 89-108.
15. Kashyap PC, Choi KM, Dutta N et al. Carbon monoxide reverses diabetic gastroparesis in NOD mice. Am J Physiol Gastrointest Liver Physiol 2010; 298: G1013-9.
16. Choi KM, Kashyap PC, Dutta N et al. CD206-positive M2 macrophages that express heme oxygenase-1 protect against diabetic gastroparesis in mice. Gastroenterology 2010; 138: 2399-409, 2409, e2391.
17. Kinoshita K, Horiguchi K, Fujisawa M et al. 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 2007; 127: 41-53.
18. Ohama T, Hori M, Momotani E, Elorza M, Gerthoffer WT, Ozaki H. IL-1beta inhibits intestinal smooth muscle proliferation in an organ culture system: involvement of COX-2 and iNOS induction in muscularis resident macrophages. Am J Physiol Gastrointest Liver Physiol 2007; 292: G1315-22.
19. Chokechanachaisakul U, Kaneko T, Yamanaka Y et al. Gene expression analysis of resident macrophages in lipopolysaccharide-stimulated rat molar pulps. J Endod 2011; 37: 1258-63.
20. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006; 86: 583-650.
21. Loboda A, Jazwa A, Grochot-Przeczek A et al. Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2008; 10: 1767-812.
22. Shan Y, Lambrecht RW, Donohue SE, Bonkovsky HL. Role of Bach1 and Nrf2 in up-regulation of the heme oxygenase-1 gene by cobalt protoporphyrin. FASEB J 2006; 20: 2651-3.
23. Piao MS, Park JJ, Choi JY et al. Nrf2-dependent and Nrf2-independent induction of phase 2 detoxifying and antioxidant enzymes during keratinocyte differentiation. Arch Dermatol Res 2012; 304: 387-95.
24. Reisman SA, Aleksunes LM, Klaassen CD. Oleanolic acid activates Nrf2 and protects from acetaminophen hepatotoxicity via Nrf2-dependent and Nrf2-independent processes. Biochem Pharmacol 2009; 77: 1273-82.