Recent advances in the investigation of pancreatic inflammation induced by large doses of basic amino acids in rodents

Laboratory Investigation

Volumn 94, Issue 2, 2014, Pages 138-149

  Kui, Balázs ^a   Balla, Zsolt ^a   Végh, Eszter T ^a   Pallagi, Petra ^a   Venglovecz, Viktória ^a   Iványi, Béla ^a   Takács, Tamás ^a   Hegyi, Péter ^a   Rakonczay, Zoltán ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

Author keywords

basic amino acids; L arginine; L lysine; L ornithine; pancreas; pancreatitis

Indexed keywords

ADRENALIN; AMINO ACID; ARGININE; BETACELLULIN; DOPAMINE; HEAT SHOCK PROTEIN; LYSINE; NESTIN; NORADRENALIN; ORNITHINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; POLYAMINE; SEROTONIN; SOMATOMEDIN BINDING PROTEIN 4; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR;

ACUTE HEMORRHAGIC PANCREATITIS; ACUTE PANCREATITIS; ADRENALIN BLOOD LEVEL; AMINO ACID METABOLISM; AUTONOMIC NERVOUS SYSTEM; BLOOD CELL; CELL PROLIFERATION; CHRONIC PANCREATITIS; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM STRESS; EXPERIMENTAL PANCREATITIS; GENE; HOMEOSTASIS; HUMAN; KIDNEY INJURY; LIVER INJURY; LUNG INJURY; MODULATION; MORPHOLOGY; MOUSE MODEL; NITROSATIVE STRESS; NONHUMAN; NORADRENALIN BLOOD LEVEL; OXIDATIVE STRESS; PANCREAS; PANCREAS INJURY; PANCREATIC REGENERATION; PARASYMPATHETIC TONE; PATHOGENESIS; PRIORITY JOURNAL; RAT MODEL; REGENERATING GENE 4; REVIEW; RODENT MODEL; SEROTONIN BLOOD LEVEL; TISSUE REGENERATION; TRANSCRIPTION INITIATION;

AMINO ACIDS, BASIC; ANIMALS; ARGININE; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; HISTOLOGICAL TECHNIQUES; LYSINE; MICE; MOLECULAR STRUCTURE; ORNITHINE; OXIDATIVE STRESS; PANCREAS; PANCREATITIS; RATS; REGENERATION;

EID: 84893245062     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2013.143     Document Type: Review

References (104)

