Pancreatic STAT3 protects mice against caerulein-induced pancreatitis via PAP1 induction

American Journal of Pathology

Volumn 181, Issue 6, 2012, Pages 2105-2113

  Shigekawa, Minoru ^a   Hikita, Hayato ^a   Kodama, Takahiro ^a   Shimizu, Satoshi ^a   Li, Wei ^a   Uemura, Akio ^a   Miyagi, Takuya ^a   Hosui, Atsushi ^a   Kanto, Tatsuya ^a   Hiramatsu, Naoki ^a   Tatsumi, Tomohide ^a   Takeda, Kiyoshi ^b   Akira, Shizuo ^c   Takehara, Tetsuo ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^c Laboratory of Host Defense   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE PHASE PROTEIN; AMYLASE; CERULETIDE; CRE RECOMBINASE; PANCREATITIS ASSOCIATED PROTEIN; PANCREATITIS ASSOCIATED PROTEIN 1; STAT3 PROTEIN; TRANSCRIPTION FACTOR PDX 1; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

ACINAR CELL; ACUTE PANCREATITIS; AMYLASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; HYDRODYNAMICS; MOUSE; NONHUMAN; PANCREAS INJURY; PANCREAS NECROSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; TRIACYLGLYCEROL LIPASE BLOOD LEVEL;

ANIMALS; ANTIGENS, NEOPLASM; CAERULEIN; FEMALE; GENE DELETION; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; LECTINS, C-TYPE; LIVER; MALE; MICE; MICE, KNOCKOUT; PANCREAS; PANCREATITIS; STAT3 TRANSCRIPTION FACTOR; TUMOR MARKERS, BIOLOGICAL;

EID: 84869192369     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.08.038     Document Type: Article

References (49)

