Heme oxygenase-1 suppresses the infiltration of neutrophils in rat liver during sepsis through inactivation of p38 MAPK

Shock

Volumn 34, Issue 6, 2010, Pages 615-621

  Lin, Yi Tseng ^a   Chen, Yen Hsu ^a,b,c   Yang, Yi Hsin ^d   Jao, Hsiao Ching ^a   Abiko, Yoshimitsu ^e   Yokoyama, Kazushige ^a,f   Hsu, Chin ^f  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b Division of Infectious Diseases   (Australia)

^c Tropical Medicine Research Center   (Iran)

^d KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e NIHON UNIVERSITY   (Japan)

^f KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

hepatic failure; HO 1; infection; MAP kinase; neutrophil migration

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANISOMYCIN; DIMER; FORMYLMETHIONYLLEUCYLPHENYLALANINE; HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTOPORPHYRIN COBALT; PROTOPORPHYRIN ZINC;

ACTIN POLYMERIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; CELL MIGRATION; CELL POLARITY; EX VIVO STUDY; IN VIVO STUDY; LIVER; MALE; MOLECULAR MECHANICS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SEPSIS; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANIMALS; ANISOMYCIN; BLOTTING, WESTERN; CELL MOVEMENT; ENZYME ACTIVATION; HEME OXYGENASE-1; LIVER; MALE; NEUTROPHIL INFILTRATION; NEUTROPHILS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROTOPORPHYRINS; RATS; RATS, SPRAGUE-DAWLEY; SEPSIS;

EID: 78649555758     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e3181e46ee0     Document Type: Article

References (35)

