Cyclooxygenase-2 deficiency enhances Th2 immune responses and impairs neutrophil recruitment in hepatic ischemia/reperfusion injury

Journal of Immunology

Volumn 180, Issue 3, 2008, Pages 1843-1853

  Hamada, Takashi ^a   Tsuchihashi, Seiichiro ^a,b   Avanesyan, Armine ^a   Duarte, Sergio ^a   Moore, Carolina ^a   Busuttil, Ronald W ^a   Coito, Ana J ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CXCL2 CHEMOKINE; CYCLOOXYGENASE 2; GELATINASE B; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; PROTEIN BCL 2; PROTEIN BCL XL; CELECOXIB; CYCLOOXYGENASE 2 INHIBITOR; CYTOKINE; PROTEIN BCL X; PYRAZOLE DERIVATIVE; SULFONAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CELL INFILTRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; EFFECTOR CELL; ENZYME ACTIVATION; ENZYME DEFICIENCY; LIVER INJURY; LIVER ISCHEMIA; MACROPHAGE ACTIVATION; MALE; MOUSE; NEUTROPHIL; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; TH1 CELL; TH2 CELL; WILD TYPE; ANIMAL; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; IMMUNOLOGY; LIVER; METABOLISM; MOUSE MUTANT; NEUTROPHIL CHEMOTAXIS; VASCULARIZATION;

ANIMALS; BCL-X PROTEIN; CHEMOKINE CXCL2; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; CYTOKINES; DOWN-REGULATION; LIVER; MACROPHAGE ACTIVATION; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRAZOLES; REPERFUSION INJURY; SULFONAMIDES; TH1 CELLS; TH2 CELLS;

EID: 40749128112     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.3.1843     Document Type: Article

References (67)

