Rho-kinase signaling regulates trypsinogen activation and tissue damage in severe acute pancreatitis

British Journal of Pharmacology

Volumn 162, Issue 3, 2011, Pages 648-658

  Awla, D ^a   Hartman, H ^a   Abdulla, A ^a   Zhang, S ^a   Rahman, M ^a   Regner S ^a   Thorlacius, H ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

amylase; chemokines; inflammation; leucocytes; macrophage inflammatory protein 2; pancreas; trypsinogen

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; AMYLASE; MACROPHAGE INFLAMMATORY PROTEIN 2; MYELOPEROXIDASE; RHO KINASE; TAUROCHOLIC ACID; TRYPSINOGEN; TRYPSINOGEN ACTIVATION PEPTIDE; AMIDE; CHOLAGOGUE; CXCL2 CHEMOKINE; ENZYME INHIBITOR; PEROXIDASE; PYRIDINE DERIVATIVE;

ACINAR CELL; ACUTE PANCREATITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL DEATH; CONTROLLED STUDY; DOSE RESPONSE; EDEMA; ENZYME ACTIVATION; ENZYME INHIBITION; IN VITRO STUDY; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PANCREAS INJURY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SEVERE ACUTE PANCREATITIS; SIGNAL TRANSDUCTION; ANIMAL; BLOOD; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; DRUG ANTAGONISM; ENZYMOLOGY; FLOW CYTOMETRY; METABOLISM; NECROSIS; PANCREAS; PANCREATITIS; PATHOLOGY;

AMIDES; AMYLASES; ANIMALS; CHEMOKINE CXCL2; CHOLAGOGUES AND CHOLERETICS; ENZYME INHIBITORS; FLOW CYTOMETRY; MALE; MICE; MICE, INBRED C57BL; NECROSIS; NEUTROPHIL INFILTRATION; PANCREAS; PANCREATITIS; PEROXIDASE; PYRIDINES; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; TAUROCHOLIC ACID; TRYPSINOGEN;

EID: 78651467246     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.01060.x     Document Type: Article

References (55)

