Free radicals and the pancreatic acinar cells: Role in physiology and pathology

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 360, Issue 1464, 2005, Pages 2273-2284

  Chvanov, M ^a   Petersen, O H ^a   Tepikin, A ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Nitric oxide; Pancreatic acinar cells; Pancreatitis; Reactive nitrogen species; Reactive oxygen species

Indexed keywords

APOPTOSIS; ENZYME ACTIVITY; FREE RADICAL; HOMEOSTASIS; NITRIC OXIDE; OXYGEN; PHYSIOLOGICAL RESPONSE;

FREE RADICAL; NITRIC OXIDE SYNTHASE;

APOPTOSIS; BIOLOGICAL MODEL; HOMEOSTASIS; HUMAN; METABOLISM; PANCREAS; PATHOLOGY; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

APOPTOSIS; FREE RADICALS; HOMEOSTASIS; HUMANS; MODELS, BIOLOGICAL; NITRIC OXIDE SYNTHASE; PANCREAS; SIGNAL TRANSDUCTION;

EID: 33745265721     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2005.1757     Document Type: Conference Paper

References (167)

1. Acheson, D. W., Rose, P., Houston, J. B. & Braganza, J. M. 1985 Induction of cytochromes P-450 in pancreatic disease: consequence, coincidence or cause? Clin. Chim. Acta 153, 73-84. (doi:10.1016/0009-8981(85) 90158-5.)
2. Ager, A., Wenham, D. J. & Gordon, J. L. 1984 Stimulation of endothelial cells by protease activity in commercial preparations of xanthine oxidase. Thromb. Res. 35, 43-52. (doi:10.1016/0049-3848(84)90311- 6.)
3. Ahn, S. H., Seo, D. W., Ko, Y. K., Sung, D. S., Bae, G. U., Yoon, J. W., Hong, S. Y., Han, J. W. & Lee, H. W. 1998 NO/cGMP pathway is involved in exocrine secretion from rat pancreatic acinar cells. Arch. Pharm. Res. 21, 657-663.
4. Al Mufti, R. A., Williamson, R. C. & Mathie, R. T. 1998 Increased nitric oxide activity in a rat model of acute pancreatitis. Gut 43, 564-570.
5. Andrzejewska, A., Jurkowska, G. & Augustynowicz, A. 2002 The influence of nitric oxide synthesis modulation on the pancreatic acinar cells in caerulein-induced acute pancreatitis. An ultrastructural and morphometric study. Pol. J. Pathol. 53, 215-221.
6. Ayub, K., Serracino-Inglott, F., Williamson, R. C. & Mathie, R. T. 2001 Expression of inducible nitric oxide synthase contributes to the development of pancreatitis following pancreatic ischaemia and reperfusion. Br. J. Surg. 88, 1189-1193. (doi:10.1046/j.0007-1323.2001.01841.x. )
7. 2+ entry in pancreatic acinar cells. J. Biol. Chem. 268, 10 808-10 812.
8. Beckman, J. & Tsai, H.-H. 1994 Reactions and diffusion of nitric oxide and peroxynitrite. Biochemist 16, 8-10.
9. Benz, S. et al. 2002 Effect of nitric oxide in ischemia/reperfusion of the pancreas. J. Surg. Res. 106, 46-53. (doi:10.1006/jsre.2002.6457.)
10. Blaise, G. A., Gauvin, D., Gangal, M. & Authier, S. 2005 Nitric oxide, cell signaling and cell death. Toxicology 208, 177-192. (doi:10.1016/j.tox.2004.11.032.)
11. Braganza, J. M. 1998 A framework for the aetiogenesis of chronic pancreatitis. Digestion 59(Suppl. 4), 1-12. (doi:10.1159/ 000051438.)
12. 2+ release. Free Radic. Biol. Med. 29, 343-348. (doi:10.1016/S0891- 5849(00)00318-X.)
13. Burrell, M. A., Montuenga, L. M., Garcia, M. & Villaro, A. C. 1996 Detection of nitric oxide synthase (NOS) in somatostatin-producing cells of human and murine stomach and pancreas. J. Histochem. Cytochem. 44, 339-346.
14. Cassone, E., Maneschi, E. M. & Faccas, J. G. 1991 Effects of allopurinol on ischemic experimental pancreatitis. Int. J. Pancreatol. 8, 227-234.
15. 2+. J. Biol. Chem. 274, 282-287. (doi:10.1074/jbc.274.1.282.)
16. Chen, C. C., Wang, S. S., Tsay, S. H., Lee, F. Y., Lu, R. H., Chang, F. Y. & Lee, S. D. 2004 Effects of nitric oxide synthase inhibitors on retrograde bile salt-induced pancreatitis rats. J. Chin. Med. Assoc. 67, 9-14.
17. Closa, D., Bulbena, O., Hotter, G., Rosello-Catafau, J., Fernandez-Cruz, L. & Gelpi, E. 1994a Xanthine oxidase activation in cerulein- and taurocholate-induced acute pancreatitis in rats. Arch. Int. Physiol. Biochim. Biophys. 102, 167-170.
18. Closa, D., Hotter, G., Prats, N., Bulbena, O., Rosello-Catafau, J., Fernandez-Cruz, L. & Gelpi, E. 1994b Prostanoid generation in early stages of acute pancreatitis: a role for nitric oxide. Inflammation 18, 469-480. (doi:10.1007/BF01560694.)
19. Closa, D., Hotter, G., Rosello-Catafau, J., Bulbena, O., Fernandez-Cruz, L. & Gelpi, E. 1994c Prostanoids and oxygen free radicals in early stages of experimental acute pancreatitis. Dig. Dis. Sci. 39, 1537-1543. (doi:10.1007/BF02088061.)
20. Cuzzocrea, S. et al. 2002 Inducible nitric oxide synthase-deficient mice exhibit resistance to the acute pancreatitis induced by cerulein. Shock 17, 416-422. (doi:10.1097/00024382-200205000- 00013.)