1. Howard, T. K., G. B. Klintmalm, J. B. Cofer, B. S. Husberg, R. M. Goldstein, and T. A. Gonwa. 1990. The influence of preservation injury on rejection in the hepatic transplant recipient. Transplantation 49: 103-107.
2. Jaeschke, H., A. Farhood, and C. W. Smith. 1990. Neutrophils contribute to ischemia/reperfusion injury in rat liver in vivo. FASEB J. 4: 3355-3359.
3. Caldwell-Kenkel, J. C., R. T. Currin, Y. Tanaka, R. G. Thurman, and J. J. Lemasters. 1991. Kupffer cell activation and endothelial cell damage after storage of rat livers: effects of reperfusion. Hepatology 13: 83-95.
4. Funk, C. D. 2001. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294: 1871-1875.
5. Yokoyama, C., and T. Tanabe. 1989. Cloning of human gene encoding prostaglandin endoperoxide synthase and primary structure of the enzyme. Biochem. Biophys. Res. Commun. 165: 888-894.
6. Smith, W. L., and D. L. DeWitt. 1996. Prostaglandin endoperoxide H synthases-1 and -2. Adv. Immunol. 62: 167-215.
7. Seibert, K., Y. Zhang, K. Leahy, S. Hauser, J. Masferrer, and P. Isakson. 1997. Distribution of COX-1 and COX-2 in normal and inflamed tissues. Adv. Exp. Med. Biol. 400A: 167-170.
8. Morita, I. 2002. Distinct functions of COX-1 and COX-2. Prostaglandins Other Lipid Mediat. 68-69: 165-175.
9. Masferrer, J. L., B. S. Zweifel, P. T. Manning, S. D. Hauser, K. M. Leahy, W. G. Smith, P. C. Isakson, and K. Seibert. 1994. Selective inhibition of inducible cyclooxygenase 2 in vivo is antiinflammatory and nonulcerogenic. Proc. Natl. Acad. Sci. USA 91: 3228-3232.
10. Tilley, S. L., T. M. Coffman, and B. H. Koller. 2001. Mixed messages: modulation of inflammation and immune responses by prostaglandins and thromboxanes. J. Clin. Invest. 108: 15-23.
11. Cheng, H. F., C. J. Wang, G. W. Moeckel, M. Z. Zhang, J. A. McKanna, and R. C. Harris. 2002. Cyclooxygenase-2 inhibitor blocks expression of mediators of renal injury in a model of diabetes and hypertension. Kidney Int. 62: 929-939.
12. Iadecola, C., K. Niwa, S. Nogawa, X. Zhao, M. Nagayama, E. Araki, S. Morham, and M. E. Ross. 2001. Reduced susceptibility to ischemic brain injury and N-methyl-D-aspartate-mediated neurotoxicity in cyclooxygenase-2- deficient mice. Proc. Natl. Acad. Sci. USA 98: 1294-1299.
13. Myers, L. K., A. H. Kang, A. E. Postlethwaite, E. F. Rosloniec, S. G. Morham, B. V. Shlopov, S. Goorha, and L. R. Ballou. 2000. The genetic ablation of cyclooxygenase 2 prevents the development of autoimmune arthritis. Arthritis Rheum. 43: 2687-2693.
14. Bonner, J. C., A. B. Rice, J. L. Ingram, C. R. Moomaw, A. Nyska, A. Bradbury, A. R. Sessoms, P. C. Chulada, D. L. Morgan, D. C. Zeldin, and R. Langenbach. 2002. Susceptibility of cyclooxygenase-2-deficient mice to pulmonary fibrogenesis. Am. J. Pathol. 161: 459-470.
15. Cheng, A. S., H. L. Chan, N. W. Leung, C. T. Liew, K. F. To, P. B. Lai, and J. J. Sung. 2002. Expression of cyclooxygenase-2 in chronic hepatitis B and the effects of anti-viral therapy. Aliment. Pharmacol. Ther. 16: 251-260.
16. Manning, D. S., K. M. Sheehan, M. F. Byrne, E. W. Kay, and F. E. Murray. 2007. Cyclooxygenase-2 expression in chronic hepatitis C and the effect of interferon α treatment. J. Gastroenterol. Hepatol. 22: 1633-1637.
17. Cheng, A. S., H. L. Chan, W. K. Leung, K. F. To, M. Y. Go, J. Y. Chan, C. T. Liew, and J. J. Sung. 2004. Expression of HBx and COX-2 in chronic hepatitis B, cirrhosis, and hepatocellular carcinoma: implication of HBx in upregulation of COX-2. Mod. Pathol. 17: 1169-1179.
18. Claria, J., J. D. Kent, M. Lopez-Parra, G. Escolar, L. Ruiz-Del-Arbol, P. Gines, W. Jimenez, B. Vucelic, and V. Arroyo. 2005. Effects of celecoxib and naproxen on renal function in nonazotemic patients with cirrhosis and ascites. Hepatology 41: 579-587.
19. Yu, J., L. Qiao, L. Zimmermann, M. P. Ebert, H. Zhang, W. Lin, C. Rocken, P. Malfertheiner, and G. C. Farrell. 2006. Troglitazone inhibits tumor growth in hepatocellular carcinoma in vitro and in vivo. Hepatology 43: 134-143.
20. Moore, C., X. D. Shen, C. Fondevila, F. Gao, and A. J. Coito. 2005. Blockade of fibronectin-α4β1 adhesive interactions down-regulates cyclooxygenase-2 inducible nitric oxide synthase and prolongs recipient survival in a 24-hour model of cold hepatic ischemia-reperfusion injury. Transplant. Proc. 37: 1682-1683.
21. Takeyoshi, I., Y. Sunose, S. Iwazaki, H. Tsutsumi, M. Aiba, M. Kasahara, S. Ohwada, K. Matsumoto, and Y. Morishita. 2001. The effect of a selective cyclooxygenase-2 inhibitor in extended liver resection with ischemia in dogs. J. Surg. Res. 100: 25-31.