1. M.G. Raraty, J.A. Murphy, E. Mcloughlin, D. Smith, D. Criddle, R. Sutton Mechanisms of acinar cell injury in acute pancreatitis Scand J Surg 94 2005 89 96
2. A.K. Saluja, E.A. Donovan, K. Yamanaka, Y. Yamaguchi, B. Hofbauer, M.L. Steer Cerulein-induced in vitro activation of trypsinogen in rat pancreatic acini is mediated by cathepsin B Gastroenterology 113 1997 304 310
3. J. Norman The role of cytokines in the pathogenesis of acute pancreatitis Am J Surg 175 1998 76 83
4. M. Bhatia, M. Brady, S. Shokuhi, S. Christmas, J.P. Neoptolemos, J. Slavin Inflammatory mediators in acute pancreatitis J Pathol 190 2000 117 125
5. M. Bhatia, F.L. Wong, Y. Cao, H.Y. Lau, J. Huang, P. Puneet, L. Chevali Pathophysiology of acute pancreatitis Pancreatology 5 2005 132 144
6. N. Pooran, A. Indaram, P. Singh, S. Bank Cytokines (IL-6. IL-8, TNF): early and reliable predictors of severe acute pancreatitis J Clin Gastroenterol 37 2003 263 266
7. J. Mayer, B. Rau, F. Gansauge, H.G. Beger Inflammatory mediators in human acute pancreatitis: clinical and pathophysiological implications Gut 47 2000 546 552
8. T.L. Dugernier, P.F. Laterre, X. Wittebole, J. Roeseler, D. Latinne, M.S. Reynaert, J. Pugin Compartmentalization of the inflammatory response during acute pancreatitis: correlation with local and systemic complications Am J Respir Crit Care Med 168 2003 148 157
9. J.J. O'Shea, M. Gadina, R.D. Schreiber Cytokine signaling in 2002: new surprises in the Jak/Stat pathway Cell 109 Suppl 2002 S121 S131
10. S. Akira, Y. Nishio, M. Inoue, X.J. Wang, S. Wei, T. Matsusaka, K. Yoshida, T. Sudo, M. Naruto, T. Kishimoto Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p91-related transcription factor involved in the gp130-mediated signaling pathway Cell 77 1994 63 71
11. Z. Zhong, Z. Wen, J.E. Darnell Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6 Science 264 1994 95 98
12. L.A. Kobierski, S. Srivastava, D. Borsook Systemic lipopolysaccharide and interleukin-1beta activate the interleukin 6: sTAT intracellular signaling pathway in neurons of mouse trigeminal ganglion Neurosci Lett 281 2000 61 64
13. M. Obana, M. Maeda, K. Takeda, A. Hayama, T. Mohri, T. Yamashita, Y. Nakaoka, I. Komuro, G. Matsumiya, J. Azuma, Y. Fujio Therapeutic activation of signal transducer and activator of transcription 3 by interleukin-11 ameliorates cardiac fibrosis after myocardial infarction Circulation 121 2010 684 691
14. W. Li, X. Liang, C. Kellendonk, V. Poli, R. Taub STAT3 contributes to the mitogenic response of hepatocytes during liver regeneration J Biol Chem 277 2002 28411 28417
15. R. Sakamori, T. Takehara, C. Ohnishi, T. Tatsumi, K. Ohkawa, K. Takeda, S. Akira, N. Hayashi Signal transducer and activator of transcription 3 signaling within hepatocytes attenuates systemic inflammatory response and lethality in septic mice Hepatology 46 2007 1564 1573
16. K. Robinson, L. Vona-Davis, D. Riggs, B. Jackson, D. McFadden Peptide YY attenuates STAT1 and STAT3 activation induced by TNF-alpha in acinar cell line AR42J J Am Coll Surg 202 2006 788 796
17. L.C. Vona-Davis, K.A. Frankenberry, U. Waheed, E. Peterson, D.W. McFadden Expression of STAT3 and SOCS3 in pancreatic acinar cells J Surg Res 127 2005 14 120
18. S. Yubero, L. Ramudo, M.A. Manso, I. De Dios The role of redox status on chemokine expression in acute pancreatitis Biochim Biophys Acta 1792 2009 148 154
19. K. Takeda, K. Noguchi, W. Shi, T. Tanaka, M. Matsumoto, N. Yoshida, T. Kishimoto, S. Akira Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality Proc Natl Acad Sci U S A 94 1997 3801 3804
