Pancreas Recovery Following Cerulein-Induced Pancreatitis Is Impaired in Plasminogen-Deficient Mice

Gastroenterology

Volumn 131, Issue 3, 2006, Pages 885-899

  Lugea, Aurelia ^a   Nan, Li ^b   French, Samuel W ^b   Bezerra, Jorge A ^c   Gukovskaya, Anna S ^a   Pandol, Stephen J ^a  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b HARBOR UCLA MEDICAL CENTER   (United States)

^c UNIVERSITY OF CINCINNATI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERULETIDE; COLLAGEN; FIBRONECTIN; METALLOPROTEINASE; PLASMIN; PLASMINOGEN; SCLEROPROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TRYPSIN;

ACINAR CELL; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL INFILTRATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; INFLAMMATORY CELL; MOUSE; NONHUMAN; PANCREAS INJURY; PANCREAS NECROSIS; PANCREATITIS; PARENCHYMA; PRIORITY JOURNAL; PROTEIN FUNCTION; STELLATE CELL; TISSUE SECTION; UPREGULATION;

EID: 33748098707     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2006.06.023     Document Type: Article

References (70)

1. Etemad B., and Whitcomb D.C. Chronic pancreatitis: diagnosis, classification, and new genetic developments. Gastroenterology 120 (2001) 682-707
2. Bataller R., and Brenner D.A. Liver fibrosis. J Clin Invest 115 (2005) 209-218
3. Lieber C.S. Biochemical mechanisms of alcohol-induced hepatic injury. Alcohol Alcohol Suppl 1 (1991) 283-290
4. Lieber C.S. Ethanol metabolism, cirrhosis and alcoholism. Clin Chim Acta 257 (1997) 59-84
5. Neubauer K., Knittel T., Armbrust T., and Ramadori G. Accumulation and cellular localization of fibrinogen/fibrin during short-term and long-term rat liver injury. Gastroenterology 108 (1995) 1124-1135
6. Brenner D.A., Waterboer T., Choi S.K., Lindquist J.N., Stefanovic B., Burchardt E., Yamauchi M., Gillan A., and Rippe R.A. New aspects of hepatic fibrosis. J Hepatol 32 (2000) 32-38
7. Stetler-Stevenson W.G. Dynamics of matrix turnover during pathologic remodeling of the extracellular matrix. Am J Pathol 148 (1996) 1345-1350
8. Parks W.C. A confederacy of proteinases. J Clin Invest 110 (2002) 613-614
9. Nagase H., and Woessner Jr. J.F. Matrix metalloproteinases. J Biol Chem 274 (1999) 21491-21494
10. Collen D. The plasminogen (fibrinolytic) system. Thromb Haemost 82 (1999) 259-270
11. Plow E.F., and Hoover-Plow J. The functions of plasminogen in cardiovascular disease. Trends Cardiovasc Med 14 (2004) 180-186
12. Blasi F. Proteolysis, cell adhesion, chemotaxis, and invasiveness are regulated by the u-PA-u-PAR-PAI-1 system. Thromb Haemost 82 (1999) 298-304
13. Takeuchi T., Harris J.L., Huang W., Yan K.W., Coughlin S.R., and Craik C.S. Cellular localization of membrane-type serine protease 1 and identification of protease-activated receptor-2 and single-chain urokinase-type plasminogen activator as substrates. J Biol Chem 275 (2000) 26333-26342
14. Mondino A., and Blasi F. uPA and uPAR in fibrinolysis, immunity and pathology. Trends Immunol 25 (2004) 450-455
15. Blasi F., and Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 3 (2002) 932-943
16. Lijnen H.R. Pleiotropic functions of plasminogen activator inhibitor-1. J Thromb Haemost 3 (2005) 35-45
17. Binder B.R., Christ G., Gruber F., Grubic N., Hufnagl P., Krebs M., Mihaly J., and Prager G.W. Plasminogen activator inhibitor 1: physiological and pathophysiological roles. News Physiol Sci 17 (2002) 56-61
18. Ng V.L., Sabla G.E., Melin-Aldana H., Kelley-Loughnane N., Degen J.L., and Bezerra J.A. Plasminogen deficiency results in poor clearance of non-fibrin matrix and persistent activation of hepatic stellate cells after an acute injury. J Hepatol 35 (2001) 781-789