22. Ozturk, H., A. Gezici, and H. Ozturk. 2006. The effect of celecoxib, a selective COX-2 inhibitor, on liver ischemia/reperfusion-induced oxidative stress in rats. Hepatol. Res. 34: 76-83.
23. Kobayashi, M., I. Takeyoshi, M. Kurabayashi, K. Matsumoto, and Y. Morishita. 2007. The effects of a cyclooxygenase-2 inhibitor, FK3311, on total hepatic ischemia-reperfusion injury of the rat. Hepatogastroenterology 54: 522-526.
24. Katagiri, H., Y. Ito, K. Ishii, I. Hayashi, M. Suematsu, S. Yamashina, T. Murata, S. Narumiya, A. Kakita, and M. Majima. 2004. Role of thromboxane derived from COX-1 and -2 in hepatic microcirculatory dysfunction during endotoxemia in mice. Hepatology 39: 139-150.
25. Leach, M., L. C. Hamilton, A. Olbrich, G. M. Wray, and C. Thiemermann. 1998. Effects of inhibitors of the activity of cyclo-oxygenase-2 on the hypotension and multiple organ dysfunction caused by endotoxin: a comparison with dexamethasone. Br. J. Pharmacol. 124: 586-592.
26. 2 mediate the protective effects of cyclooxygenase-2 in a mouse model of immunemediated liver injury. Hepatology 45: 159-169.
27. 2 and cyclooxygenase-2. J. Biol. Chem. 275: 20136-20145.
28. Salinas, G., U. C. Rangasetty, B. F. Uretsky, and Y. Birnbaum. 2007. The cyclooxygenase 2 (COX-2) story: it's time to explain, not inflame. J. Cardiovasc. Pharmacol. Ther. 12: 98-111.
29. Hamada, T., C. Fondevila, R. W. Busuttil, and A. J. Coito. 2007. Metalloproteinase-9 deficiency protects against hepatic ischemia/reperfusion injury. Hepatology. In press.
30. Penning, T. D., J. J. Talley, S. R. Bertenshaw, J. S. Carter, P. W. Collins, S. Docter, M. J. Graneto, L. F. Lee, J. W. Malecha, J. M. Miyashiro, et al. 1997. Synthesis and biological evaluation of the 1,5-diarylpyrazole class of cyclooxygenase-2 inhibitors: identification of 4-[5-(4-methylphenyl)-3- (trifluoromethyl)-1H-pyrazol-1-yl]benzenesulfonamide (SC-58635, celecoxib). J. Med. Chem. 40: 1347-1365.
31. Amersi, F., X. D. Shen, C. Moore, J. Melinek, R. W. Busuttil, J. W. Kupiec-Weglinski, and A. J. Coito. 2003. Fibronectin-α4β1 integrin-mediated blockade protects genetically fat Zucker rat livers from ischemia/reperfusion injury. Am. J. Pathol. 162: 1229-1239.
32. Coito, A. J., J. Binder, L. F. Brown, M. de Sousa, W. L. Van De, and J. W. Kupiec-Weglinski. 1995. Anti-TNF-α treatment down-regulates the expression of fibronectin and decreases cellular infiltration of cardiac allografts in rats. J. Immunol. 154: 2949-2958.
33. Moore, C., X. D. Shen, F. Gao, R. W. Busuttil, and A. J. Coito. 2007. Fibronectin-α4β1 integrin interactions regulate metalloproteinase-9 expression in steatotic liver ischemia and reperfusion injury. Am. J. Pathol. 170: 567-577.
34. Warford-Woolgar, L., C. Y. Peng, J. Shuhyta, A. Wakefield, D. Sankaran, M. Ogborn, and H. M. Aukema. 2006. Selectivity of cyclooxygenase isoform activity and prostanoid production in normal and diseased Han:SPRD-cy rat kidneys. Am. J. Physiol 290: F897-F904.
35. Chao, D. T., and S. J. Korsmeyer. 1998. BCL-2 family: regulators of cell death. Annu. Rev. Immunol. 16: 395-419.
36. Ellis, T. N., and B. L. Beaman. 2002. Murine polymorphonuclear neutrophils produce interferon-γ in response to pulmonary infection with Nocardia asteroides. J. Leukocyte Biol. 72: 373-381.
37. Ho, M. K., and T. A. Springer. 1982. Mac-1 antigen: quantitative expression in macrophage populations and tissues, and immunofluorescent localization in spleen. J. Immunol. 128: 2281-2286.
38. Luther, S. A., and J. G. Cyster. 2001. Chemokines as regulators of T cell differentiation. Nat. Immunol. 2: 102-107.
39. Baggiolini, M. 1998. Chemokines and leukocyte traffic. Nature 392: 565-568.
40. + T-lymphocytes mediate ischemia/reperfusion- induced inflammatory responses in mouse liver. J. Clin. Invest. 100: 279-289.
41. Moore, K. W., M. R. de Waal, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765.
42. Hunter, C. A. 2005. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat. Rev. Immunol. 5: 521-531.
43. Iniguez, M. A., C. Punzon, and M. Fresno. 1999. Induction of cyclooxygenase-2 on activated T lymphocytes: regulation of T cell activation by cyclooxygenase-2 inhibitors. J. Immunol. 163: 111-119.
44. Kim, S. F., D. A. Huri, and S. H. Snyder. 2005. Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2. Science 310: 1966-1970.
45. Nathan, C. 1997. Inducible nitric oxide synthase: what difference does it make? J. Clin. Invest. 100: 2417-2423.