21. Cuzzocrea, S., Genovese, T., Mazzon, E., Di Paola, R., Muia, C., Britti, D. & Salvemini, D. 2004 Reduction in the development of cerulein-induced acute pancreatitis by treatment with M40401, a new selective superoxide dismutase mimetic. Shock 22, 254-261. (doi:10.1097/01.shk. 0000132490.79498.11.)
22. Czako, L., Takacs, T., Varga, I. S., Tiszlavicz, L., Hai, D. Q., Hegyi, P., Matkovics, B. & Lonovics, J. 1998 Involvement of oxygen-derived free radicals in L-arginine-induced acute pancreatitis. Dig. Dis. Sci. 43, 1770-1777. (doi:10.1023/A:1018839821176.)
23. Dabrowski, A. 2003 Exocrine pancreas; molecular basis for intracellular signaling, damage and protection - Polish experience. J. Physiol. Pharmacol. 54(Suppl. 3), 167-181.
24. Dabrowski, A. & Gabryelewicz, A. 1994 Nitric oxide contributes to multiorgan oxidative stress in acute experimental pancreatitis. Scand. J. Gastroenterol. 29, 943-948.
25. Dabrowski, A., Boguslowicz, C., Dabrowska, M., Tribillo, I. & Gabryelewicz, A. 2000 Reactive oxygen species activate mitogen-activated protein kinases in pancreatic acinar cells. Pancreas 21, 376-384. (doi:10.1097/00006676-200011000-00008.)
26. Dembinski, A., Warzecha, Z., Konturek, P. J., Ceranowicz, P. & Konturek, S. J. 1996 Influence of capsaicin-sensitive afferent neurons and nitric oxide (NO) on cerulein-induced pancreatitis in rats. Int. J. Pancreatol. 19, 179-189.
27. DiMagno, M. J., Hao, Y., Tsunoda, Y., Williams, J. A. & Owyang, C. 2004a Secretagogue-stimulated pancreatic secretion is differentially regulated by constitutive nitric oxide synthase isoforms in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G428-G436. (doi:10.1152/ajpgi.00368.2003.)
28. DiMagno, M. J., Williams, J. A., Hao, Y., Ernst, S. A. & Owyang, C. 2004b Endothelial nitric oxide synthase is protective in the initiation of caerulein-induced acute pancreatitis in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G80-G87. (doi:10.1152/ajpgi.00525. 2003.)
29. + channels TALK-1 and TALK-2 are activated by nitric oxide and reactive oxygen species. J. Physiol. 562, 235-244. (doi:10.1113/jphysiol.2004.071266.)
30. Ehlers, R. A., Hernandez, A., Bloemendal, L. S., Ethridge, R. T., Farrow, B. & Evers, B. M. 1999 Mitochondrial DNA damage and altered membrane potential (delta psi) in pancreatic acinar cells induced by reactive oxygen species. Surgery 126, 148-155. (doi:10.1067/msy.1999.98725.)
31. Ember, Z., Reti, A. & Feher, E. 2000 Enzyme- and immunohistochemical localization of nitric oxide synthase in nerves of the porcine pancreas. Neurosci. Lett. 292, 163-166. (doi:10.1016/S0304-3940(00)01455-5.)
32. Fleming, I. & Busse, R. 2003 Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284, R1-12.
33. Flodstrom, M., Horwitz, M. S., Maday, A., Balakrishna, D., Rodriguez, E. & Sarvetnick, N. 2001 A critical role for inducible nitric oxide synthase in host survival following coxsackievirus B4 infection. Virology 281, 205-215. (doi:10.1006/viro.2000.0801.)
34. Foster, J. R., Idle, J. R., Hardwick, J. P., Bars, R., Scott, P. & Braganza, J. M. 1993 Induction of drug-metabolizing enzymes in human pancreatic cancer and chronic pancreatitis. J. Pathol. 169, 457-463. (doi:10.1002/path.1711690412.)
35. Fu, K., Sarras Jr, M. P., De Lisle, R. C. & Andrews, G. K. 1997 Expression of oxidative stress-responsive genes and cytokine genes during caerulein-induced acute pancreatitis. Am. J. Physiol. 273, G696-G705.
36. Garcia-Benito, M., San Roman, J. I., Lopez, M. A., Garcia-Marin, L. J. & Calvo, J. J. 2000 Nitric oxide stimulates tyrosine phosphorylation of p125(FAK) and paxillin in rat pancreatic acini. Biochem. Biophys. Res. Commun. 274, 635-640. (doi:10.1006/bbrc.2000.3192.)
37. Gardner, J. D. & Rottman, A. J. 1980 Evidence against cyclic GMP as a mediator of the actions of secretagogues on amylase release from guinea-pig pancreas. Biochim. Biophys. Acta 627, 230-243.
38. Gerasimenko, J. V., Gerasimenko, O. V., Palejwala, A., Tepikin, A. V., Petersen, O. H. & Watson, A. J. 2002 Menadione-induced apoptosis: roles of cytosolic Ca(2+) elevations and the mitochondrial permeability transition pore. J. Cell Sci. 115, 485-497.
39. Ghafourifar, P. & Richter, C. 1997 Nitric oxide synthase activity in mitochondria. FEBS Lett. 418, 291-296. (doi:10.1016/S0014-5793(97) 01397-5.)
40. Ghafourifar, P., Schenk, U., Klein, S. D. & Richter, C. 1999 Mitochondrial nitric-oxide synthase stimulation causes cytochrome c release from isolated mitochondria. Evidence for intramitochondrial peroxynitrite formation. J. Biol. Chem. 274, 31 185-31 188. (doi:10.1074/jbc.274.44.31185.)
41. 2+ entry in rat pancreatic acinar cells. Biochem. J. 311, 649-656.