1. Hegyi P, Perides G, Steer ML, et al. Commonly Employed Rodent Models of Experimental Acute Pancreatitis: Their Strenghts and Weakness, Relevance to Human Disease, Selection, and Appropriate Use. The Pancreapedia Exocrine Pancreas Knowledge Base 2013; doi:10.3998/panc.2013.4; http://www.pancreapedia. org/reviews/commonly-employed-rodent-models-of-experimental-acutepancreatitis- their-strengths-and-weakn.
2. Su KH, Cuthbertson C, Christophi C. Review of experimental animal models of acute pancreatitis. HPB 2006;8:264-286.
3. Mizunuma T, Kawamura S, Kishino Y. Effects of injecting excess arginine on rat pancreas. J Nutr 1984;114:467-471.
4. Aho HJ, Koskensalo SM, Nevalainen TJ. Experimental pancreatitis in the rat. Sodium taurocholate-induced acute haemorrhagic pancreatitis. Scand J Gastroenterol 1980;15:411-416.
5. Lampel M, Kern HF. Acute interstitial pancreatitis in the rat induced by excessive doses of a pancreatic secretagogue. Virchows Arch A Pathol Anat Histol 1977;373:97-117.
6. Lombardi B, Estes LW, Longnecker DS. Acute hemorrhagic pancreatitis (massive necrosis) with fat necrosis induced in mice by DL-ethionine fed with a choline-deficient diet. Am J Pathol 1975;79:465-480.
7. Hegyi P, Rakonczay Jr Z, Sá ri R, et al. L-arginine-induced experimental pancreatitis. World J Gastroenterol 2004;10:2003-2009.
8. Morris Jr. SM. Enzymes of arginine metabolism. J Nutr 2004;134:2743S-2747S, discussion 2765S-2767S.
9. Rakonczay Jr Z, Hegyi P, Dó sa S, et al. A new severe acute necrotizing pancreatitis model induced by L-ornithine in rats. Crit Care Med 2008; 36:2117-2127.
10. Biczó G, Hegyi P, Dó sa S, et al. The crucial role of early mitochondrial injury in L-lysine-induced acute pancreatitis. Antioxid Redox Signal 2011;15:2669-2681.
11. Biczó G, Hegyi P, Dó sa S, et al. Aliphatic, but not imidazole, basic amino acids cause severe acute necrotizing pancreatitis in rats. Pancreas 2011;40:486-487.
12. Huang W, Chvanov M, Criddle D, et al. L-histidine-but not L-arginineinduced acute pancreatitis in mice involves cyclophilin D-dependent opening of mitochondrial permeability transition pore. Pancreatology 2013;13:S8.
13. Dawra R, Sharif R, Phillips P, et al. Development of a new mouse model of acute pancreatitis induced by administration of L-arginine. Am J Physiol Gastrointest Liver Physiol 2007;292:G1009-G1018.
14. Dawra R, Saluja AK. L-arginine-induced experimental acute pancreatitis. The Pancreapedia Exocrine Pancreas Knowledge Base 2012; doi:10.3998/panc.2012.6; http://www.pancreapedia.org/?q=node/1394.
15. Cui HF, Bai ZL. Protective effects of transplanted and mobilized bone marrow stem cells on mice with severe acute pancreatitis. World J Gastroenterol 2003;9:2274-2277.
16. Yuan H, Jin X, Sun J, et al. Protective effect of HMGB1 a box on organ injury of acute pancreatitis in mice. Pancreas 2009;38:143-148.
17. Singh VP, Bhagat L, Navina S, et al. Protease-activated receptor-2 protects against pancreatitis by stimulating exocrine secretion. Gut 2007;56:958-964.
18. Sakai A, Nishiumi S, Shiomi Y, et al. Metabolomic analysis to discover candidate therapeutic agents against acute pancreatitis. Arch Biochem Biophys 2012;522:107-120.
19. Lunova M, Zizer E, Kucukoglu O, et al. Hsp72 overexpression accelerates the recovery from caerulein-induced pancreatitis. PloS One 2012;7:e39972.
20. Huang L, Wang M-H, Cheng Z-Y, et al. Effects of Chai-Qin-Cheng-Qi decoction on acute pancreatitis-associated lung injury in mice with acute necrotizing pancreatitis. Chin J Integr Med 2012; e-pub ahead of print.