46. Colletti, L. M., D. G. Remick, G. D. Burtch, S. L. Kunkel, R. M. Strieter, and D. A. Campbell, Jr. 1990. Role of tumor necrosis factor-α in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J. Clin. Invest. 85: 1936-1943.
47. Selvaraj, S. K., R. K. Giri, N. Perelman, C. Johnson, P. Malik, and V. K. Kalra. 2003. Mechanism of monocyte activation and expression of proinflammatory cytochemokines by placenta growth factor. Blood 102: 1515-1524.
48. Sass, G., K. Koerber, R. Bang, H. Guehring, and G. Tiegs. 2001. Inducible nitric oxide synthase is critical for immune-mediated liver injury in mice. J. Clin. Invest. 107: 439-447.
49. Adams, J. M., and S. Cory. 1998. The Bcl-2 protein family: arbiters of cell survival. Science 281: 1322-1326.
50. Krebs, J. F., R. C. Armstrong, A. Srinivasan, T. Aja, A. M. Wong, A. Aboy, R. Sayers, B. Pham, T. Vu, K. Hoang, et al. 1999. Activation of membrane-associated procaspase-3 is regulated by Bcl-2. J. Cell Biol. 144: 915-926.
51. Ikeda-Matsuo, Y., A. Ota, T. Fukada, S. Uematsu, S. Akira, and Y. Sasaki. 2006. Microsomal prostaglandin E synthase-1 is a critical factor of stroke-reperfusion injury. Proc. Natl. Acad. Sci. USA 103: 11790-11795.
52. Yadav, V. K., G. Lakshmi, and R. Medhamurthy. 2005. Prostaglandin F2α-mediated activation of apoptotic signaling cascades in the corpus luteum during apoptosis: involvement of caspase-activated DNase. J. Biol. Chem. 280: 10357-10367.
53. Jaeschke, H., and T. Hasegawa. 2006. Role of neutrophils in acute inflammatory liver injury. Liver Int. 26: 912-919.
54. Lau, D., H. Mollnau, J. P. Eiserich, B. A. Freeman, A. Daiber, U. M. Gehling, J. Brummer, V. Rudolph, T. Munzel, T. Heitzer, et al. 2005. Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins. Proc. Natl. Acad. Sci. USA 102: 431-436.
55. Khan, K. M., L. R. Howe, and D. J. Falcone. 2004. Extracellular matrix-induced cyclooxygenase-2 regulates macrophage proteinase expression. J. Biol. Chem. 279: 22039-22046.
56. Pavlovic, S., B. Du, K. Sakamoto, K. M. Khan, C. Natarajan, R. M. Breyer, A. J. Dannenberg, and D. J. Falcone. 2006. Targeting prostaglandin E2 receptors as an alternative strategy to block cyclooxygenase-2-dependent extracellular matrix-induced matrix metalloproteinase-9 expression by macrophages. J. Biol. Chem. 281: 3321-3328.
57. Pierce, K. L., D. W. Gil, D. F. Woodward, and J. W. Regan. 1995. Cloning of human prostanoid receptors. Trends Pharmacol. Sci. 16: 253-256.
58. Salgame, P., J. S. Abrams, C. Clayberger, H. Goldstein, J. Convit, R. L. Modlin, and B. R. Bloom. 1991. Differing lymphokine profiles of functional subsets of human CD4 and CD8 T cell clones. Science 254: 279-282.
59. Muthian, G., H. P. Raikwar, C. Johnson, J. Rajasingh, A. Kalgutkar, L. J. Marnett, and J. J. Bright. 2006. COX-2 inhibitors modulate IL-12 signaling through JAK-STAT pathway leading to Th1 response in experimental allergic encephalomyelitis. J. Clin. Immunol. 26: 73-85.
60. Ni, J., Y. Y. Shu, Y. N. Zhu, Y. F. Fu, W. Tang, X. G. Zhong, H. Wang, Y. F. Yang, J. Ren, M. W. Wang, and J. P. Zuo. 2007. COX-2 inhibitors ameliorate experimental autoimmune encephalomyelitis through modulating IFN-γ and IL-10 production by inhibiting T-bet expression. J. Neuroimmunol. 186: 94-103.
61. Suzuki, J., M. Ogawa, H. Futamatsu, H. Kosuge, H. Tanaka, and M. Isobe. 2006. A cyclooxygenase-2 inhibitor alters Th1/Th2 cytokine balance and suppresses autoimmune myocarditis in rats. J. Mol. Cell. Cardiol. 40: 688-695.
62. Yokoyama, Y., B. Toth, W. C. Kitchens, M. G. Schwacha, K. I. Bland, and I. H. Chaudry. 2003. Role of thromboxane in producing portal hypertension following trauma-hemorrhage. Am. J. Physiol. 285: G1293-G1299.
63. Ruiz, P., L. Rey, R. Spurney, T. Coffman, and A. Viciana. 1992. Thromboxane augmentation of alloreactive T cell function. Transplantation 54: 498-505.
64. Rieser, C., G. Bock, H. Klocker, G. Bartsch, and M. Thurnher. 1997. Prostaglandin E2 and tumor necrosis factor α cooperate to activate human dendritic cells: synergistic activation of interleukin 12 production. J. Exp. Med. 186: 1603-1608.
65. Parker, C. W., M. G. Huber, and S. M. Godt. 1995. Modulation of IL-4 production in murine spleen cells by prostaglandins. Cell. Immunol. 160: 278-285.
66. Kaur, K., S. G. Harris, J. Padilla, B. A. Graf, and R. P. Phipps. 1999. Prostaglandin E2 as a modulator of lymphocyte mediated inflammatory and humoral responses. Adv. Exp. Med. Biol. 469: 409-412.
67. McCoy, J. M., J. R. Wicks, and L. P. Audoly. 2002. The role of prostaglandin E2 receptors in the pathogenesis of rheumatoid arthritis. J. Clin. Invest. 110: 651-658.