42. Giulivi, C., Poderoso, J. J. & Boveris, A. 1998 Production of nitric oxide by mitochondria. J. Biol. Chem. 273, 11 038-11 043. (doi:10.1074/jbc.273.18.11038.)
43. Gonzalez, A., Schmid, A., Salido, G. M., Camello, P. J. & Pariente, J. A. 2002 XOD-catalyzed ROS generation mobilizes calcium from intracellular stores in mouse pancreatic acinar cells. Cell. Signal. 14, 153-159. (doi:10.1016/S0898-6568(01)00247-9.)
44. Gough, D. B., Boyle, B., Joyce, W. P., Delaney, C. P., McGeeney, K. F., Gorey, T. F. & Fitzpatrick, J. M. 1990 Free radical inhibition and serial chemiluminescence in evolving experimental pancreatitis. Br. J. Surg. 77, 1256-1259.
45. 2+ transients in pancreatic beta cells lacking contact. Pancreas 23, 387-392. (doi:10.1097/00006676- 200111000-00009.)
46. Greenbaum, L. M., Hirshkowitz, A. & Shoichet, I. 1959 The activation of trypsinogen by cathepsin B. J. Biol. Chem. 234, 2885-2890.
47. Guice, K. S., Miller, D. E., Oldham, K. T., Townsend Jr, C. M. & Thompson, J. C. 1986 Superoxide dismutase and catalase: a possible role in established pancreatitis. Am. J. Surg. 151, 163-169. (doi:10.1016/0002-9610(86)90027-9.)
48. Gukovskaya, A. S. & Pandol, S. J. 1994 Nitric oxide production regulates cGMP formation and calcium influx in pancreatic acinar cells. Am. J. Physiol. 266, G350-G356.
49. Gukovskaya, A. S. & Pandol, S. J. 1995 Dual regulation of cGMP formation by calcium in pancreatic acinar cells. Am. J. Physiol. 268, G900-G907.
50. Gukovskaya, A. S., Vaquero, E., Zaninovic, V., Gorelick, F. S., Lusis, A. J., Brennan, M. L., Holland, S. & Pandol, S. J. 2002 Neutrophils ADPH oxidase mediate intrapancreatic trypsin activation in murine experimental acute pancreatitis. Gastroenterology 122, 974-984. (doi:10.1053/gast. 2002.32409.)
51. Gunther, G. R. & Jamieson, J. D. 1979 Increased intracellular cyclic GMP does not correlate with protein discharge from pancreatic acinar cells. Nature 280, 318-320. (doi:10.1038/280318a0.)
52. Guyan, P. M., Uden, S. & Braganza, J. M. 1990 Heightened free radical activity in pancreatitis. Free Radic. Biol. Med. 8, 347-354. (doi:10.1016/0891-5849(90)90100-W.)
53. Halangk, W. & Lerch, M. M. 2004 Early events in acute pancreatitis. Gastroenterol. Clin. North Am. 33, 717-731. (doi:10.1016/j.gtc. 2004.07.009.)
54. Han, B., Klonowski-Stumpe, H., Luthen, R., Schreiber, R., Haussinger, D. & Niederau, C. 2000 Menadione-induced oxidative stress inhibits cholecystokinin-stimulated secretion of pancreatic acini by cell dehydration. Pancreas 21, 191-202. (doi:10.1097/00006676-200008000-00013.)
55. Haymovits, A. & Scheele, G. A. 1976 Cellular cyclic nucleotides and enzyme secretion in the pancreatic acinar cell. Proc. Natl Acad. Sci. USA 73, 156-160.
56. Hegyi, P., Rakonczay Jr, Z., Sari, R., Gog, C., Lonovics, J., Takacs, T. & Czako, L. 2004 L-Arginine-induced experimental pancreatitis. World J. Gastroenterol. 10, 2003-2009.
57. Holst, J. J., Rasmussen, T. N. & Schmidt, P. 1994 Role of nitric oxide in neurally induced pancreatic exocrine secretion in pigs. Am. J. Physiol. 266, G206-G213.
58. Hotter, G., Closa, D., Pi, F., Prats, N., Fernandez-Cruz, L., Bulbena, O., Gelpi, E. & Rosello-Catafau, J. 1995 Nitric oxide and arachidonate metabolism in ischemia-reperfusion associated with pancreas transplantation. Transplantation 59, 417-421.
59. Ischiropoulos, H. 2003 Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 305, 776-783. (doi:10.1016/S0006-291X(03)00814-3.)
60. Isik, A. T. et al. 2004 The effect of combination therapy of hyperbaric oxygen, meropenem, and selective nitric oxide synthase inhibitor in experimental acute pancreatitis. Pancreas 28, 53-57. (doi:10.1097/00006676-200401000-00008.)
61. Jaworek, J., Jachimczak, B., Tomaszewska, R., Konturek, P. C., Pawlik, W. W., Sendur, R., Hahn, E. G., Stachura, J. & Konturek, S. J. 2000 Protective action of lipopolysaccharides in rat caerulein-induced pancreatitis: role of nitric oxide. Digestion 62, 1-13. (doi:10.1159/000007771.)
62. Jaworek, J., Bonio, J., Leja-Szpa, A., Nawrot, K., Tomaszewska, M. R., Stachura, J., Pawlik, W. W. & Konturek, S. J. 2002a Sensory nerves in central and peripheral control of pancreatic integrity by leptin and melatonin. J. Physiol. Pharmacol. 53, 51-74.
63. Jaworek, J. et al. 2002b Leptin protects the pancreas from damage induced by caerulein overstimulation by modulating cytokine production. Pancreatology 2, 89-99. (doi:10.1159/000055897.)
64. Jungermann, J., Lerch, M. M., Weidenbach, H., Lutz, M. P., Kruger, B. & Adler, G. 1995 Disassembly of rat pancreatic acinar cell cytoskeleton during supramaximal secretagogue stimulation. Am. J. Physiol. 268, G328-G338.