21. Bedrosian AS, Nguyen AH, Hackman M, et al. Dendritic cells promote pancreatic viability in mice with acute pancreatitis. Gastroenterology 2011;141:1915-1926, e1-14.
22. Elder ASF, Saccone GTP, Bersten AD, et al. L-Arginine-induced acute pancreatitis results in mild lung inflammation without altered respiratory mechanics. Exp Lung Res 2011;37:1-9.
23. Kitajima S, Kishino Y. Pancreatic damage produced by injecting excess lysine in rats. Virchows Arch B Cell Pathol Incl Mol Pathol 1985;49:295-305.
24. Abdulla A, Awla D, Hartman H, et al. Role of platelets in experimental acute pancreatitis. Br J Surg 2011;98:93-103.
25. Biradar S, Veeresh B. Protective effect of lawsone on L-Arginine induced acute pancreatitis in rats. Indian J Exp Biol 2013;51:256-261.
26. Chen J, Cai QP, Shen PJ, et al. Netrin-1 protects against L-Arginineinduced acute pancreatitis in mice. PloS One 2012;7:e46201.
27. Merza M, Wetterholm E, Zhang S, et al. Inhibition of geranylgeranyltransferase attenuates neutrophil accumulation and tissue injury in severe acute pancreatitis. J Leukoc Biol 2013;94: 493-502.
28. Yenicerioglu A, Cetinkaya Z, Girgin M, et al. Effects of trimetazidine in acute pancreatitis induced by L-arginine. Can J Surg J Can Chir 2013;56:175-179.
29. Hu G, Shen J, Cheng L, et al. Reg4 protects against acinar cell necrosis in experimental pancreatitis. Gut 2011;60:820-828.
30. Sung KF, Odinokova IV, Mareninova OA, et al. Prosurvival Bcl-2 proteins stabilize pancreatic mitochondria and protect against necrosis in experimental pancreatitis. Exp Cell Res 2009;315: 1975-1989.
31. Kong XY, Du YQ, Li L, et al. Plasma miR-216a as a potential marker of pancreatic injury in a rat model of acute pancreatitis. World J Gastroenterol 2010;16:4599-4604.
32. Bohus E, Coen M, Keun HC, et al. Temporal metabonomic modeling of l-arginine-induced exocrine pancreatitis. J Proteome Res 2008;7: 4435-4445.
33. Chen X, Sans MD, Strahler JR, et al. Quantitative organellar proteomics analysis of rough endoplasmic reticulum from normal and acute pancreatitis rat pancreas. J Proteome Res 2010;9:885-896.
34. Biczó G, Hegyi P, Berczi S, et al. Inhibition of arginase activity ameliorates L-arginine-induced acute pancreatitis in rats. Pancreas 2010;39:868-874.
35. Czakó L, Szabolcs A, Vajda A, et al. Hyperlipidemia induced by a cholesterol-rich diet aggravates necrotizing pancreatitis in rats. Eur J Pharmacol 2007;572:74-81.
36. Kishino Y, Takama S, Kitajima S. Ultracytochemistry of pancreatic damage induced by excess lysine. Virchows Arch B Cell Pathol Incl Mol Pathol 1986;52:153-167.
37. Kubisch CH, Sans MD, Arumugam T, et al. Early activation of endoplasmic reticulum stress is associated with arginine-induced acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 2006; 291:G238-G245.
38. Schild L, Matthias R, Stanarius A, et al. Induction of permeability transition in pancreatic mitochondria by cerulein in rats. Mol Cell Biochem 1999;195:191-197.
39. Gukovskaya AS, Gukovsky I, Jung Y, et al. Cholecystokinin induces caspase activation and mitochondrial dysfunction in pancreatic acinar cells. Roles in cell injury processes of pancreatitis. J Biol Chem 2002;277:22595-22604.
40. Shen J, Wan R, Hu G, et al. Involvement of thrombopoietin in acinar cell necrosis in L-arginine-induced acute pancreatitis in mice. Cytokine 2012;60:294-301.
41. Hartman H, Abdulla A, Awla D, et al. P-selectin mediates neutrophil rolling and recruitment in acute pancreatitis. Br J Surg 2012;99: 246-255.
42. Saeki K, Kanai T, Nakano M, et al. CCL2-induced migration and SOCS3-mediated activation of macrophages are involved in cerulein-induced pancreatitis in mice. Gastroenterology 2012;142:1010-1020, e9.
