Protective effect of melatonin on myenteric neuron damage in experimental colitis in rats

Fundamental and Clinical Pharmacology

Volumn 30, Issue 2, 2016, Pages 117-127

  Shang, Boxin ^a   Shi, Haitao ^a   Wang, Xiaoyan ^a   Guo, Xiaoyan ^a   Wang, Nan ^a   Wang, Yan ^a   Dong, Lei ^a  

^a THE SECOND AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

Inflammation; Melatonin; Myenteric neurons; Nuclear factor erythroid 2 related factor 2; Oxidative stress; Ulcerative colitis

Indexed keywords

HEME OXYGENASE 1; MALONALDEHYDE; MELATONIN; MYELOPEROXIDASE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; 1 FLUORO 2,4 DINITROBENZENE; 2,4-DINITROFLUOROBENZENE SULFONIC ACID; PEROXIDASE; PROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL COLITIS; MALE; MYENTERIC NEURON; MYENTERIC PLEXUS; NERVE CELL; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TREATMENT DURATION; ULCERATIVE COLITIS; WEIGHT REDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; CHEMICALLY INDUCED; COLITIS; COLON; DISEASE MODEL; DRUG EFFECTS; INFLAMMATION; METABOLISM;

ANIMALS; COLITIS; COLON; DINITROFLUOROBENZENE; DISEASE MODELS, ANIMAL; HEME OXYGENASE-1; INFLAMMATION; MALONDIALDEHYDE; MELATONIN; NEURONS; OXIDATIVE STRESS; PEROXIDASE; PROTECTIVE AGENTS; RATS; SUPEROXIDE DISMUTASE;

EID: 84959479866     PISSN: 07673981     EISSN: 14728206     Source Type: Journal    
DOI: 10.1111/fcp.12181     Document Type: Article

References (52)