65. Jyotheeswaran, S., Li, P., Chang, T. M. & Chey, W. Y. 2000 Endogenous nitric oxide mediates pancreatic exocrine secretion stimulated by secretin and cholecystokinin in rats. Pancreas 20, 401-407. (doi:10.1097/00006676-200005000-00011.)
66. Kawabata, A., Kuroda, R., Nishida, M., Nagata, N., Sakaguchi, Y., Kawao, N., Nishikawa, H., Arizono, N. & Kawai, K. 2002 Protease-activated receptor-2 (PAR-2) in the pancreas and parotid gland: immunolocalization and involvement of nitric oxide in the evoked amylase secretion. Life Sci. 71, 2435-2446. (doi:10.1016/S0024-3205(02)02044-1.)
67. Kirchgessner, A. L., Liu, M. T. & Gershon, M. D. 1994 NADPH diaphorase (nitric oxide synthase)-containing nerves in the enteropancreatic innervation: sources, co-stored neuropeptides, and pancreatic function. J. Comp. Neurol. 342, 115-130. (doi:10.1002/cne.903420111.)
68. Klonowski-Stumpe, H., Schreiber, R., Grolik, M., Schulz, H. U., Haussinger, D. & Niederau, C. 1997 Effect of oxidative stress on cellular functions and cytosolic free calcium of rat pancreatic acinar cells. Am. J. Physiol. 272, G1489-G1498.
69. Kolaja, K. L., Bell, R. R., Janssen, D., Manning, P. T., Schlosser, M. J. & Khan, K. N. 2004 Evaluation of the long-term pancreatic effects of constitutive nitric oxide synthase inhibition in dogs. Inflammopharmacology 12, 33-45. (doi:10.1163/156856004773121356.)
70. Konig, P., Dedio, J., Muller-Esterl, W. & Kummer, W. 2002 Distribution of the novel eNOS-interacting protein NOSIP in the liver, pancreas, and gastrointestinal tract of the rat. Gastroenterology 123, 314-324. (doi:10.1053/gast.2002.34212.)
71. Konturek, S. J., Bilski, J., Konturek, P. K., Cieszkowski, M. & Pawlik, W. 1993 Role of endogenous nitric oxide in the control of canine pancreatic secretion and blood flow. Gastroenterology 104, 896-902.
72. Konturek, S. J., Szlachcic, A., Dembinski, A., Warzecha, Z., Jaworek, J. & Stachura, J. 1994 Nitric oxide in pancreatic secretion and hormone-induced pancreatitis in rats. Int. J. Pancreatol. 15, 19-28.
73. Konturek, J. W., Hengst, K., Kulesza, E., Gabryelewicz, A., Konturek, S. J. & Domschke, W. 1997 Role of endogenous nitric oxide in the control of exocrine and endocrine pancreatic secretion in humans. Gut 40, 86-91.
74. Konturek, P. C., Jaworek, J., Maniatoglou, A., Bonior, J., Meixner, H., Konturek, S. J. & Hahn, E. G. 2002 Leptin modulates the inflammatory response in acute pancreatitis. Digestion 65, 149-160. (doi:10.1159/000064935.)
75. Kozlov, A. V., Staniek, K. & Nohl, H. 1999 Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett. 454, 127-130. (doi:10.1016/S0014-5793(99)00788-7.)
76. Kruse, P., Anderson, M. E. & Loft, S. 2001 Minor role of oxidative stress during intermediate phase of acute pancreatitis in rats. Free Radic. Biol. Med. 30, 309-317. (doi:10.1016/S0891-5849(00)00472-X.)
77. Lacza, Z., Snipes, J. A., Zhang, J., Horvath, E. M., Figueroa, J. P., Szabo, C. & Busija, D. W. 2003 Mitochondrial nitric oxide synthase is not eNOS, nNOS or iNOS. Free Radic. Biol. Med. 35, 1217-1228. (doi:10.1016/S0891-5849(03) 00510-0.)
78. Lerch, M. M. & Adler, G. 1994 Experimental animal models of acute pancreatitis. Int. J. Pancreatol. 15, 159-170.
79. Lomis, T. J. et al. 1995 First place winner of the Conrad Jobst Award in the gold medal paper competition. Nitric oxide synthase inhibitors N-monomethylarginine and aminoguanidine prevent the progressive and severe hypotension associated with a rat model of pancreatitis. Am. Surg. 61, 7-10.
80. Looms, D., Tritsaris, K., Pedersen, A. M., Nauntofte, B. & Dissing, S. 2002 Nitric oxide signalling in salivary glands. J. Oral Pathol. Med. 31, 569-584. (doi:10.1034/j.1600-0714.2002.00047.x.)
81. 2+ signals between pancreatic beta-cells. Am. J. Physiol. Endocrinol. Metab. 285, E1055-E1063.
82. Luthen, R., Niederau, C. & Grendell, J. H. 1995 Intrapancreatic zymogen activation and levels of ATP and glutathione during caerulein pancreatitis in rats. Am. J. Physiol. 268, G592-G604.
83. Maczka, M., Thor, P., Bilski, J. & Konturek, S. J. 1994 Nitric oxide and the interrelation between intestinal motility and pancreatic secretion in fasted and fed dogs. J. Physiol. Pharmacol. 45, 285-298.
84. Millar, T. M., Stevens, C. R., Benjamin, N., Eisenthal, R., Harrison, R. & Blake, D. R. 1998 Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Lett. 427, 225-228. (doi:10.1016/S0014-5793(98)00430-X.)
85. Mizunuma, T., Kawamura, S. & Kishino, Y. 1984 Effects of injecting excess arginine on rat pancreas. J. Nutr. 114, 467-471.