1. Moss M, Martin GS: A global perspective on the epidemiology of sepsis. Intensive Care Med 30:527-529, 2004.
2. Derikx JP, Poeze M, van Bijnen AA, Buurman WA, Heineman E: Evidence for intestinal and liver epithelial cell injury in the early phase of sepsis. Shock 28:544-548, 2007.
3. Hoesel LM, Neff TA, Neff SB, Younger JG, Olle EW, Gao H, Pianko MJ, Bernacki KD, Sarma JV, Ward PA: Harmful and protective roles of neutrophils in sepsis. Shock 24:40-47, 2005.
4. Jaeschke H, Hasegawa T: Role of neutrophils in acute inflammatory liver injury. Liver Int 26:912-919, 2006. (Pubitemid 44323408)
5. Jaeschke H: Mechanisms of liver injury. II. Mechanisms of neutrophil-induced liver cell injury during hepatic ischemia-reperfusion and other acute inflammatory conditions. Am J Physiol 290:G1083-G1088, 2006.
6. Fredenburgh LE, Perrella MA, Mitsialis SA: The role of heme oxygenase-1 in pulmonary disease. Am J Respir Cell Mol Biol 36:158-165, 2007.
7. Chung SW, Liu X, Macias AA, Baron RM, Perrella MA: Heme oxygenase-1Yderived carbon monoxide enhances the host defense response to microbial sepsis in mice. J Clin Invest 118:239-247, 2008.
8. Wiesel P, Patel AP, DiFonzo N, Marria PB, Sim CU, Pellacani A, Maemura K, LeBlanc BW, Marino K, Doerschuk CM, et al.: Endotoxin-induced mortality is related to increased oxidative stress and end-organ dysfunction, not refractory hypotension, in heme oxygenase-1Ydeficient mice. Circulation 102: 3015-3022, 2000.
9. Jao HC, Lin YT, Tsai LY, Wang CC, Liu HW, Hsu C: Early expression of heme oxygenase-1 in leukocytes correlates negatively with oxidative stress and predicts hepatic and renal dysfunction at late stage of sepsis. Shock 23:464-469, 2005.
10. Cicchetti G, Allen PG, Glogauer M: Chemotactic signaling pathways in neu-trophils: from receptor to actin assembly. Crit Rev Oral Biol Med 13:220-228, 2002.
11. Freitas A, Alves-Filho JC, Secco DD, Neto AF, Ferreira SH, Barja-Fidalgo C, Cunha FQ: Heme oxygenase/carbon monoxide-biliverdin pathway down regulates neutrophil rolling, adhesion and migration in acute inflammation. Br J Pharmacol 149:345-354, 2006.
12. Ryter SW, Alam J, Choi AM: Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583-650, 2006.
13. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM: Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6:422-428, 2000.
14. Ryter SW, Morse D, Choi AM: Carbon monoxide and bilirubin: potential therapies for pulmonary/vascular injury and disease. Am J Respir Cell Mol Biol 36:175-182, 2007.
15. Zabalgoitia M, Colston JT, Reddy SV, Holt JW, Regan RF, Stec DE, Rimoldi JM, Valente AJ, Chandrasekar B: Carbon monoxide donors or heme oxygenase-1 (HO-1) overexpression blocks interleukin-18Ymediated NF-kappaB-PTENYdependent human cardiac endothelial cell death. Free Radic Biol Med 44:284-298, 2008.
16. Wang Q, Yerukhimovich M, Gaarde WA, Popoff IJ, Doerschuk CM: MKK3 and-6Ydependent activation of p38alpha MAP kinase is required for cytoske-letal changes in pulmonary microvascular endothelial cells induced by ICAM-1 ligation. Am J Physiol Lung Cell Mol Physiol 288:L359-L369, 2005.
17. Coxon PY, Rane MJ, Uriarte S, Powell DW, Singh S, Butt W, Chen Q, McLeish KR: MAPK-activated protein kinase-2 participates in p38 MAPKYdependent and ERK-dependent functions in human neutrophils. Cell Signal 15:993-1001, 2003.
18. Wichterman KA, Baue AE, Chaudry IH: Sepsis and septic shockVa review of laboratory models and a proposal. J Surg Res 29:189-201, 1980.
19. Chen YH, Hong IC, Kuo KK, Hsu HK, Hsu C: Role of retinoid-X receptor-alpha in the suppression of rat bile acid coenzyme A-amino acid N-acyltransferase in liver during sepsis. Shock 28:65-70, 2007.
20. Chen BC, Kuo KK, Chen KY, Liu CH, Tsai LY, Hsu HK, Hsu C: Retinoid X receptor alpha participation in dexamethasone-induced rat bile acid coenzyme A-amino acid N-acyltransferase expression in septic liver. Shock 32:164-171, 2009.
21. Froh M, Conzelmann L, Walbrun P, Netter S, Wiest R, Wheeler MD, Lehnert M, Uesugi T, Scholmerich J, Thurman RG: Heme oxygenase-1 overexpression increases liver injury after bile duct ligation in rats. World J Gastroenterol 13:3478-3486, 2007.
22. Iwasashi H, Suzuki M, Unno M, Utiyama T, Oikawa M, Kondo N, Matsuno S: Inhibition of heme oxygenase ameliorates sepsis-induced liver dysfunction in rats. Surg Today 33:30-38, 2003.
23. Wang F, Duan ZJ, Sun YJ: Influence of heme oxygenase-1 expression on immune liver fibrosis induced by cobalt protoporphyrin in rats. World J Gastro-enterol 15:3009-3014, 2009.
24. Ryu H, Lee JH, Kim KS, Jeong SM, Kim PH, Chung HT: Regulation of neu-trophil adhesion by pituitary growth hormone accompanies tyrosine phos-phorylation of Jak2, p125FAK, and paxillin. J Immunol 165:2116-2123, 2000.
25. Gujral JS, Farhood A, Bajt ML, Jaeschke H: Neutrophils aggravate acute liver injury during obstructive cholestasis in bile ductYligated mice. Hepatology 38:355-363, 2003.
26. Schagat TL, Wofford JA, Greene KE, Wright JR: Surfactant protein A differentially regulates peripheral and inflammatory neutrophil chemotaxis. Am J Physiol Lung Cell Mol Physiol 284:L140-L147, 2003.
27. Lee TS, Tsai HL, Chau LY: Induction of heme oxygenase-1 expression in murine macrophages is essential for the anti-inflammatory effect of low dose 15-deoxy-Delta 12,14-prostaglandin J2. J Biol Chem 278:19325-19330, 2003.
28. Sakamoto K, Kuribayashi F, Nakamura M, Takeshige K: Involvement of p38 MAP kinase in not only activation of the phagocyte NADPH oxidase induced by formyl-methionyl-leucyl-phenylalanine but also determination of the extent of the activity. J Biochem 140:739-745, 2006.
29. Weiner OD, Rentel MC, Ott A, Brown GE, Jedrychowski M, Yaffe MB, Gygi SP, Cantley LC, Bourne HR, Kirschner MW: Hem-1 complexes are essential for Rac activation, actin polymerization, and myosin regulation during neu-trophil chemotaxis. PLoS Biol 4:e38, 2006.
30. Kutsuna H, Suzuki K, Kamata N, Kato T, Hato F, Mizuno K, Kobayashi H, Ishii M, Kitagawa S: Actin reorganization and morphological changes in human neutrophils stimulated by TNF, GM-CSF, and G-CSF: the role of MAP kinases. Am J Physiol Cell Physiol 286:C55-C64, 2004.
31. Heit B, Colarusso P, Kubes P: Fundamentally different roles for LFA-1, Mac-1 and alpha4-integrin in neutrophil chemotaxis. J Cell Sci 118:5205-5220, 2005.
32. Heit B, Liu L, Colarusso P, Puri KD, Kubes P: PI3K accelerates, but is not required for, neutrophil chemotaxis to fMLP. J Cell Sci 121:205-214, 2008.
33. Vicente AM, Guillen MI, Habib A, Alcaraz MJ: Beneficial effects of heme oxygenase-1 up-regulation in the development of experimental inflammation induced by zymosan. J Pharmacol Exp Ther 307:1030-1037, 2003.
34. Kaizu T, Ikeda A, Nakao A, Tsung A, Toyokawa H, Ueki S, Geller DA, Murase N: Protection of transplant-induced hepatic ischemia/reperfusion injury with carbon monoxide via MEK/ERK1/2 pathway downregulation. Am J Physiol Gastrointest Liver Physiol 294:G236-G244, 2008.
35. Selvatici R, Falzarano S, Mollica A, Spisani S: Signal transduction pathways triggered by selective formylpeptide analogues in human neutrophils. Eur J Pharmacol 534:1-11, 2006.