1. Reddy S.N., Bazzocchi G., Chan S. et al. Colonic motility and transit in health and ulcerative colitis. Gastroenterology (1991) 101 1289-1297.
2. Boisse L., Chisholm S.P., Lukewich M.K., Lomax A.E. Clinical and experimental evidence of sympathetic neural dysfunction during inflammatory bowel disease. Clin. Exp. Pharmacol P. (2009) 36 1026-1033.
3. Sanovic S., Lamb D.P., Blennerhassett M.G. Damage to the enteric nervous system in experimental colitis. Am. J. Pathol. (1999) 155 1051-1057.
4. Bernardini N., Segnani C., Ippolito C. et al. Immunohistochemical analysis of myenteric ganglia and interstitial cells of Cajal in ulcerative colitis. J. Cell Mol. Med. (2012) 16 318-327.
5. Ramond A., Godin-Ribuot D., Ribuot C. et al. Oxidative stress mediates cardiac infarction aggravation induced by intermittent hypoxia. Fundam. Clin. Pharmacol. (2013) 27 252-261.
6. Mas S., Gassó P., Trias G., Bernardo M., Lafuente A. Sulforaphane protects SK-N-SH cells against antipsychotic-induced oxidative stress. Fund. Clin. Pharmacol. (2012) 26 712-721.
7. Venkataramana S., Lourenssen S., Miller K.G., Blennerhassett M.G. Early inflammatory damage to intestinal neurons occurs via inducible nitric oxide synthase. Neurobiol. Dis. (2015) 75 40-52.
8. Korsak K., Silva A.T., Saffrey M.J. Differing effects of NT-3 and GDNF on dissociated enteric ganglion cells exposed to hydrogen peroxide in vitro. Neurosci. Lett. (2012) 517 102-106.
9. Cirilo C.P., Schoffen J.P.F., de Santi-Rampazzo A.P. et al. Dietary restriction interferes with oxidative status and intrinsic intestinal innervation in aging rats. Nutrition (2013) 29 673-680.
10. Tahan G., Gramignoli R., Marongiu F. et al. Melatonin expresses powerful anti-inflammatory and antioxidant activities resulting in complete improvement of acetic-acid-induced colitis in rats. Dig. Dis. Sci. (2011) 56 715-720.
11. Lerner A.B., Case J.D., Takahashi Y., Lee T.H., Mori W. Isolation of melatonin, the pineal gland factor that lightens melanocytes J. Am. Chem. Soc. (1958) 80 2587.
12. Raikhlin N.T., Kvetnoy I.M., Kadagidze Z.G., Sokolov A.V. Immunomorphological studies on synthesis of melatonin in enterochromaffine cells. Acta Histochem. Cytoc. (1978) 11 75-77.
13. Kvetnoi I.M., Raikhlin N.T., Tolkachev V.N. Chromatographic detection of melatonin (5-methoxy-N-acetyltryptamine) and its biological precursors in enterochromaffin cells. Dokl. Akad. Nauk SSSR (1975) 221 226-227.
14. Bubenik G.A., Pang S.F., Hacker R.R., Smith P.S. Melatonin concentrations in serum and tissues of porcine gastrointestinal tract and their relationship to the intake and passage of food. J. Pineal Res. (1996) 21 251-256.
15. Bubenik G.A., Hacker R.R., Brown G.M., Bartos L. Melatonin concentrations in the luminal fluid, mucosa, and muscularis of the bovine and porcine gastrointestinal tract. J. Pineal Res. (1999) 26 56-63.
16. Reiter R.J. Circannual reproductive rhythms in mammals related to photoperiod and pineal function: a review. Chronobiologia. (1974) 1 365-395.
17. Reiter R.J. The melatonin rhythm: both a clock and a calendar. Experientia (1993) 49 654-664.
18. Jung K.H., Hong S.W., Zheng H.M. et al. Melatonin ameliorates cerulein-induced pancreatitis by the modulation of nuclear erythroid 2-related factor 2 and nuclear factor-kappaB in rats. J. Pineal Res. (2010) 48 239-250.
19. Sharma A.K., Mehta A.K., Rathor N. Chalawadi Hanumantappa M.K., Khanna N., Bhattacharya S.K. Melatonin attenuates cognitive dysfunction and reduces neural oxidative stress induced by phosphamidon. Fundam. Clin. Pharmacol. (2013) 27 146-151.
20. Reiter R.J., Tan D.X., Poeggeler B., Menendez-Pelaez A., Chen L.D., Saarela S. Melatonin as a free radical scavenger: implications for aging and age-related diseases. Ann. N. Y. Acad. Sci. (1994) 719 1-12.
21. Tasdemir S., Parlakpinar H., Vardi N., Kaya E., Acet A. Effect of endogen-exogenous melatonin and erythropoietin on dinitrobenzene sulfonic acid induced colitis. Fund. Clin. Pharmacol. (2013) 27 299-307.
22. Trivedi P.P., Jena G.B. Melatonin reduces ulcerative colitis-associated local and systemic damage in mice: investigation on possible mechanisms. Dig. Dis. Sci. (2013) 58 3460-3474.
23. Jena G., Trivedi P.P. A review of the use of melatonin in ulcerative colitis: experimental evidence and new approaches. Inflamm. Bowel Dis. (2014) 20 553-563.
24. Sayyed H.G., Jaumdally R.J., Idriss N.K., El Sers D.A., Blann A. The effect of melatonin on plasma markers of inflammation and on expression of nuclear factor-kappa beta in acetic acid-induced colitis in the rat. Dig. Dis. Sci. (2013) 58 3156-3164.
25. Harder B., Jiang T., Wu T. et al. Molecular mechanisms of Nrf2 regulation and how these influence chemical modulation for disease intervention. Biochem. Soc. Trans. (2015) 43 680-686.
26. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. (2007) 47 89-116.
27. Crespo I., Miguel B.S., Laliena A. et al. Melatonin prevents the decreased activity of antioxidant enzymes and activates nuclear erythroid 2-related factor 2 signaling in an animal model of fulminant hepatic failure of viral origin. J. Pineal Res. (2010) 49 193-200.