19. Pohl J.F., Melin-Aldana H., Sabla G., Degen J.L., and Bezerra J.A. Plasminogen deficiency leads to impaired lobular reorganization and matrix accumulation after chronic liver injury. Am J Pathol 159 (2001) 2179-2186
20. Swaisgood C.M., French E.L., Noga C., Simon R.H., and Ploplis V.A. The development of bleomycin-induced pulmonary fibrosis in mice deficient for components of the fibrinolytic system. Am J Pathol 157 (2000) 177-187
21. Rakic J.M., Lambert V., Munaut C., Bajou K., Peyrollier K., Alvarez-Gonzalez M.L., Carmeliet P., Foidart J.M., and Noel A. Mice without uPA, tPA, or plasminogen genes are resistant to experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 44 (2003) 1732-1739
22. Ploplis V.A., Carmeliet P., Vazirzadeh S., Van V.I., Moons L., Plow E.F., and Collen D. Effects of disruption of the plasminogen gene on thrombosis, growth, and health in mice. Circulation 92 (1995) 2585-2593
23. Romer J., Bugge T.H., Pyke C., Lund L.R., Flick M.J., Degen J.L., and Dano K. Impaired wound healing in mice with a disrupted plasminogen gene. Nat Med 2 (1996) 287-292
24. Hattori N., Degen J.L., Sisson T.H., Liu H., Moore B.B., Pandrangi R.G., Simon R.H., and Drew A.F. Bleomycin-induced pulmonary fibrosis in fibrinogen-null mice. J Clin Invest 106 (2000) 1341-1350
25. Yang J., Shultz R.W., Mars W.M., Wegner R.E., Li Y., Dai C., Nejak K., and Liu Y. Disruption of tissue-type plasminogen activator gene in mice reduces renal interstitial fibrosis in obstructive nephropathy. J Clin Invest 110 (2002) 1525-1538
26. Lijnen H.R. Extracellular proteolysis in the development and progression of atherosclerosis. Biochem Soc Trans 30 (2002) 163-167
27. Paciucci R., Vila M.R., Adell T., Diaz V.M., Tora M., Nakamura T., and Real F.X. Activation of the urokinase plasminogen activator/urokinase plasminogen activator receptor system and redistribution of E-cadherin are associated with hepatocyte growth factor-induced motility of pancreas tumor cells overexpressing Met. Am J Pathol 153 (1998) 201-212
28. Lugea A., Gukovsky I., Gukovskaya A.S., and Pandol S.J. Non-oxidative ethanol metabolites alter extracellular matrix protein content in rat pancreas. Gastroenterology 125 (2003) 1845-1859
29. Paciucci R., Tora M., Diaz V.M., and Real F.X. The plasminogen activator system in pancreas cancer: role of t-PA in the invasive potential in vitro. Oncogene 16 (1998) 625-633
30. Cantero D., Friess H., Deflorin J., Zimmermann A., Brundler M.A., Riesle E., Korc M., and Buchler M.W. Enhanced expression of urokinase plasminogen activator and its receptor in pancreatic carcinoma. Br J Cancer 75 (1997) 388-395
31. Han H., Bearss D.J., Browne L.W., Calaluce R., Nagle R.B., and Von Hoff D.D. Identification of differentially expressed genes in pancreatic cancer cells using cDNA microarray. Cancer Res 62 (2002) 2890-2896
32. Chen H.M., Sunamura M., Shibuya K., Yamauchi J.I., Sakai Y., Fukuyama S., Mikami Y., Takeda K., and Matsuno S. Early microcirculatory derangement in mild and severe pancreatitis models in mice. Surg Today 31 (2001) 634-642
33. Kruse P., Lasson A., and Hage E. Proteases and protease inhibitors in cerulein-induced acute pancreatitis in rats. J Surg Res 85 (1999) 294-300
34. Lasson A., and Ohlsson K. Disseminated intravascular coagulation and antiprotease activity in acute human pancreatitis. Scand J Gastroenterol Suppl 126 (1986) 35-39
35. Segal I., Chaloner C., Douglas J., John K.D., Zaidi A., Cotter L., Appelros S., Borgstrom A., and Braganza J.M. Acute pancreatitis in Soweto, South Africa: relationship between trypsinogen load, trypsinogen activation, and fibrinolysis. Am J Gastroenterol 97 (2002) 883-892