86. Molero, X., Guarner, F., Salas, A., Mourelle, M., Puig, V. & Malagelada, J. R. 1995 Nitric oxide modulates pancreatic basal secretion and response to cerulein in the rat: effects in acute pancreatitis. Gastroenterology 108, 1855-1862. (doi:10.1016/0016-5085(95)90150- 7.)
87. Moncada, S. & Erusalimsky, J. D. 2002 Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell Biol. 3, 214-220. (doi:10.1038/nrm762.)
88. Nakada, S., Ishikawa, T., Yamamoto, Y., Kaneko, Y. & Nakayama, K. 2003 Constitutive nitric oxide synthases in rat pancreatic islets: direct imaging of glucose-induced nitric oxide production in beta-cells. Pflugers Arch. 447, 305-311. (doi:10.1007/s00424-003-1176-y.)
89. Nam, S. W., Seo, D. W., Sung, D. S., Han, J. W., Hong, S. Y. & Lee, H. W. 1998 Nitric oxide synthase from bovine pancreas: purification and characterization. Arch. Pharm. Res. 21, 128-134.
90. Namkung, W., Han, W., Luo, X., Muallem, S., Cho, K. H., Kim, K. H. & Lee, M. G. 2004 Protease-activated receptor 2 exerts local protection and mediates some systemic complications in acute pancreatitis. Gastroenterology 126, 1844-1859. (doi:10.1053/j.gastro.2004.03. 019.)
91. Nathan, C. 2003 Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J. Clin. Invest. 111, 769-778. (doi:10.1172/JCI200318174.)
92. Neuschwander-Tetri, B. A., Barnidge, M. & Janney, C. G. 1994 Cerulein-induced pancreatic cysteine depletion: prevention does not diminish acute pancreatitis in the mouse. Gastroenterology 107, 824-830.
93. Neuschwander-Tetri, B. A., Presti, M. E. & Wells, L. D. 1997 Glutathione synthesis in the exocrine pancreas. Pancreas 14, 342-349.
94. Niederau, C., Schultz, H. U. & Letko, G. 1991 Involvement of free radicals in the pathophysiology of chronic pancreatitis: potential of treatment with antioxidant and scavenger substances. Klin. Wochenschr. 69, 1018-1024. (doi:10.1007/BF01645151.)
95. Niederau, C., Klonowski, H., Schulz, H. U., Sarbia, M., Luthen, R. & Haussinger, D. 1996 Oxidative injury to isolated rat pancreatic acinar cells vs. isolated zymogen granules. Free Radic. Biol. Med. 20, 877-886. (doi:10.1016/0891-5849(95)02153-1.)
96. Nonaka, A., Manabe, T., Asano, N., Kyogoku, T., Imanishi, K., Tamura, K., Tobe, T., Sugiura, Y. & Makino, K. 1989a Direct ESR measurement of free radicals in mouse pancreatic lesions. Int. J. Pancreatol. 5, 203-211.
97. Nonaka, A., Manabe, T., Tamura, K., Asano, N., Imanishi, K. & Tobe, T. 1989b Changes of xanthine oxidase, lipid peroxide and superoxide dismutase in mouse acute pancreatitis. Digestion 43, 41-46.
98. Nonaka, A., Manabe, T., Kyogoku, T., Tamura, K. & Tobe, T. 1990 Changes in lipid peroxide and oxygen radical scavengers in cerulein-induced acute pancreatitis. Imbalance between the offense and defense systems. Digestion 47, 130-137.
99. Nonaka, A., Manabe, T. & Tobe, T. 1991 Effect of a new synthetic ascorbic acid derivative as a free radical scavenger on the development of acute pancreatitis in mice. Gut 32, 528-532.
100. Nonaka, A., Manabe, T., Kyogoku, T., Tamura, K. & Tobe, T. 1992 Evidence for a role of free radicals by synthesized scavenger, 2-octadecylascorbic acid, in cerulein-induced mouse acute pancreatitis. Dig. Dis. Sci. 37, 274-279. (doi:10.1007/BF01308183.)
101. Nordback, I. H. & Cameron, J. L. 1993 The mechanism of conversion of xanthine dehydrogenase to xanthine oxidase in acute pancreatitis in the canine isolated pancreas preparation. Surgery 113, 90-97.
102. Obermaier, R., Von Dobschuetz, E., Benthues, A., Ansorge, N., Schareck, W., Hopt, U. T. & Benz, S. 2004a Exogenous and endogenous nitric oxide donors improve post-ischemic tissue oxygenation in early pancreatic ischemia/reperfusion injury in the rat. Eur. Surg. Res. 36, 219-225. (doi:10.1159/000078856.)
103. Obermaier, R., Von Dobschuetz, E., Muhs, O., Keck, T., Drognitz, O., Jonas, L., Schareck, W., Hopt, U. T. & Benz, S. 2004b Influence of nitric oxide on microcirculation in pancreatic ischemia/reperfusion injury: an intravital microscopic study. Transpl. Int. 17, 208-214. (doi:10.1111/j.1432-2277.2004.tb00430.x.)
104. Ozturk, M. et al. 2003 The role of inducible nitric oxide synthase inhibitor, meropenem, and taurine in experimental acute necrotizing pancreatitis. Pancreas 26, 357-362. (doi:10.1097/00006676- 200305000-00008.)
105. Pandol, S. J. & Schoeffield-Payne, M. S. 1990 Cyclic GMP mediates the agonist-stimulated increase in plasma membrane calcium entry in the pancreatic acinar cell. J. Biol. Chem. 265, 12 846-12 853.
106. Patel, A. G., Toyama, M. T., Nguyen, T. N., Cohen, G. A., Ignarro, L. J., Reber, H. A. & Ashley, S. W. 1995 Role of nitric oxide in the relationship of pancreatic blood flow and exocrine secretion in cats. Gastroenterology 108, 1215-1220. (doi:10.1016/0016-5085(95)90222-8.)
