Apolipoprotein A-II suppressed concanavalin a-induced hepatitis via the inhibition of CD4 T cell function

Journal of Immunology

Volumn 186, Issue 6, 2011, Pages 3410-3420

  Yamashita, Junji ^a,b   Iwamura, Chiaki ^a   Sasaki, Tetsuya ^a,b   Mitsumori, Kunitoshi ^c   Ohshima, Kazutoshi ^b   Hada, Kaori ^b   Hara, Naoko ^b   Takahashi, Munehisa ^b   Kaneshiro, Yoshiaki ^b   Tanaka, Hitoshi ^b   Kaneko, Kenji ^b   Nakayama, Toshinori ^a  

^a CHIBA UNIVERSITY   (Japan)

^b Research Division   (Japan)

^c TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A2; CONCANAVALIN A; GAMMA INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE; PREDNISOLONE; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELL NUCLEUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TOXIC HEPATITIS;

ANIMALS; APOLIPOPROTEIN A-II; AUTOIMMUNE DISEASES; CD4-POSITIVE T-LYMPHOCYTES; CELL MIGRATION INHIBITION; CELL MOVEMENT; CONCANAVALIN A; FEMALE; GENE KNOCKOUT TECHNIQUES; GROWTH INHIBITORS; HEPATITIS, ANIMAL; HUMANS; INTERFERON-GAMMA; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT;

EID: 79953183018     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002924     Document Type: Article

References (55)