20. K. Takeda, T. Kaisho, N. Yoshida, J. Takeda, T. Kishimoto, S. Akira Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: generation and characterization of T cell-specific Stat3-deficient mice J Immunol 161 1998 4652 4660
21. M. Shigekawa, T. Takehara, T. Kodama, H. Hikita, S. Shimizu, W. Li, T. Miyagi, A. Hosui, T. Tatsumi, H. Ishida, T. Kanto, N. Hiramatsu, N. Hayashi Involvement of STAT3-regulated hepatic soluble factors in attenuation of stellate cell activity and liver fibrogenesis in mice Biochem Biophys Res Commun 406 2011 614 620
22. A. Uemura, T. Takehara, T. Miyagi, T. Suzuki, T. Tatsumi, K. Ohkawa, T. Kanto, N. Hiramatsu, N. Hayashi Natural killer cell is a major producer of interferon gamma that is critical for the IL-12-induced anti-tumor effect in mice Cancer Immunol Immunother 59 2010 453 463
23. C. Chen, R. Fang, C. Davis, C. Maravelias, E. Sibley Pdx1 inactivation restricted to the intestinal epithelium in mice alters duodenal gene expression in enterocytes and enteroendocrine cells Am J Physiol Gastrointest Liver Physiol 297 2009 G1126 G1137
24. J.N. Jensen, E. Cameron, M.V. Garay, T.W. Starkey, R. Gianani, J. Jensen Recapitulation of elements of embryonic development in adult mouse pancreatic regeneration Gastroenterology 128 2005 728 741
25. V. Keim, G. Rohr, H.G. Stöckert, F.J. Haberich An additional secretory protein in the rat pancreas Digestion 29 1984 242 249
26. J.L. Iovanna, V. Keim, I. Nordback, G. Montalto, J. Camarena, C. Letoublon, P. Lévy, P. Berthézène, J.C. Dagorn Multicentric Study Group on Acute Pancreatitis Serum levels of pancreatitis-associated protein as indicators of the course of acute pancreatitis Gastroenterology 106 1994 728 734
27. E. Folch-Puy, S. Granell, J.C. Dagorn, J.L. Iovanna, D. Closa Pancreatitis-associated protein I suppresses NF-kappa B activation through a JAK/STAT-mediated mechanism in epithelial cells J Immunol 176 2006 3774 3779
28. N.J. Dusetti, E.M. Ortiz, G.V. Mallo, J.C. Dagorn, J.L. Iovanna Pancreatitis-associated protein I (PAP I), an acute phase protein induced by cytokines Identification of two functional interleukin-6 response elements in the rat PAP I promoter region J Biol Chem 270 1995 22417 22421
29. T. Miyatsuka, H. Kaneto, T. Shiraiwa, T.A. Matsuoka, K. Yamamoto, K. Kato, Y. Nakamura, S. Akira, K. Takeda, Y. Kajimoto, Y. Yamasaki, E.P. Sandgren, Y. Kawaguchi, C.V. Wright, Y. Fujitani Persistent expression of PDX-1 in the pancreas causes acinar-to-ductal metaplasia through Stat3 activation Genes Dev 20 2006 1435 1440
30. A. Scholz, S. Heinze, K.M. Detjen, M. Peters, M. Welzel, P. Hauff, M. Schirner, B. Wiedenmann, S. Rosewicz Activated signal transducer and activator of transcription 3 (STAT3) supports the malignant phenotype of human pancreatic cancer Gastroenterology 125 2003 891 905
31. F.R. Greten, C.K. Weber, T.F. Greten, G. Schneider, M. Wagner, G. Adler, R.M. Schmid Stat3 and NF-kappaB activation prevents apoptosis in pancreatic carcinogenesis Gastroenterology 123 2002 2052 2063
32. B.B. Aggarwal, A.B. Kunnumakkara, K.B. Harikumar, S.R. Gupta, S.T. Tharakan, C. Koca, S. Dey, B. Sung Signal transducer and activator of transcription-3, inflammation, and cancer: how intimate is the relationship Ann N Y Acad Sci 1171 2009 59 76
33. N. Moniaux, H. Song, M. Darnaud, K. Garbin, M. Gigou, C. Mitchell, D. Samuel, L. Jamot, P. Amouyal, G. Amouyal, C. Bréchot, J. Faivre Human hepatocarcinoma-intestine-pancreas/pancreatitis-associated protein cures fas-induced acute liver failure in mice by attenuating free-radical damage in injured livers Hepatology 53 2011 618 627
