Vasoactive intestinal peptide reduces oxidative stress in pancreatic acinar cells through the inhibition of NADPH oxidase

Peptides

Volumn 32, Issue 10, 2011, Pages 2067-2076

  Fujimori, Nao ^a   Oono, Takamasa ^a   Igarashi, Hisato ^a   Ito, Tetsuhide ^a   Nakamura, Taichi ^a   Uchida, Masahiko ^a   Coy, David H ^b   Jensen, Robert T ^c   Takayanagi, Ryoichi ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Antioxidant; NADPH oxidase; Reactive oxygen species; Vasoactive intestinal peptide

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; RNA; VASOACTIVE INTESTINAL POLYPEPTIDE;

ACINAR CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL ISOLATION; CELL VIABILITY; CONTROLLED STUDY; INHIBITION KINETICS; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PURIFICATION;

ACINAR CELLS; ANIMALS; CELLS, CULTURED; MALE; NADPH OXIDASE; OXIDATIVE STRESS; PANCREAS, EXOCRINE; RATS; RATS, INBRED LEW; REACTIVE OXYGEN SPECIES; VASOACTIVE INTESTINAL PEPTIDE;

RATTUS;

EID: 80054054255     PISSN: 01969781     EISSN: 18735169     Source Type: Journal    
DOI: 10.1016/j.peptides.2011.08.027     Document Type: Article

References (53)