43. Moreira M, Matias JEF, Souza de CJF, et al. Action of tacrolimus in arginine induced experimental acute pancreatitis. Rev Colégio Bras Cir 2011;38:260-265.
44. Hyvonen MT, Merentie M, Uimari A, et al. Mechanisms of polyamine catabolism-induced acute pancreatitis. Biochem Soc Trans 2007; 35:326-330.
45. Alhonen L, Parkkinen JJ, Keinanen T, et al. Activation of polyamine catabolism in transgenic rats induces acute pancreatitis. Proc Natl Acad Sci USA 2000;97:8290-8295.
46. Herzig K-H, Janne J, Alhonen L. Acute pancreatitis induced by activation of the polyamine catabolism in gene-modified mice and rats overexpressing spermidine/spermine N1-acetyltransferase. Scand J Gastroenterol 2005;40:120-121.
47. Hyvonen MT, Herzig KH, Sinervirta R, et al. Activated polyamine catabolism in acute pancreatitis: alpha-methylated polyamine analogues prevent trypsinogen activation and pancreatitisassociated mortality. Am J Pathol 2006;168:115-122.
48. Biczó G, Hegyi P, Sinervirta R, et al. Characterization of polyamine homeostasis in l-ornithine-induced acute pancreatitis in rats. Pancreas 2010;39:1047-1056.
49. Booth DM, Mukherjee R, Sutton R, et al. Calcium and reactive oxygen species in acute pancreatitis: friend or foe? Antioxid Redox Signal 2011;15:2683-2698.
50. Leung PS, Chan YC. Role of oxidative stress in pancreatic inflammation. Antioxid Redox Signal 2009;11:135-165.
51. Hegyi P, Rakonczay Jr. Z. The role of nitric oxide in the physiology and pathophysiology of the exocrine pancreas. Antioxidants Redox Signal 2011;15:2723-2741.
52. Jacewicz D, Dabrowska A, Wyrzykowski D, et al. A novel biosensor for evaluation of apoptotic or necrotic effects of nitrogen dioxide during acute pancreatitis in rat. Sensors 2010;10:280-291.
53. Varga IS, Matkovics B, Czako L, et al. Oxidative stress changes in L-arginine-induced pancreatitis in rats. Pancreas 1997;14:355-359.
54. Czakó L, Takács T, Varga IS, et al. Involvement of oxygen-derived free radicals in L-arginine-induced acute pancreatitis. Dig Dis Sci 1998;43: 1770-1777.
55. Sidhu S, Pandhi P, Malhotra S, et al. Melatonin treatment is beneficial in pancreatic repair process after experimental acute pancreatitis. Eur J Pharmacol 2010;628:282-289.
56. Szabolcs A, Reiter RJ, Letoha T, et al. Effect of melatonin on the severity of L-arginine-induced experimental acute pancreatitis in rats. World J Gastroenterol 2006;12:251-258.
57. Rakonczay Jr Z, Jármay K, Kaszaki J, et al. NF-kappaB activation is detrimental in arginine-induced acute pancreatitis. Free Radic Biol Med 2003;34:696-709.
58. Onur E, Paksoy M, Baca B, et al. Hyperbaric oxygen and N-acetylcysteine treatment in L-arginine-induced acute pancreatitis in rats. J Investig Surg 2012;25:20-28.
59. Abdin AA, El-Hamid MAA, El-Seoud SHA, et al. Effect of pentoxifylline and/or alpha lipoic acid on experimentally induced acute pancreatitis. Eur J Pharmacol 2010;643:289-296.
60. Melo CM, Carvalho KMMB, Neves JCS, et al. Alpha,beta-amyrin, a natural triterpenoid ameliorates L-arginine-induced acute pancreatitis in rats. World J Gastroenterol 2010;16:4272-4280.
61. Hardman J, Jamdar S, Shields C, et al. Intravenous selenium modulates L-arginine-induced experimental acute pancreatitis. JOP 2005;6:431-437.
62. Dabrowska A, Jacewicz D, Aapińska A, et al. Pivotal participation of nitrogen dioxide in L-arginine induced acute necrotizing pancreatitis: protective role of superoxide scavenger 4-OH-TEMPO. Biochem Biophys Res Commun 2005;326:313-320.
63. Krajewski E, Krajewski J, Spodnik JH, et al. Changes in the morphology of the acinar cells of the rat pancreas in the oedematous and necrotic types of experimental acute pancreatitis. Folia Morphol 2005;64:292-303.