28. Zhou L., Zhao D., An H., Zhang H., Jiang C., Yang B. Melatonin prevents lung injury induced by hepatic ischemia-reperfusion through anti-inflammatory and anti-apoptosis effects. Int. Immunopharmacol. (2015) 29 462-467.
29. Wang D., Wei Y., Wang T. et al. Melatonin attenuates (-)-epigallocatehin-3-gallate-triggered hepatotoxicity without compromising its downregulation of hepatic gluconeogenic and lipogenic genes in mice. J. Pineal Res. (2015) 59 497-507.
30. Nosal'ova V., Zeman M., Cerna S., Navarova J., Zakalova M. Protective effect of melatonin in acetic acid induced colitis in rats. J. Pineal Res. (2007) 42 364-370.
31. Ippolito C., Segnani C., De Giorgio R. et al. Quantitative evaluation of myenteric ganglion cells in normal human left colon: implications for histopathological analysis. Cell Tissue Res. (2009) 336 191-201.
32. Chandrasekharan B., Anitha M., Blatt R. et al. Colonic motor dysfunction in human diabetes is associated with enteric neuronal loss and increased oxidative stress. Neurogastroent Motil. (2011) 23 000-000.
33. Liet C., Amenouche F., Freret T. et al. Effects of acute administration of melatonin on attentional, executive, and working memory processes in rats. Fundam. Clin. Pharmacol. (2015) 29 472-477.
34. Knowles C.H., De Giorgio R., Kapur R.P. et al. The London Classification of gastrointestinal neuromuscular pathology: report on behalf of the Gastro 2009 International Working Group. Gut (2010) 59 882-887.
35. Linden D.R., Couvrette J.M., Ciolino A. et al. Indiscriminate loss of myenteric neurones in the TNBS-inflamed guinea-pig distal colon. Neurogastroent Motil. (2005) 17 751-760.
36. Depoortere I., Thijs T., Peeters T.L. Generalized loss of inhibitory innervation reverses serotonergic inhibition into excitation in a rabbit model of TNBS-colitis. Brit. J. Pharmacol. (2002) 135 2011-2019.
37. Roberts J.A., Durnin L., Sharkey K.A., Mutafova-Yambolieva V.N., Mawe G.M. Oxidative stress disrupts purinergic neuromuscular transmission in the inflamed colon. J. Physiol-London. (2013) 591 3725-3737.
38. Poli E., Lazzaretti M., Grandi D., Pozzoli C., Coruzzi G. Morphological and functional alterations of the myenteric plexus in rats with TNBS-induced colitis. Neurochem. Res. (2001) 26 1085-1093.
39. Lourenssen S., Miller K.G., Blennerhassett M.G. Discrete responses of myenteric neurons to structural and functional damage by neurotoxins in vitro. Am. J. Physiol-Gastr L. (2009) 297 G228-G39.
40. Boussenna A., Goncalves-Mendes N., Joubert-Zakeyh J. et al. Impact of basal diet on dextran sodium sulphate (DSS)-induced colitis in rats. Eur. J. Nutr. (2015) 54 1217-1227.
41. Paul G., Bataille F., Obermeier F. et al. Analysis of intestinal haem-oxygenase-1 (HO-1) in clinical and experimental colitis. Clin. Exp. Immunol. (2005) 140 547-555.
42. Schoffen J.P.F., Rampazzo A.P.S., Cirilo C.P. et al. Food restriction enhances oxidative status in aging rats with neuroprotective effects on myenteric neuron populations in the proximal colon. Exp. Gerontol. (2014) 51 54-64.
43. Chojnacki C., Wisniewska-Jarosinska M., Walecka-Kapica E., Klupinska G., Jaworek J., Chojnacki J. Evaluation of melatonin effectiveness in the adjuvant treatment of ulcerative colitis. J. Physiol. Pharmacol. (2011) 62 327-334.
44. Ximenes V.F., Silva S.O., Rodrigues M.R. et al. Superoxide-dependent oxidation of melatonin by myeloperoxidase. J. Biol. Chem. (2005) 280 38160-38169.
45. Reiter R.J., Tan D.X., Terron M.P., Flores L.J., Czarnocki Z. Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim. Pol. (2007) 54 1-9.
46. Tomas-Zapico C., Coto-Montes A. A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. J. Pineal Res. (2005) 39 99-104.
47. Ding K., Wang H.D., Xu J.G. et al. Melatonin stimulates antioxidant enzymes and reduces oxidative stress in experimental traumatic brain injury: the Nrf2-ARE signaling pathway as a potential mechanism. Free Radical Bio Med. (2014) 73 1-11.
48. Yu D., Jiayu Z., Chao M. et al. Melatonin antagonizes Mn-induced oxidative injury through the activation of keap1-Nrf2-ARE signaling pathway in the striatum of mice. Neurotox. Res. (2015) 27 1-16.
49. Yalniz M., Demirel U., Orhan C. et al. Nadroparin Sodium Activates Nrf2/HO-1 Pathway in Acetic Acid-Induced Colitis in Rats. Inflammation (2012) 35 1213-1221.
50. Choi H.-J., Choi H.-J., Park M.-J. et al. The inhibitory effects of Geranium thunbergii on interferon-gamma- and LPS-induced inflammatory responses are mediated by Nrf2 activation. Int. J. Mol. Med. (2015) 35 1237-1245.
51. Vriend J., Reiter R.J. The Keap1-Nrf2-antioxidant response element pathway: A review of its regulation by melatonin and the proteasome. Mol. Cell. Endocrinol. (2015) 401 213-220.
52. Trivedi P.P., Jena G.B., Tikoo K.B., Kumar V. Melatonin modulated autophagy and Nrf2 signaling pathways in mice with colitis-associated colon carcinogenesis. Mol. Carcinog. (2015) doi: 10.1002/mc.22274.