1. Alblas J, Ulfman L, Hordijk P, Koenderman L, (2001). Activation of Rhoa and ROCK are essential for detachment of migrating leucocytes. Mol Biol Cell 12: 2137-2145.
2. Andersson R, Andersson B, Andersson E, Axelsson J, Eckerwall G, Tingstedt B, (2007). Acute pancreatitis-from cellular signalling to complicated clinical course. HPB (Oxford) 9: 414-420.
3. Asaduzzaman M, Zhang S, Lavasani S, Wang Y, Thorlacius H, (2008). LFA-1 and MAC-1 mediate pulmonary recruitment of neutrophils and tissue damage in abdominal sepsis. Shock 30: 254-259.
4. Bacon KB, Oppenheim JJ, (1998). Chemokines in disease models and pathogenesis. Cytokine Growth Factor Rev 9: 167-173.
5. Bao W, Hu E, Tao L, Boyce R, Mirabile R, Thudium DT, et al. (2004). Inhibition of Rho-kinase protects the heart against ischemia/reperfusion injury. Cardiovasc Res 61: 548-558.
6. Bhatia M, Brady M, Shokuhi S, Christmas S, Neoptolemos JP, Slavin J, (2000). Inflammatory mediators in acute pancreatitis. J Pathol 190: 117-125.
7. Bokoch GM, (2005). Regulation of innate immunity by Rho GTPases. Trends Cell Biol 15: 163-171.
8. Bourgier C, Haydont V, Milliat F, Francois A, Holler V, Lasser P, et al. (2005). Inhibition of Rho kinase modulates radiation induced fibrogenic phenotype in intestinal smooth muscle cells through alteration of the cytoskeleton and connective tissue growth factor expression. Gut 54: 336-343.
9. Cacalano G, Lee J, Kikly K, Ryan AM, Pitts-Meek S, Hultgren B, et al. (1994). Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265: 682-684.
10. Carlos TM, Harlan JM, (1994). Leucocyte-endothelial adhesion molecules. Blood 84: 2068-2101.
11. Chen P, Zhang Y, Qiao M, Yuan Y, (2007). Activated protein C, an anticoagulant polypeptide, ameliorates severe acute pancreatitis via regulation of mitogen-activated protein kinases. J Gastroenterol 42: 887-896.
12. Feng L, Xia Y, Yoshimura T, Wilson CB, (1995). Modulation of neutrophil influx in glomerulonephritis in the rat with anti-macrophage inflammatory protein-2 (MIP-2) antibody. J Clin Invest 95: 1009-1017.
13. Glasbrenner B, Adler G, (1993). Pathophysiology of acute pancreatitis. Hepatogastroenterology 40: 517-521.
14. Granger J, Remick D, (2005). Acute pancreatitis: models, markers, and mediators. Shock 24 (Suppl. 1): 45-51.
15. Gudgeon AM, Heath DI, Hurley P, Jehanli A, Patel G, Wilson C, et al. (1990). Trypsinogen activation peptides assay in the early prediction of severity of acute pancreatitis. Lancet 335: 4-8.
16. Hartwig W, Werner J, Jimenez RE, Z'Graggen K, Weimann J, Lewandrowski KB, et al. (1999). Trypsin and activation of circulating trypsinogen contribute to pancreatitis-associated lung injury. Am J Physiol 277: G1008-G1016.
17. Itoh K, Yoshioka K, Akedo H, Uehata M, Ishizaki T, Narumiya S, (1999). An essential part for Rho-associated kinase in the transcellular invasion of tumor cells. Nat Med 5: 221-225.
18. Jones SA, Dewald B, Clark-Lewis I, Baggiolini M, (1997). Chemokine antagonists that discriminate between interleukin-8 receptors. Selective blockers of CXCR2. J Biol Chem 272: 16166-16169.
19. Kawabata S, Miura T, Morita T, Kato H, Fujikawa K, Iwanaga S, et al. (1988). Hghly sensitive peptide-4-methylcoumaryl-7-amide substrates for blood-clotting proteases and trypsin. Eur J Biochem 172: 17-25.
20. Kelly M, Hwang JM, Kubes P, (2007). Modulating leukocyte recruitment in inflammation. J Allergy Clin Immunol 120: 3-10.
21. Kitamura K, Tada S, Nakamoto N, Toda K, Horikawa H, Kurita S, et al. (2007). Rho/Rho kinase is a key enzyme system involved in the angiotensin II signaling pathway of liver fibrosis and steatosis. J Gastroenterol Hepatol 22: 2022-2033.
22. Klein M, Paul R, Angele B, Popp B, Pfister HW, Koedel U, (2006). Protein expression pattern in experimental pneumococcal meningitis. Microbes Infect 8: 974-983.
23. Kusama K, Nozu F, Awai T, Tanaka S, Honma I, Tsunoda Y, et al. (2003). Deactivation of ROCK-II by Y-27632 enhances basolateral pancreatic enzyme secretion and acute pancreatitis induced by CCK analogues. Biochem Biophys Res Commun 305: 339-344.
24. Kyriakides C, Jasleen J, Wang Y, Moore FD, Ashley SW Jr, Hechtman HB, (2001). Neutrophils, not complement, mediate the mortality of experimental hemorrhagic pancreatitis. Pancreas 22: 40-46.
25. Laschke MW, Menger MD, Wang Y, Lindell G, Jeppsson B, Thorlacius H, (2007). Sepsis-associated cholestasis is critically dependent on P-selectin-dependent leukocyte recruitment in mice. Am J Physiol Gastrointest Liver Physiol 292: G1396-G1402.
26. Laschke MW, Dold S, Jeppsson B, Schilling MK, Menger MD, Thorlacius H, (2008). Rho-Kinase Inhibitor Attenuates Cholestasis-Induced CXC Chemokine Formation, Leukocyte Recruitment, and Hepatocellular Damage in the Liver. J Surg Res 159: 666-673.
27. Laschke MW, Dold S, Menger MD, Jeppsson B, Thorlacius H, (2009). The Rho-kinase inhibitor Y-27632 inhibits cholestasis-induced platelet interactions in the hepatic microcirculation. Microvasc Res 78: 95-99.
28. Lee S, Bowrin K, Hamad AR, Chakravarti S, (2009). Extracellular matrix lumican deposited on the surface of neutrophils promotes migration by binding to beta2 integrin. J Biol Chem 284: 23662-23669.
29. Li X, Klintman D, Liu Q, Sato T, Jeppsson B, Thorlacius H, (2004). Critical role of CXC chemokines in endotoxemic liver injury in mice. J Leukoc Biol 75: 443-452.