64. Takács T, Czakó L, Morschl E, et al. The role of nitric oxide in edema formation in L-arginine-induced acute pancreatitis. Pancreas 2002;25:277-282.
65. Sidhu S, Pandhi P, Malhotra S, et al. Beneficial effects of Emblica officinalis in L-arginine-induced acute pancreatitis in rats. J Med Food 2011;14:147-155.
66. Shields CJ, Delaney CP, Winter DC, et al. Induction of nitric oxide synthase is a key determinant of progression to pulmonary injury in experimental pancreatitis. Surg Infect 2006;7:501-511.
67. Matalka II, Mhaidat NM, Fatlawi LA. Antioxidant activity of simvastatin prevents L-arginine-induced acute toxicity of pancreas. Int J Physiol Pathophysiol Pharmacol 2013;5:102-108.
68. Chen H, Sun YP, Li Y, et al. Hydrogen-rich saline ameliorates the severity of l-arginine-induced acute pancreatitis in rats. Biochem Biophys Res Commun 2010;393:308-313.
69. Czakó L, Takács T, Varga IS, et al. The pathogenesis of L-arginineinduced acute necrotizing pancreatitis: inflammatory mediators and endogenous cholecystokinin. J Physiol Paris 2000;94:43-50.
70. Pereda J, Sabater L, Aparisi L, et al. Interaction between cytokines and oxidative stress in acute pancreatitis. Curr Med Chem 2006;13: 2775-2787.
71. Rakonczay Jr Z, Hegyi P, Takács T, et al. The role of NF-kappaB activation in the pathogenesis of acute pancreatitis. Gut 2008;57: 259-267.
72. Lechin F, van der Dijs B. Arginine-induced pancreatitis: involvement of the autonomic nervous system? Am J Physiol Gastrointest Liver Physiol 2008;294:G1450-G1451, author reply G1452.
73. Lechin F, Dijs B, Baez S, et al. The effects of oral arginine on neuroautonomic parameters in. J Appl Res 2006;6:201-213.
74. Wick EC, Hoge SG, Grahn SW, et al. Transient receptor potential vanilloid 1, calcitonin gene-related peptide, and substance P mediate nociception in acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 2006;290:G959-G969.
75. Wick EC, Pikios S, Grady EF, et al. Calcitonin gene-related peptide partially mediates nociception in acute experimental pancreatitis. Surgery 2006;139:197-201.
76. Neuhofer P, Liang S, Einwachter H, et al Deletion of IkBa activates RelA to reduce acute pancreatitis in mice through up-regulation of Spi2A. Gastroenterology 2013 144 192-201.
77. Molero X, Vaquero EC, Flández M, et al. Gene expression dynamics after murine pancreatitis unveils novel roles for Hnf1a in acinar cell homeostasis. Gut 2012;61:1187-1196.
78. Awla D, Zetterqvist AV, Abdulla A, et al. NFATc3 regulates trypsinogen activation, neutrophil recruitment, and tissue damage in acute pancreatitis in mice. Gastroenterology 2012;143:1352-1360, e1-7.
79. Zhou H, Liu L, Bai Y, et al. Damage of the interstitial cells of Cajal and myenteric neurons causing ileus in acute necrotizing pancreatitis rats. Surgery 2011;149:262-275.
80. Zhou H, Gao J, Wu W, et al. Octreotide ameliorates intestinal dysmotility by interstitial cells of Cajal protection in a rat acute necrotizing pancreatitis model. Pancreas 2011;40:1226-1233.
81. Hegyi P, Takács T, Jármay K, et al. Spontaneous and cholecystokininoctapeptide-promoted regeneration of the pancreas following L-arginine-induced pancreatitis in rat. Int J Pancreatol 1997;22: 193-200.
82. Hegyi P, Rakonczay Jr Z, Sari R, et al. Insulin is necessary for the hypertrophic effect of cholecystokinin-octapeptide following acute necrotizing experimental pancreatitis. World J Gastroenterol 2004;10:2275-2277.
83. Shen JQ, Shen J, Wang XP. Expression of insulin-like growth factor binding protein-4 (IGFBP-4) in acute pancreatitis induced by L-arginine in mice. Acta Histochem 2012;114:379-385.