107. Qader, S. S., Ekelund, M., Andersson, R., Obermuller, S. & Salehi, A. 2003 Acute pancreatitis, expression of inducible nitric oxide synthase and defective insulin secretion. Cell Tissue Res. 313, 271-279. (doi:10.1007/s00441-003-0764-7.)
108. Qui, B., Mei, Q. B., Ma, J. J. & Korsten, M. A. 2001 Susceptibility to cerulein-induced pancreatitis in inducible nitric oxide synthase-deficient mice. Pancreas 23, 89-93. (doi:10.1097/00006676-200107000-00013.)
109. Rahman, S. H., Ibrahim, K., Larvin, M., Kingsnorth, A. & McMahon, M. J. 2004 Association of antioxidant enzyme gene polymorphisms and glutathione status with severe acute pancreatitis. Gastroenterology 126, 1312-1322. (doi:10.1053/j.gastro.2004.02.002.)
110. Rau, B., Poch, B., Gansauge, F., Bauer, A., Nussler, A. K., Nevalainen, T., Schoenberg, M. H. & Beger, H. G. 2000 Pathophysiologic role of oxygen free radicals in acute pancreatitis: initiating event or mediator of tissue damage? Ann. Surg. 231, 352-360. (doi:10.1097/00000658-200003000- 00008.)
111. Rau, B., Bauer, A., Wang, A., Gansauge, F., Weidenbach, H., Nevalainen, T., Poch, B., Beger, H. G. & Nussler, A. K. 2001 Modulation of endogenous nitric oxide synthase in experimental acute pancreatitis: role of anti-ICAM-1 and oxygen free radical scavengers. Ann. Surg. 233, 195-203. (doi:10.1097/00000658-200102000-00008.)
112. Reinheckel, T., Nedelev, B., Prause, J., Augustin, W., Schulz, H. U., Lippert, H. & Halangk, W. 1998 Occurrence of oxidatively modified proteins: an early event in experimental acute pancreatitis. Free Radic. Biol. Med. 24, 393-400. (doi:10.1016/S0891-5849(97)00271-2.)
113. Rosado, J. A., Gonzalez, A., Salido, G. M. & Pariente, J. A. 2002 Effects of reactive oxygen species on actin filament polymerisation and amylase secretion in mouse pancreatic acinar cells. Cell. Signal. 14, 547-556. (doi:10.1016/S0898-6568(01)00273-X.)
114. Salehi, A., Carlberg, M., Henningson, R. & Lundquist, I. 1996 Islet constitutive nitric oxide synthase: biochemical determination and regulatory function. Am. J. Physiol. 270, C1634-C1641.
115. Sanchez-Bernal, C., Garcia-Morales, O. H., Dominguez, C., Martin-Gallan, P., Calvo, J. J., Ferreira, L. & Perez-Gonzalez, N. 2004 Nitric oxide protects against pancreatic subcellular damage in acute pancreatitis. Pancreas 28, e9-e15. (doi:10.1097/00006676-200401000-00021.)
116. Sandstrom, P., Gasslander, T., Sundqvist, T., Franke, J. & Svanvik, J. 2003 Depletion of serum L-arginine in patients with acute pancreatitis. Pancreas 27, 261-266. (doi:10.1097/00006676- 200310000-00012.)
117. Sandstrom, P., Brooke-Smith, M. E., Thomas, A. C., Grivell, M. B., Saccone, G. T., Toouli, J. & Svanvik, J. 2005 Highly selective inhibition of inducible nitric oxide synthase ameliorates experimental acute pancreatitis. Pancreas 30, e10-e15.
118. Sanfey, H., Bulkley, G. B. & Cameron, J. L. 1984 The role of oxygen-derived free radicals in the pathogenesis of acute pancreatitis. Ann. Surg. 200, 405-413.
119. Sato, K., Akaike, T., Sawa, T., Miyamoto, Y., Suga, M., Ando, M. & Maeda, H. 1997 Nitric oxide generation from hydroxyurea via copper-catalyzed peroxidation and implications for pharmacological actions of hydroxyurea. Jpn. J. Cancer Res. 88, 1199-1204.
120. Satoh, A., Shimosegawa, T., Kimura, K., Moriizumi, S., Masamune, A., Koizumi, M. & Toyota, T. 1998 Nitric oxide is overproduced by peritoneal macrophages in rat taurocholate pancreatitis: the mechanism of inducible nitric oxide synthase expression. Pancreas 17, 402-411.
121. Schoenberg, M. H., Buchler, M., Baczako, K., Bultmann, B., Younes, M., Gasper, M., Kirchmayr, R. & Beger, H. G. 1991 The involvement of oxygen radicals in acute pancreatitis. Klin. Wochenschr. 69, 1025-1031. (doi:10.1007/BF01645152.)
122. Schoenberg, M. H., Buchler, M., Younes, M., Kirchmayr, R., Bruckner, U. B. & Beger, H. G. 1994 Effect of antioxidant treatment in rats with acute hemorrhagic pancreatitis. Dig. Dis. Sci. 39, 1034-1040. (doi:10.1007/BF02087555.)
123. Schoenberg, M. H., Buchler, M., Pietrzyk, C., Uhl, W., Birk, D., Eisele, S., Marzinzig, M. & Beger, H. G. 1995 Lipid peroxidation and glutathione metabolism in chronic pancreatitis. Pancreas 10, 36-43.
124. Schulz, H. U., Niederau, C., Klonowski-Stumpe, H., Halangk, W., Luthen, R. & Lippert, H. 1999 Oxidative stress in acute pancreatitis. Hepatogastroenterology 46, 2736-2750.
125. Schulz, H. U. et al. 2001 Randomized, placebo-controlled trial of lazaroid effects on severe acute pancreatitis in rats. Crit. Care Med. 29, 861-869. (doi:10.1097/00003246-200104000-00035.)