34. M. Gironella, J.L. Iovanna, M. Sans, F. Gil, M. Peñalva, D. Closa, R. Miquel, J.M. Piqué, J. Panés Anti-inflammatory effects of pancreatitis associated protein in inflammatory bowel disease Gut 54 2005 1244 1253
35. V. Moucadel, P. Soubeyran, S. Vasseur, N.J. Dusetti, J.C. Dagorn, J.L. Iovanna Cdx1 promotes cellular growth of epithelial intestinal cells through induction of the secretory protein PAP I Eur J Cell Biol 80 2001 156 163
36. M.T. Simon, A. Pauloin, G. Normand, H.T. Lieu, H. Mouly, G. Pivert, F. Carnot, J.G. Tralhao, C. Brechot, L. Christa HIP/PAP stimulates liver regeneration after partial hepatectomy and combines mitogenic and anti-apoptotic functions through the PKA signaling pathway FASEB J 17 2003 1441 1450
37. B.K. Dieckgraefe, W.F. Stenson, J.R. Korzenik, P.E. Swanson, C.A. Harrington Analysis of mucosal gene expression in inflammatory bowel disease by parallel oligonucleotide arrays Physiol Genomics 4 2000 1 11
38. S. Averill, D.R. Davis, P.J. Shortland, J.V. Priestley, S.P. Hunt Dynamic pattern of reg-2 expression in rat sensory neurons after peripheral nerve injury J Neurosci 22 2002 7493 7501
39. B. Orelle, V. Keim, L. Masciotra, J.C. Dagorn, J.L. Iovanna Human pancreatitis-associated protein Messenger RNA cloning and expression in pancreatic diseases J Clin Invest 90 1992 2284 2291
40. A.T. McKie, R.J. Simpson, S. Ghosh, T.J. Peters, F. Farzaneh Regulation of pancreatitis-associated protein (HIP/PAP) mRNA levels in mouse pancreas and small intestine Clin Sci (Lond) 91 1996 213 218
41. M.I. Vaccaro, E.L. Calvo, A.M. Suburo, D.O. Sordelli, G. Lanosa, J.L. Iovanna Lipopolysaccharide directly affects pancreatic acinar cells: implications on acute pancreatitis pathophysiology Dig Dis Sci 45 2000 915 926
42. J.W. van der Pijl, J.G. Boonstra, S. Barthellemy, Y.F. Smets, J. Hermans, J.A. Bruijn, J.W. de Fijter, M.R. Daha, J.C. Dagorn Pancreatitis-associated protein: a putative marker for pancreas graft rejection Transplantation 63 1997 995 1003
43. S. Vasseur, E. Folch-Puy, V. Hlouschek, S. Garcia, F. Fiedler, M.M. Lerch, J.C. Dagorn, D. Closa, J.L. Iovanna p8 improves pancreatic response to acute pancreatitis by enhancing the expression of the anti-inflammatory protein pancreatitis-associated protein I J Biol Chem 279 2004 7199 7207
44. M. Gironella, E. Folch-Puy, A. LeGoffic, S. Garcia, L. Christa, A. Smith, L. Tebar, S.P. Hunt, R. Bayne, A.J. Smith, J.C. Dagorn, D. Closa, J.L. Iovanna Experimental acute pancreatitis in PAP/HIP knock-out mice Gut 56 2007 1091 1097
45. H. Algül, M. Treiber, M. Lesina, H. Nakhai, D. Saur, F. Geisler, A. Pfeifer, S. Paxian, R.M. Schmid Pancreas-specific RelA/p65 truncation increases susceptibility of acini to inflammation-associated cell death following cerulein pancreatitis J Clin Invest 117 2007 1490 1501
46. E.M. Ortiz, N.J. Dusetti, S. Vasseur, D. Malka, H. Bödeker, J.C. Dagorn, J.L. Iovanna The pancreatitis-associated protein is induced by free radicals in AR4-2J cells and confers cell resistance to apoptosis Gastroenterology 114 1998 808 816
47. D. Malka, S. Vasseur, H. Bödeker, E.M. Ortiz, N.J. Dusetti, P. Verrando, J.C. Dagorn, J.L. Iovanna Tumor necrosis factor alpha triggers antiapoptotic mechanisms in rat pancreatic cells through pancreatitis-associated protein I activation Gastroenterology 119 2000 816 828
48. H. Yu, D. Pardoll, R. Jove STATs in cancer inflammation and immunity: a leading role for STAT3 Nat Rev Cancer 9 2009 798 809
49. P.K. Epling-Burnette, J.H. Liu, R. Catlett-Falcone, J. Turkson, M. Oshiro, R. Kothapalli, Y. Li, J.M. Wang, H.F. Yang-Yen, J. Karras, R. Jove, T.P. Loughran Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression J Clin Invest 107 2001 351 362