84. Ishiwata T, Kudo M, Onda M, et al. Defined localization of nestinexpressing cells in L-arginine-induced acute pancreatitis. Pancreas 2006;32:360-368.
85. Paszt A, Eder K, Szabolcs A, et al. Effects of glucocorticoid agonist and antagonist on the pathogenesis of L-arginine-induced acute pancreatitis in rat. Pancreas 2008;36:369-376.
86. Zhang Z, Wang Y, Dong M, et al. Oxymatrine ameliorates L-arginine-induced acute pancreatitis in rats. Inflammation 2012;35: 605-613.
87. Menendez-Gutierrez MP, Roszer T, Ricote M. Biology and therapeutic applications of peroxisome proliferator-activated receptors. Curr Top Med Chem 2012;12:548-584.
88. Sidhu S, Pandhi P, Malhotra S, et al. Rosiglitazone promotes pancreatic regeneration in experimental model of acute pancreatitis. Fundam Clin Pharmacol 2011;25:237-247.
89. Neher MD, Weckbach S, Huber-Lang MS, et al. New insights into the role of peroxisome proliferator-activated receptors in regulating the inflammatory response after tissue injury. PPAR Res 2012; 2012:728461.
90. Dahlhoff M, Algul H, Siveke JT, et al. Betacellulin protects from pancreatitis by activating stress-activated protein kinase. Gastroenterology 2010;138:1585-1594, 1594.e1-3.
91. Sharif R, Dawra R, Wasiluk K, et al. Impact of toll-like receptor 4 on the severity of acute pancreatitis and pancreatitis-associated lung injury in mice. Gut 2009;58:813-819.
92. Besselink MGH, van Santvoort HC, Buskens E, et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet 2008;371:651-659.
93. Muftuoglu MAT, Isikgor S, Tosun S, et al. Effects of probiotics on the severity of experimental acute pancreatitis. Eur J Clin Nutr 2006;60: 464-468.
94. Rakonczay Jr Z, Takács T, Boros I, et al. Heat shock proteins and the pancreas. J Cell Physiol 2003;195:383-391.
95. Tashiro M, Schafer C, Yao H, et al. Arginine induced acute pancreatitis alters the actin cytoskeleton and increases heat shock protein expression in rat pancreatic acinar cells. Gut 2001;49:241-250.
96. Bhagat L, Singh VP, Dawra RK, et al. Sodium arsenite induces heat shock protein 70 expression and protects against secretagogueinduced trypsinogen and NF-kappaB activation. J Cell Physiol 2008;215:37-46.
97. Habtezion A, Kwan R, Akhtar E, et al. Panhematin provides a therapeutic benefit in experimental pancreatitis. Gut 2011;60:671-679.
98. Delaney CP, McGeeney KF, Dervan P, et al. Pancreatic atrophy: a new model using serial intra-peritoneal injections of L-arginine. Scand J Gastroenterol 1993;28:1086-1090.
99. Fredstrom SB, Jessurun J, Gallaher DD. Pancreatitis induced in rats by repetitive administration of L-arginine. Pancreas 2009;38:344-345.
100. González AM, Garcia T, Samper E, et al. Assessment of the protective effects of oral tocotrienols in arginine chronic-like pancreatitis. Am J Physiol Gastrointest Liver Physiol 2011;301:G846-G855.
101. Weaver C, Bishop AE, Polak JM. Pancreatic changes elicited by chronic administration of excess L-arginine. Exp Mol Pathol 1994;60:71-87.
102. Yamaguchi T, Kihara Y, Taguchi M, et al. Persistent destruction of the basement membrane of the pancreatic duct contributes to progressive acinar atrophy in rats with experimentally induced pancreatitis. Pancreas 2005;31:365-372.
103. Saka M, Tuzun A, Ates Y, et al. Acute pancreatitis possibly due to arginine use: a case report. Turk J Gastroenterol 2004;15:56-58.
104. Wang J, Ohmuraya M, Suyama K, et al. Relationship of straindependent susceptibility to experimentally induced acute pancreatitis with regulation of Prss1 and Spink3 expression. Lab Invest 2010;90:654-664.