30. Lindkvist B, Wierup N, Sundler F, Borgstrom A, (2008). Long-term nicotine exposure causes increased concentrations of trypsinogens and amylase in pancreatic extracts in the rat. Pancreas 37: 288-294.
31. Mangalmurti NS, Xiong Z, Hulver M, Ranganathan M, Liu XH, Oriss T, et al. (2009). Loss of red cell chemokine scavenging promotes transfusion-related lung inflammation. Blood 113: 1158-1166.
32. Mithöfer K, Fernández-del Castillo C, Rattner D, Warshaw AL, (1998). Subcellular kinetics of early trypsinogen activation in acute rodent pancreatitis. Am J Physiol 274: G71-G79.
33. Monson KM, Dowlatshahi S, Crockett ET, (2007). CXC-chemokine regulation and neutrophil trafficking in hepatic ischemia-reperfusion injury in P-selectin/ICAM-1 deficient mice. J Inflamm (Lond) 4: 11.
34. Oka M, Fagan KA, Jones PL, McMurtry IF, (2008). Therapeutic potential of RhoA/Rho kinase inhibitors in pulmonary hypertension. Br J Pharmacol 155: 444-454.
35. Pastor CM, Rubbia-Brandt L, Hadengue A, Jordan M, Morel P, Frossard JL, (2003). Role of macrophage inflammatory peptide-2 in cerulein-induced acute pancreatitis and pancreatitis-associated lung injury. Lab Invest 83: 471-478.
36. Quaid GA, Cave C, Robinson C, Williams MA, Solomkin JS, (1999). Preferential loss of CXCR-2 receptor expression and function in patients who have undergone trauma. Arch Surg 134: 1367-1371.
37. Rahman M, Zhang S, Chew M, Ersson A, Jeppsson B, Thorlacius H, (2009). Platelet-derived CD40L (CD154) mediates neutrophil upregulation of Mac-1 and recruitment in septic lung injury. Ann Surg 250: 783-790.
38. Regner S, Manjer J, Appelros S, Hjalmarsson C, Sadic J, Borgstrom A, (2008). Protease activation, pancreatic leakage, and inflammation in acute pancreatitis: differences between mild and severe cases and changes over the first three days. Pancreatology 8: 600-607.
39. Riento K, Ridley AJ, (2003). Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 4: 446-456.
40. Rios-Santos F, Alves-Filho JC, Souto FO, Spiller F, Freitas A, Lotufo CM, et al. (2007). Down-regulation of CXCR2 on neutrophils in severe sepsis is mediated by inducible nitric oxide synthase-derived nitric oxide. Am J Respir Crit Care Med 175: 490-497.
41. Ryschich E, Kerkadze V, Deduchovas O, Salnikova O, Parseliunas A, Marten A, et al. (2009). Intracapillary leucocyte accumulation as a novel antihaemorrhagic mechanism in acute pancreatitis in mice. Gut 58: 1508-1516.
42. Saluja AK, Bhagat L, Lee HS, Bhatia M, Frossard JL, Steer ML, (1999). Secretagogue-induced digestive enzyme activation and cell injury in rat pancreatic acini. Am J Physiol 276: G835-G842.
43. Santen S, Wang Y, Laschke MW, Menger MD, Jeppsson B, Thorlacius H, (2010). Rho-kinase signalling regulates CXC chemokine formation and leukocyte recruitment in colonic ischemia-reperfusion. Int J Colorectal Dis 25: 1063-1070.
44. Satoh S, Utsunomiya T, Tsurui K, Kobayashi T, Ikegaki I, Sasaki Y, et al. (2001). Pharmacological profile of hydroxy fasudil as a selective Rho kinase inhibitor on ischemic brain damage. Life Sci 69: 1441-1453.
45. Schmidt J, Rattner DW, Lewandrowski K, Compton CC, Mandavilli U, Knoefel WT, et al. (1992). A better model of acute pancreatitis for evaluating therapy. Ann Surg 215: 44-56.
46. Sharif R, Dawra R, Wasiluk K, Phillips P, Dudeja V, Kurt-Jones E, et al. (2009). Impact of toll-like receptor 4 on the severity of acute pancreatitis and pancreatitis-associated lung injury in mice. Gut 58: 813-819.
47. Shin HK, Salomone S, Potts EM, Lee SW, Millican E, Noma K, et al. (2007). Rho-kinase inhibition acutely augments blood flow in focal cerebral ischemia via endothelial mechanisms. J Cereb Blood Flow Metab 27: 998-1009.
48. Shiotani S, Shimada M, Suehiro T, Soejima Y, Yosizumi T, Shimokawa H, et al. (2004). Involvement of Rho-kinase in cold ischemia-reperfusion injury after liver transplantation in rats. Transplantation 78: 375-382.
49. Slotta JE, Braun OO, Menger MD, Thorlacius H, (2006). Fasudil, a Rho-kinase inhibitor, inhibits leucocyte adhesion in inflamed large blood vessels in vivo. Inflamm Res 55: 364-367.
50. Slotta JE, Laschke MW, Menger MD, Thorlacius H, (2008). Rho-kinase signalling mediates endotoxin hypersensitivity after partial hepatectomy. Br J Surg 95: 976-984.
51. Tasaka S, Koh H, Yamada W, Shimizu M, Ogawa Y, Hasegawa N, et al. (2005). Attenuation of endotoxin-induced acute lung injury by the Rho-associated kinase inhibitor, Y-27632. Am J Respir Cell Mol Biol 32: 504-510.
52. Tekamp-Olson P, Gallegos C, Bauer D, McClain J, Sherry B, Fabre M, et al. (1990). Cloning and characterization of cDNAs for murine macrophage inflammatory protein 2 and its human homologues. J Exp Med 172: 911-919.
53. Thorlacius K, Slotta JE, Laschke MW, Wang Y, Menger MD, Jeppsson B, et al. (2006). Protective effect of fasudil, a Rho-kinase inhibitor, on chemokine expression, leukocyte recruitment, and hepatocellular apoptosis in septic liver injury. J Leukoc Biol 79: 923-931.
54. Wang GJ, Gao CF, Wei D, Wang C, Ding SQ, (2009). Acute pancreatitis: etiology and common pathogenesis. World J Gastroenterol 15: 1427-1430.
55. Zhang XP, Li ZJ, Zhang J, (2009). Inflammatory mediators and microcirculatory disturbance in acute pancreatitis. Hepatobiliary Pancreat Dis Int 8: 351-357.