126. Sevillano, S., De la Mano, A. M., De Dios, I., Ramudo, L. & Manso, M. A. 2003 Major pathological mechanisms of acute pancreatitis are prevented by N-acetylcysteine. Digestion 68, 34-40. (doi:10.1159/ 000073223.)
127. Sharma, A., Tao, X., Gopal, A., Ligon, B., Andrade-Gordon, P., Steer, M. L. & Perides, G. 2005 Protection against acute pancreatitis by activation of protease-activated receptor-2. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G388-G395. (doi:10.1152/ajpgi.00341.2004.)
128. Simsek, I. et al. 2001 Inhibition of inducible nitric oxide synthase reduces bacterial translocation in a rat model of acute pancreatitis. Pancreas 23, 296-301. (doi:10.1097/00006676-200110000-00011.)
129. Song, A. M., Bhagat, L., Singh, V. P., Van Acker, G. G., Steer, M. L. & Saluja, A. K. 2002 Inhibition of cyclooxygenase-2 ameliorates the severity of pancreatitis and associated lung injury. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G1166-G1174.
130. Stamler, J. S., Simon, D. I., Osborne, J. A., Mullins, M., Jaraki, O., Michel, T., Singel, D. & Loscalzo, J. 1992 Exposure of sulfhydryl containing proteins to nitric oxide and endothelium-derived relaxing factor confers novel bioactivity and modulates their intrinsic functional properties. In The biology of nitric oxide (ed. S. Moncada, M. Marietta, J. Hibbs & A. Higgs), pp. 20-23. London: Portland Press.
131. Steer, M. L., Rutledge, P. L., Powers, R. E., Saluja, M. & Saluja, A. K. 1991 The role of oxygen-derived free radicals in two models of experimental acute pancreatitis: effects of catalase, superoxide dismutase, dimethylsulfoxide, and allopurinol. Klin. Wochenschr. 69, 1012-1017. (doi:10.1007/BF01645149.)
132. Suzuki, H., Suematsu, M., Miura, S., Asako, H., Kurose, I., Ishii, H., Houzawa, S. & Tsuchiya, M. 1993 Xanthine oxidase-mediated intracellular oxidative stress in response to cerulein in rat pancreatic acinar cells. Pancreas 8, 465-470.
133. 2+ spiking in rat exocrine pancreas. Biochim. Biophys. Acta 1454, 19-30.
134. Takacs, T., Czako, L., Morschl, E., Laszlo, F., Tiszlavicz, L., Rakonczay Jr, Z. & Lonovics, J. 2002 The role of nitric oxide in edema formation in L-arginine-induced acute pancreatitis. Pancreas 25, 277-282. (doi:10.1097/00006676-200210000-00010.)
135. Tanaka, S., Kamiike, W., Kosaka, H., Ito, T., Kumura, E., Shiga, T. & Matsuda, H. 1996 Detection of nitric oxide production and its role in pancreatic ischemia-reperfusion in rats. Am. J. Physiol. 271, G405-G409.
136. Tapia, J. A., Camello, C., Jensen, R. T. & Garcia, L. J. 1999 EGF stimulates tyrosine phosphorylation of focal adhesion kinase (p125FAK) and paxillin in rat pancreatic acini by a phospholipase C-independent process that depends on phosphatidylinositol 3-kinase, the small GTP-binding protein, p21rho, and the integrity of the actin cytoskeleton. Biochim. Biophys. Acta 1448, 486-499. (doi:10.1016/S0167-4889(98)00157-8.)
137. Telek, G., Regoly-Merei, J., Kovacs, G. C., Simon, L., Nagy, Z., Hamar, J. & Jakab, F. 2001 The first histological demonstration of pancreatic oxidative stress in human acute pancreatitis. Hepatogastroenterology 48, 1252-1258.
138. 2+ spikes evoked by the thiol reagent thimerosal in both intact and internally perfused single pancreatic acinar cells. Pflugers Arch. 422, 173-178. (doi:10.1007/BF00370417.)
139. Trulsson, L. M., Svanvik, J., Permert, J. & Gasslander, T. 2001 Cholecystokinin octapeptide induces both proliferation and apoptosis in the rat pancreas. Regul. Pept. 98, 41-48. (doi:10.1016/S0167-0115(00) 00223-8.)
140. Trulsson, L. M., Gasslander, T., Sundqvist, T. & Svanvik, J. 2002 The influence of nitric oxide on basal and cholecystokinin-8-induced proliferation and apoptosis in the rat pancreas. Regul. Pept. 106, 97-104. (doi:10.1016/S0167-0115(02)00056-3.)
141. Trulsson, L. M., Gasslander, T. & Svanvik, J. 2004 Cholecystokinin-8-induced hypoplasia of the rat pancreas: influence of nitric oxide on cell proliferation and programmed cell death. Basic Clin. Pharmacol. Toxicol. 95, 183-190.
142. Tsai, K., Wang, S. S., Chen, T. S., Kong, C. W., Chang, F. Y., Lee, S. D. & Lu, F. J. 1998 Oxidative stress: an important phenomenon with pathogenetic significance in the progression of acute pancreatitis. Gut 42, 850-855.
143. Um, S. H. et al. 2003 The role of nitric oxide in experimental cerulein induced pancreatitis. J. Korean Med. Sci. 18, 520-526.
144. Umehara, K., Kataoka, K., Ogura, T., Esumi, H., Kashima, K., Ibata, Y. & Okamura, H. 1997 Comparative distribution of nitric oxide synthase (NOS) in pancreas of the dog and rat: immunocytochemistry of neuronal type NOS and histochemistry of NADPH-diaphorase. Brain Res. Bull. 42, 469-478. (doi:10.1016/S0361-9230(96)00374-7.)
145. Urunuela, A., Sevillano, S., De la Mano, A. M., Manso, M. A., Orfao, A. & De Dios, I. 2002 Time-course of oxygen free radical production in acinar cells during acute pancreatitis induced by pancreatic duct obstruction. Biochim. Biophys. Acta 1588, 159-164.