36. Ji B., Chen X.Q., Misek D.E., Kuick R., Hanash S., Ernst S., Najarian R., and Logsdon C.D. Pancreatic gene expression during the initiation of acute pancreatitis: identification of EGR-1 as a key regulator. Physiol Genomics 14 (2003) 59-72
37. Friess H., Duarte R., Kleeff J., Fukuda A., Tang W.H., Graber H., Schilling M., Zimmermann A., Korc M., and Buchler M.W. The plasminogen activator/plasmin system is up-regulated after acute necrotizing pancreatitis in human beings. Surgery 124 (1998) 79-86
38. Friess H., Cantero D., Graber H., Tang W.H., Guo X., Kashiwagi M., Zimmermann A., Gold L., Korc M., and Buchler M.W. Enhanced urokinase plasminogen activation in chronic pancreatitis suggests a role in its pathogenesis. Gastroenterology 113 (1997) 904-913
39. Bugge T.H., Flick M.J., Daugherty C.C., and Degen J.L. Plasminogen deficiency causes severe thrombosis but is compatible with development and reproduction. Genes Dev 9 (1995) 794-807
40. Vasseur S., Folch-Puy E., Hlouschek V., Garcia S., Fiedler F., Lerch M.M., Dagorn J.C., Closa D., and Iovanna J.L. 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
41. Vaquero E., Gukovsky I., Zaninovic V., Gukovskaya A.S., and Pandol S.J. Localized pancreatic NF-κB activation and inflammatory response in taurocholate-induced pancreatitis. Am J Physiol Gastrointest Liver Physiol 280 (2001) G1197-G1208
42. Folch E., Closa D., Prats N., Gelpi E., and Rosello-Catafau J. Leukotriene generation and neutrophil infiltration after experimental acute pancreatitis. Inflammation 22 (1998) 83-93
43. Labarca C., and Paigen K. A simple, rapid, and sensitive DNA assay procedure. Anal Biochem 102 (1980) 344-352
44. Goguen J.D., Bugge T., and Degen J.L. Role of the pleiotropic effects of plasminogen deficiency in infection experiments with plasminogen-deficient mice. Methods 21 (2000) 179-183
45. Bugge T.H., Kombrinck K.W., Flick M.J., Daugherty C.C., Danton M.J., and Degen J.L. Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell 87 (1996) 709-719
46. Lahteenmaki K., Kuusela P., and Korhonen T.K. Bacterial plasminogen activators and receptors. FEMS Microbiol Rev 25 (2001) 531-552
47. Zhou A., Huntington J.A., Pannu N.S., Carrell R.W., and Read R.J. How vitronectin binds PAI-1 to modulate fibrinolysis and cell migration. Nat Struct Biol 10 (2003) 541-544
48. Mareninova O.A., Sung K.F., Hong P., Lugea A., Pandol S.J., Gukovsky I., and Gukovskaya A.S. Cell death in pancreatitis: caspases protect from necrotizing pancreatitis. J Biol Chem 281 (2006) 3370-3381
49. Apte M.V., Haber P.S., Darby S.J., Rodgers S.C., McCaughan G.W., Korsten M.A., Pirola R.C., and Wilson J.S. Pancreatic stellate cells are activated by proinflammatory cytokines: implications for pancreatic fibrogenesis. Gut 44 (1999) 534-541
50. Schneider E., Schmid-Kotsas A., Zhao J., Weidenbach H., Schmid R.M., Menke A., Adler G., Waltenberger J., Grunert A., and Bachem M.G. Identification of mediators stimulating proliferation and matrix synthesis of rat pancreatic stellate cells. Am J Physiol Cell Physiol 281 (2001) C532-C543
51. Yokota T., Denham W., Murayama K., Pelham C., Joehl R., and Bell Jr. R.H. Pancreatic stellate cell activation and MMP production in experimental pancreatic fibrosis. J Surg Res 104 (2002) 106-111
52. Zimmermann A., Gloor B., Kappeler A., Uhl W., Friess H., and Buchler M.W. Pancreatic stellate cells contribute to regeneration early after acute necrotising pancreatitis in humans. Gut 51 (2002) 574-578