1. C. Abad, C. Martinez, M.G. Juarranz, A. Arranz, J. Leceta, and M. Delgado Therapeutic effects of vasoactive intestinal peptide in the trinitrobenzene sulfonic acid mice model of Crohn's disease Gastroenterology 124 2003 961 971 (Pubitemid 36389799)
2. F.M. Abu-Zidan, M.J. Bonham, and J.A. Windsor Severity of acute pancreatitis: a multivariate analysis of oxidative stress markers and modified Glasgow criteria Br J Surg 87 2000 1019 1023 (Pubitemid 30496849)
3. X. Ao, F. Fang, and F. Xu Role of vasoactive intestinal peptide in hyperoxia-induced injury of primary type II alveolar epithelial cells Indian J Pediatr 78 2011 535 539
4. G.O. Barbezat, and M.I. Grossman Intestinal secretion: stimulation by peptides Science 174 1971 422 424
5. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol Rev 87 2007 245 313 (Pubitemid 46209993)
6. M. Calafat, L. Larocca, V. Roca, V. Hauk, N. Pregi, and A. Nesse Vasoactive intestinal peptide inhibits TNF-alpha-induced apoptotic events in acinar cells from nonobese diabetic mice submandibular glands Arthritis Res Ther 11 2009 R53
7. A. Castorina, A. Tiralongo, S. Giunta, M.L. Carnazza, G. Rasi, and V. D'Agata PACAP and VIP prevent apoptosis in schwannoma cells Brain Res 1241 2008 29 35
8. Y.C. Chan, and P.S. Leung Angiotensin II type 1 receptor-dependent nuclear factor-kappaB activation-mediated proinflammatory actions in a rat model of obstructive acute pancreatitis J Pharmacol Exp Ther 323 2007 10 18
9. M. Chvanov, O.H. Petersen, and A. Tepikin Free radicals and the pancreatic acinar cells: role in physiology and pathology Philos Trans R Soc Lond B Biol Sci 360 2005 2273 2284 (Pubitemid 46682146)
10. A. Dabrowski, S.J. Konturek, J.W. Konturek, and A. Gabryelewicz Role of oxidative stress in the pathogenesis of caerulein-induced acute pancreatitis Eur J Pharmacol 377 1999 1 11 (Pubitemid 29322751)
11. M. Delgado, C. Abad, C. Martinez, J. Leceta, and R.P. Gomariz Vasoactive intestinal peptide prevents experimental arthritis by downregulating both autoimmune and inflammatory components of the disease Nat Med 7 2001 563 568 (Pubitemid 32448323)
12. M. Delgado, and D. Ganea Neuroprotective effect of vasoactive intestinal peptide (VIP) in a mouse model of Parkinson's disease by blocking microglial activation FASEB J 17 2003 944 946
13. M. Delgado, C. Martinez, D. Pozo, J.R. Calvo, J. Leceta, and D. Ganea Vasoactive intestinal peptide (VIP) and pituitary adenylate cyclase-activation polypeptide (PACAP) protect mice from lethal endotoxemia through the inhibition of TNF-alpha and IL-6 J Immunol 162 1999 1200 1205 (Pubitemid 29035454)
14. M. Delgado, N. Varela, and E. Gonzalez-Rey Vasoactive intestinal peptide protects against beta-amyloid-induced neurodegeneration by inhibiting microglia activation at multiple levels Glia 56 2008 1091 1103
15. J. Escobar, J. Pereda, A. Arduini, J. Sandoval, L. Sabater, and L. Aparisi Cross-talk between oxidative stress and pro-inflammatory cytokines in acute pancreatitis: a key role for protein phosphatases Curr Pharm Des 15 2009 3027 3042
16. N. Foster, S.D. Hulme, and P.A. Barrow Vasoactive intestinal peptide (VIP) prevents killing of virulent and phoP mutant Salmonella typhimurium by inhibiting IFN-gamma stimulated NADPH oxidative pathways in murine macrophages Cytokine 36 2006 134 140 (Pubitemid 46275462)
17. M. Fukui, and B.T. Zhu Mitochondrial superoxide dismutase SOD2, but not cytosolic SOD1, plays a critical role in protection against glutamate-induced oxidative stress and cell death in HT22 neuronal cells Free Radic Biol Med 48 2010 821 830
18. H.Y. Gaisano, and F.S. Gorelick New insights into the mechanisms of pancreatitis Gastroenterology 136 2009 2040 2044
19. A.S. Gukovskaya, E. Vaquero, V. Zaninovic, F.S. Gorelick, A.J. Lusis, and M.L. Brennan Neutrophils and NADPH oxidase mediate intrapancreatic trypsin activation in murine experimental acute pancreatitis Gastroenterology 122 2002 974 984 (Pubitemid 34267281)
20. H. Igarashi, T. Ito, S.A. Mantey, T.K. Pradhan, W. Hou, and D.H. Coy Development of simplified vasoactive intestinal peptide analogs with receptor selectivity and stability for human vasoactive intestinal peptide/pituitary adenylate cyclase-activating polypeptide receptors J Pharmacol Exp Ther 315 2005 370 381 (Pubitemid 41380533)
21. T. Ishibashi, H. Zhao, K. Kawabe, T. Oono, K. Egashira, and K. Suzuki Blocking of monocyte chemoattractant protein-1 (MCP-1) activity attenuates the severity of acute pancreatitis in rats J Gastroenterol 43 2008 79 85 (Pubitemid 351324990)
22. T. Ito, W. Hou, T. Katsuno, H. Igarashi, T.K. Pradhan, and S.A. Mantey Rat and guinea pig pancreatic acini possess both VIP(1) and VIP(2) receptors, which mediate enzyme secretion Am J Physiol Gastrointest Liver Physiol 278 2000 G64 G74
23. T. Kaku, T. Oono, H. Zhao, J. Gibo, K. Kawabe, and T. Ito IS-741 attenuates local migration of monocytes and subsequent pancreatic fibrosis in experimental chronic pancreatitis induced by dibutyltin dichloride in rats Pancreas 34 2007 299 309 (Pubitemid 46588255)
24. K. Kikuta, A. Masamune, M. Satoh, N. Suzuki, K. Satoh, and T. Shimosegawa Hydrogen peroxide activates activator protein-1 and mitogen-activated protein kinases in pancreatic stellate cells Mol Cell Biochem 291 2006 11 20 (Pubitemid 44725297)
25. H. Kim Cerulein pancreatitis: oxidative stress, inflammation, and apoptosis Gut Liver 2 2008 74 80
26. J.S. Kim, B.A. Diebold, B.M. Babior, U.G. Knaus, and G.M. Bokoch Regulation of Nox1 activity via protein kinase A-mediated phosphorylation of NoxA1 and 14-3-3 binding J Biol Chem 282 2007 34787 34800 (Pubitemid 350232473)