146. 2+ entry mediated by store depletion, S-nitrosylation, and TRP3 channels. Comparison of coupling and function. J. Biol. Chem. 275, 28 562-28 568. (doi:10.1074/jbc.M003147200.)
147. Vaquero, E., Molero, X., Puig-Divi, V. & Malagelada, J. R. 1998 Contrasting effects of circulating nitric oxide and nitrergic transmission on exocrine pancreatic secretion in rats. Gut 43, 684-691.
148. Vaquero, E., Gukovsky, I., Zaninovic, V., Gukovskaya, A. S. & Pandol, S. J. 2001 Localized pancreatic NF-kappaB activation and inflammatory response in taurocholate-induced pancreatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 280, G1197-G1208.
149. Viola, G., Al Mufti, R. A., Sohail, M., Williamson, R. C. & Mathie, R. T. 2000 Nitric oxide induction in a rat model of selective pancreatic ischemia and reperfusion. Hepatogastroenterology 47, 1250-1255.
150. Wacke, R. et al. 1998 Up-regulation of cytochrome P450 1A2, 2C9, and 2E1 in chronic pancreatitis. Pancreas 16, 521-528.
151. Wallig, M. A. 1998 Xenobiotic metabolism, oxidant stress and chronic pancreatitis. Focus on glutathione. Digestion 59(Suppl. 4), 13-24. (doi:10.1159/000051439.)
152. Warzecha, Z., Dembinski, A., Ceranowicz, P., Jaworek, J., Konturek, P. C., Dembinski, M., Bilski, J. & Konturek, S. J. 2002 Influence of leptin administration on the course of acute ischemic pancreatitis. J. Physiol. Pharmacol. 53, 775-790.
153. Watson, E. L., Jacobson, K. L., Singh, J. C. & Ott, S. M. 1999 Nitric oxide acts independently of cGMP to modulate capacitative Ca(2+) entry in mouse parotid acini. Am. J. Physiol. 277, C262-C270.
154. 2+ amplifies oxygen radical-induced alterations of the ultrastructure and the energy metabolism of isolated rat pancreatic acinar cells. Digestion 59, 175-185. (doi:10.1159/000007486.)
155. Werner, J., Rivera, J., Fernandez-del Castillo, C., Lewandrowski, K., Adrie, C., Rattner, D. W. & Warshaw, A. L. 1997 Differing roles of nitric oxide in the pathogenesis of acute edematous versus necrotizing pancreatitis. Surgery 121, 23-30. (doi:10.1016/S0039-6060(97)90178-1.)
156. Werner, J., Fernandez-del Castillo, C., Rivera, J. A., Kollias, N., Lewandrowski, K. B., Rattner, D. W. & Warshaw, A. L. 1998 On the protective mechanisms of nitric oxide in acute pancreatitis. Gut 43, 401-407.
157. Wisner, J., Green, D., Ferrell, L. & Renner, I. 1988 Evidence for a role of oxygen derived free radicals in the pathogenesis of caerulein induced acute pancreatitis in rats. Gut 29, 1516-1523.
158. Worl, J., Wiesand, M., Mayer, B., Greskotter, K. R. & Neuhuber, W. L. 1994 Neuronal and endothelial nitric oxide synthase immunoreactivity and NADPH-diaphorase staining in rat and human pancreas: influence of fixation. Histochemistry 102, 353-364.
159. Wrenn, R. W., Currie, M. G. & Herman, L. E. 1994 Nitric oxide participates in the regulation of pancreatic acinar cell secretion. Life Sci. 55, 511-518. (doi:10.1016/0024-3205(94)00743-8.)
160. 2+ influx. J. Biol. Chem. 269, 12 645-12 653.
161. Xu, X., Zeng, W., Diaz, J., Lau, K. S., Gukovskaya, A. C., Brown, R. J., Pandol, S. J. & Muallem, S. 1997 nNOS and Ca2+ influx in rat pancreatic acinar and submandibular salivary gland cells. Cell Calcium 22, 217-228. (doi:10.1016/S0143-4160(97)90015-4.)
162. Yago, M. D., Tapia, J. A., Salido, G. M., Adeghate, E., Juma, L. M., Martinez-Victoria, E., Manas, M. & Singh, J. 2002 Effect of sodium nitroprusside and 8-bromo cyclic GMP on nerve-mediated and acetylcholine-evoked secretory responses in the rat pancreas. Br. J. Pharmacol. 136, 49-56. (doi:10.1038/sj.bjp.0704693.)
163. 2+ entry and amylase secretion from the rat pancreas. Pflugers Arch. 434, 25-37. (doi:10.1007/S004240050359.)
164. Yu, J. H., Lim, J. W., Namkung, W., Kim, H. & Kim, K. H. 2002 Suppression of cerulein-induced cytokine expression by antioxidants in pancreatic acinar cells. Lab. Invest. 82, 1359-1368.
165. Yuan, C. H., Liu, Y. F., Cheng, Y., Zhao, N., Li, G. C., Liang, J. & He, S. G. 2004 Protective effects of L-arginine on reperfusion injury after pancreaticoduodenal transplantation in rats. Hepatobiliary Pancreat. Dis. Int. 3, 349-354.
166. Zaragoza, C., Ocampo, C. J., Saura, M., Bao, C., Leppo, M., Lafond-Walker, A., Thiemann, D. R., Hruban, R. & Lowenstein, C. J. 1999 Inducible nitric oxide synthase protection against coxsackievirus pancreatitis. J. Immunol. 163, 5497-5504.
167. Zoucas, E., Nilsson, C. & Ihse, I. 2001 Differential roles of endogenous nitric oxide on neural regulation of basal exocrine pancreatic secretion in intact and denervated pancreas. Pancreatology 1, 96-101. (doi:10.1159/000055800.)