53. Liu Z., Li N., Diaz L.A., Shipley M., Senior R.M., and Werb Z. Synergy between a plasminogen cascade and MMP-9 in autoimmune disease. J Clin Invest 115 (2005) 879-887
54. Solberg H., Rinkenberger J., Dano K., Werb Z., and Lund L.R. A functional overlap of plasminogen and MMPs regulates vascularization during placental development. Development 130 (2003) 4439-4450
55. Benyon R.C., and Arthur M.J. Extracellular matrix degradation and the role of hepatic stellate cells. Semin Liver Dis 21 (2001) 373-384
56. Carmeliet P., Schoonjans L., Kieckens L., Ream B., Degen J., Bronson R., De Vos R., van den Oord J.J., Collen D., and Mulligan R.C. Physiological consequences of loss of plasminogen activator gene function in mice. Nature 368 (1994) 419-424
57. Kao W.W., Kao C.W., Kaufman A.H., Kombrinck K.W., Converse R.L., Good W.V., Bugge T.H., and Degen J.L. Healing of corneal epithelial defects in plasminogen- and fibrinogen-deficient mice. Invest Ophthalmol Vis Sci 39 (1998) 502-508
58. Nagai N., De Mol M., Lijnen H.R., Carmeliet P., and Collen D. Role of plasminogen system components in focal cerebral ischemic infarction: a gene targeting and gene transfer study in mice. Circulation 99 (1999) 2440-2444
59. Bezerra J.A., Bugge T.H., Melin-Aldana H., Sabla G., Kombrinck K.W., Witte D.P., and Degen J.L. Plasminogen deficiency leads to impaired remodeling after a toxic injury to the liver. Proc Natl Acad Sci U S A 96 (1999) 15143-15148
60. Bezerra J.A., Currier A.R., Melin-Aldana H., Sabla G., Bugge T.H., Kombrinck K.W., and Degen J.L. Plasminogen activators direct reorganization of the liver lobule after acute injury. Am J Pathol 158 (2001) 921-929
61. Ploplis V.A., French E.L., Carmeliet P., Collen D., and Plow E.F. Plasminogen deficiency differentially affects recruitment of inflammatory cell populations in mice. Blood 91 (1998) 2005-2009
62. Arthur M.J. Fibrosis and altered matrix degradation. Digestion 59 (1998) 376-380
63. Bentrem D.J., and Joehl R.J. Pancreas: healing response in critical illness. Crit Care Med 31 (2003) S582-S589
64. Hertig A., and Rondeau E. Plasminogen activator inhibitor type 1: the two faces of the same coin. Curr Opin Nephrol Hypertens 13 (2004) 39-44
65. Edgtton K.L., Gow R.M., Kelly D.J., Carmeliet P., and Kitching A.R. Plasmin is not protective in experimental renal interstitial fibrosis. Kidney Int 66 (2004) 68-76
66. Duffield J.S., Forbes S.J., Constandinou C.M., Clay S., Partolina M., Vuthoori S., Wu S., Lang R., and Iredale J.P. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest 115 (2005) 56-65
67. Gyetko M.R., Aizenberg D., and Mayo-Bond L. Urokinase-deficient and urokinase receptor-deficient mice have impaired neutrophil antimicrobial activation in vitro. J Leukoc Biol 76 (2004) 648-656
68. Syrovets T., Jendrach M., Rohwedder A., Schule A., and Simmet T. Plasmin-induced expression of cytokines and tissue factor in human monocytes involves AP-1 and IKKβ-mediated NF-κB activation. Blood 97 (2001) 3941-3950
69. Kaikita K., Fogo A.B., Ma L., Schoenhard J.A., Brown N.J., and Vaughan D.E. Plasminogen activator inhibitor-1 deficiency prevents hypertension and vascular fibrosis in response to long-term nitric oxide synthase inhibition. Circulation 104 (2001) 839-844
70. Issa R., Zhou X., Constandinou C.M., Fallowfield J., Millward-Sadler H., Gaca M.D., Sands E., Suliman I., Trim N., Knorr A., Arthur M.J., Benyon R.C., and Iredale J.P. Spontaneous recovery from micronodular cirrhosis: evidence for incomplete resolution associated with matrix cross-linking. Gastroenterology 126 (2004) 1795-1808