27. G. Koh, K.S. Suh, S. Chon, S. Oh, J.T. Woo, and S.W. Kim Elevated cAMP level attenuates 2-deoxy-d-ribose-induced oxidative damage in pancreatic beta-cells Arch Biochem Biophys 438 2005 70 79 (Pubitemid 40725209)
28. M. Kojima, T. Ito, T. Oono, T. Hisano, H. Igarashi, and Y. Arita VIP attenuation of the severity of experimental pancreatitis is due to VPAC1 receptor-mediated inhibition of cytokine production Pancreas 30 2005 62 70 (Pubitemid 40070628)
29. J.D. Lambeth Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy Free Radic Biol Med 43 2007 332 347 (Pubitemid 46992767)
30. P.S. Leung, and Y.C. Chan Role of oxidative stress in pancreatic inflammation Antioxid Redox Signal 11 2009 135 165
31. J.M. Li, A.M. Mullen, S. Yun, F. Wientjes, G.Y. Brouns, and A.J. Thrasher Essential role of the NADPH oxidase subunit p47(phox) in endothelial cell superoxide production in response to phorbol ester and tumor necrosis factor-alpha Circ Res 90 2002 143 150 (Pubitemid 34627082)
32. F. Lutgendorff, L.M. Trulsson, L.P. van Minnen, G.T. Rijkers, H.M. Timmerman, and L.E. Franzen Probiotics enhance pancreatic glutathione biosynthesis and reduce oxidative stress in experimental acute pancreatitis Am J Physiol Gastrointest Liver Physiol 295 2008 G1111 G1121
33. A. Masamune, T. Watanabe, K. Kikuta, K. Satoh, and T. Shimosegawa NADPH oxidase plays a crucial role in the activation of pancreatic stellate cells Am J Physiol Gastrointest Liver Physiol 294 2008 G99 G108
34. S. Misaka, Y. Aoki, S. Karaki, A. Kuwahara, T. Mizumoto, and S. Onoue Inhalable powder formulation of a stabilized vasoactive intestinal peptide (VIP) derivative: anti-inflammatory effect in experimental asthmatic rats Peptides 31 2010 72 78
35. H. Oeseburg, R.A. de Boer, H. Buikema, P. van der Harst, W.H. van Gilst, and H.H. Sillje Glucagon-like peptide 1 prevents reactive oxygen species-induced endothelial cell senescence through the activation of protein kinase A Arterioscler Thromb Vasc Biol 30 2010 1407 1414
36. S. Ohashi, A. Nishio, H. Nakamura, M. Kido, S. Ueno, and N. Uza Protective roles of redox-active protein thioredoxin-1 for severe acute pancreatitis Am J Physiol Gastrointest Liver Physiol 290 2006 G772 G781
37. S.J. Pandol, A.K. Saluja, C.W. Imrie, and P.A. Banks Acute pancreatitis: bench to the bedside Gastroenterology 132 2007 1127 1151 (Pubitemid 46440879)
38. M.S. Petrov Therapeutic implications of oxidative stress in acute and chronic pancreatitis Curr Opin Clin Nutr Metab Care 13 2010 562 568
39. P.J. Piper, S.I. Said, and J.R. Vane Effects on smooth muscle preparations of unidentified vasoactive peptides from intestine and lung Nature 225 1970 1144 1146
40. B. Rau, B. Poch, F. Gansauge, A. Bauer, A.K. Nussler, and T. Nevalainen Pathophysiologic role of oxygen free radicals in acute pancreatitis: initiating event or mediator of tissue damage? Ann Surg 231 2000 352 360 (Pubitemid 30137123)
41. J.C. Reubi In vitro evaluation of VIP/PACAP receptors in healthy and diseased human tissues. Clinical implications Ann N Y Acad Sci 921 2000 1 25 (Pubitemid 32094523)
42. S. Saha, Y. Li, and M.B. Anand-Srivastava Reduced levels of cyclic AMP contribute to the enhanced oxidative stress in vascular smooth muscle cells from spontaneously hypertensive rats Can J Physiol Pharmacol 86 2008 190 198 (Pubitemid 351536450)
43. S.I. Said, and V. Mutt Potent peripheral and splanchnic vasodilator peptide from normal gut Nature 225 1970 863 864
44. 2-induced pancreatic beta cell death Apoptosis 15 2010 1165 1176
45. M. Siech, Z. Zhou, S. Zhou, B. Bair, A. Alt, and S. Hamm Stimulation of stellate cells by injured acinar cells: a model of acute pancreatitis induced by alcohol and fat (VLDL) Am J Physiol Gastrointest Liver Physiol 297 2009 G1163 G1171
46. S.G. Smalley, P.A. Barrow, and N. Foster Immunomodulation of innate immune responses by vasoactive intestinal peptide (VIP): its therapeutic potential in inflammatory disease Clin Exp Immunol 157 2009 225 234
47. R.A. Steingart, B. Solomon, D.E. Brenneman, M. Fridkin, and I. Gozes VIP and peptides related to activity-dependent neurotrophic factor protect PC12 cells against oxidative stress J Mol Neurosci 15 2000 137 145 (Pubitemid 32281426)
48. A. Szeto, D.A. Nation, A.J. Mendez, J. Dominguez-Bendala, L.G. Brooks, and N. Schneiderman Oxytocin attenuates NADPH-dependent superoxide activity and IL-6 secretion in macrophages and vascular cells Am J Physiol Endocrinol Metab 295 2008 E1495 E1501
49. K. Tsai, S.S. Wang, T.S. Chen, C.W. Kong, F.Y. Chang, and S.D. Lee Oxidative stress: an important phenomenon with pathogenetic significance in the progression of acute pancreatitis Gut 42 1998 850 855 (Pubitemid 28277228)
50. H. Weber, S. Huhns, L. Jonas, G. Sparmann, M. Bastian, and P. Schuff-Werner Hydrogen peroxide-induced activation of defense mechanisms against oxidative stress in rat pancreatic acinar AR42J cells Free Radic Biol Med 42 2007 830 841 (Pubitemid 46274173)
51. J.H. Yu, K.H. Kim, D.G. Kim, and H. Kim Diphenyleneiodonium suppresses apoptosis in cerulein-stimulated pancreatic acinar cells Int J Biochem Cell Biol 39 2007 2063 2075 (Pubitemid 47376827)
52. J.H. Yu, J.W. Lim, H. Kim, and K.H. Kim NADPH oxidase mediates interleukin-6 expression in cerulein-stimulated pancreatic acinar cells Int J Biochem Cell Biol 37 2005 1458 1469
53. R. Yu, H. Zhang, L. Huang, X. Liu, and J. Chen Anti-hyperglycemic, antioxidant and anti-inflammatory effects of VIP and a VPAC1 agonist on streptozotocin-induced diabetic mice Peptides 32 2011 216 222