1. Alvarez, F., P. A. Berg, F. B. Bianchi, L. Bianchi, A. K. Burroughs, E. L. Cancado, R. W. Chapman, W. G. Cooksley, A. J. Czaja, V. J. Desmet, et al. 1999. International Autoimmune Hepatitis Group Report: review of criteria for diagnosis of autoimmune hepatitis. J. Hepatol. 31: 929-938.
2. Gregorio, G. V., B. Portmann, F. Reid, P. T. Donaldson, D. G. Doherty, M. McCartney, A. P. Mowat, D. Vergani, and G. Mieli-Vergani. 1997. Auto-immune hepatitis in childhood: a 20-year experience. Hepatology 25: 541-547. (Pubitemid 27106430)
3. Montano Loza, A. J., and A. J. Czaja. 2007. Current therapy for autoimmune hepatitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 4: 202-214.
4. Heneghan, M. A., and I. G. McFarlane. 2002. Current and novel immunosuppressive therapy for autoimmune hepatitis. Hepatology 35: 7-13.
5. Bogdanos, D. P., G. Mieli-Vergani, and D. Vergani. 2000. Virus, liver and autoimmunity. Dig. Liver Dis. 32: 440-446.
6. Chang, K. M., R. Thimme, J. J. Melpolder, D. Oldach, J. Pemberton, J. Moorhead-Loudis, J. G. McHutchison, H. J. Alter, and F. V. Chisari. 2001. Differential CD4(+) and CD8(+) T-cell responsiveness in hepatitis C virus infection. Hepatology 33: 267-276.
7. Chedid, A., C. L. Mendenhall, T. E. Moritz, S. W. French, T. S. Chen, T. R. Morgan, G. A. Roselle, B. A. Nemchausky, C. H. Tamburro, E. R. Schiff, et al. 1993. Cell-mediated hepatic injury in alcoholic liver disease. Veterans Affairs Cooperative Study Group 275. Gastroenterology 105: 254-266. (Pubitemid 23234044)
8. Kita, H., I. R. Mackay, J. Van De Water, and M. E. Gershwin. 2001. The lymphoid liver: considerations on pathways to autoimmune injury. Gastroenterology 120: 1485-1501.
9. Rehermann, B., and F. V. Chisari. 2000. Cell mediated immune response to the hepatitis C virus. Curr. Top. Microbiol. Immunol. 242: 299-325.
10. Eggink, H. F., H. J. Houthoff, S. Huitema, C. H. Gips, and S. Poppema. 1982. Cellular and humoral immune reactions in chronic active liver disease. I. Lymphocyte subsets in liver biopsies of patients with untreated idiopathic autoimmune hepatitis, chronic active hepatitis B and primary biliary cirrhosis. Clin. Exp. Immunol. 50: 17-24.
11. Löhr, H. F., J. F. Schlaak, A. W. Lohse, W. O. Böcher, M. Arenz, G. Gerken, and K. H. Meyer Zum Büschenfelde. 1996. Autoreactive CD4+ LKM-specific and anticlonotypic T-cell responses in LKM-1 antibody-positive autoimmune hepatitis. Hepatology 24: 1416-1421.
12. Tiegs, G., J. Hentschel, and A. Wendel. 1992. A T cell-dependent experimental liver injury in mice inducible by concanavalin A. J. Clin. Invest. 90: 196-203.
13. Küsters, S., F. Gantner, G. Künstle, and G. Tiegs. 1996. Interferon gamma plays a critical role in T cell-dependent liver injury in mice initiated by concanavalin A. Gastroenterology 111: 462-471. (Pubitemid 26256736)
14. Mizuhara, H., M. Uno, N. Seki, M. Yamashita, M. Yamaoka, T. Ogawa, K. Kaneda, T. Fujii, H. Senoh, and H. Fujiwara. 1996. Critical involvement of interferon gamma in the pathogenesis of T-cell activation-associated hepatitis and regulatory mechanisms of interleukin-6 for the manifestations of hepatitis. Hepatology 23: 1608-1615. (Pubitemid 26181246)
15. Toyonaga, T., O. Hino, S. Sugai, S. Wakasugi, K. Abe, M. Shichiri, and K. Yamamura. 1994. Chronic active hepatitis in transgenic mice expressing interferon-gamma in the liver. Proc. Natl. Acad. Sci. USA 91: 614-618.
16. Kaneko, Y., M. Harada, T. Kawano, M. Yamashita, Y. Shibata, F. Gejyo, T. Nakayama, and M. Taniguchi. 2000. Augmentation of Valpha14 NKT cell-mediated cytotoxicity by interleukin 4 in an autocrine mechanism resulting in the development of concanavalin A-induced hepatitis. J. Exp. Med. 191: 105-114.
17. Miller, N. E. 1987. Associations of high-density lipoprotein subclasses and apolipoproteins with ischemic heart disease and coronary atherosclerosis. Am. Heart J. 113: 589-597.
18. Tall, A. R. 1990. Plasma high density lipoproteins. Metabolism and relationship to atherogenesis. J. Clin. Invest. 86: 379-384.
19. Bu, X., C. H. Warden, Y. R. Xia, C. De Meester, D. L. Puppione, S. Teruya, B. Lokensgard, S. Daneshmand, J. Brown, R. J. Gray, et al. 1994. Linkage analysis of the genetic determinants of high density lipoprotein concentrations and composition: evidence for involvement of the apolipoprotein A-II and cholesteryl ester transfer protein loci. Hum. Genet. 93: 639-648.
20. Vu-Dac, N., K. Schoonjans, V. Kosykh, J. Dallongeville, R. A. Heyman, B. Staels, and J. Auwerx. 1996. Retinoids increase human apolipoprotein A-11 expression through activation of the retinoid X receptor but not the retinoic acid receptor. Mol. Cell. Biol. 16: 3350-3360.
21. Castellani, L. W., M. Navab, B. J. Van Lenten, C. C. Hedrick, S. Y. Hama, A. M. Goto, A. M. Fogelman, and A. J. Lusis. 1997. Overexpression of apolipoprotein AII in transgenic mice converts high density lipoproteins to proinflammatory particles. J. Clin. Invest. 100: 464-474.
22. Alexander, E. T., M. Tanaka, M. Kono, H. Saito, D. J. Rader, and M. C. Phillips. 2009. Structural and functional consequences of the Milano mutation (R173C) in human apolipoprotein A-I. J. Lipid Res. 50: 1409-1419.
23. Weng, W., and J. L. Breslow. 1996. Dramatically decreased high density lipoprotein cholesterol, increased remnant clearance, and insulin hypersensitivity in apolipoprotein A-II knockout mice suggest a complex role for apolipoprotein A-II in atherosclerosis susceptibility. Proc. Natl. Acad. Sci. USA 93: 14788-14794.
24. Weng, W., N. A. Brandenburg, S. Zhong, J. Halkias, L. Wu, X. C. Jiang, A. Tall, and J. L. Breslow. 1999. ApoA-II maintains HDL levels in part by inhibition of hepatic lipase. Studies In apoA-II and hepatic lipase double knockout mice. J. Lipid Res. 40: 1064-1070.
25. Cohn, E. J., J. L. Oncley, L. E. Strong, W. L. Hughes, and S. H. Armstrong. 1944. Chemical, clinical, and immunological studies on the products of human plasma fractionation. I. The characterization of the protein fractions of human plasma. J. Clin. Invest. 23: 417-432.
26. Peitsch, M. C., A. Kress, P. G. Lerch, J. J. Morgenthaler, H. Isliker, and H. J. Heiniger. 1989. A purification method for apolipoprotein A-I and A-II. Anal. Biochem. 178: 301-305.
27. Yang, K. S., S. W. Kang, H. A. Woo, S. C. Hwang, H. Z. Chae, K. Kim, and S. G. Rhee. 2002. Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid. J. Biol. Chem. 277: 38029-38036.
28. Kimura, M. Y., H. Hosokawa, M. Yamashita, A. Hasegawa, C. Iwamura, H. Watarai, M. Taniguchi, T. Takagi, S. Ishii, and T. Nakayama. 2005. Regulation of T helper type 2 cell differentiation by murine Schnurri-2. J. Exp. Med. 201: 397-408.
29. Goossens, P. L., H. Jouin, G. Marchal, and G. Milon. 1990. Isolation and flow cytometric analysis of the free lymphomyeloid cells present in murine liver. J. Immunol. Methods 132: 137-144. (Pubitemid 20263871)
30. Watanabe, H., K. Ohtsuka, M. Kimura, Y. Ikarashi, K. Ohmori, A. Kusumi, T. Ohteki, S. Seki, and T. Abo. 1992. Details of an isolation method for hepatic lymphocytes in mice. J. Immunol. Methods 146: 145-154.
31. Kimura, M., Y. Koseki, M. Yamashita, N. Watanabe, C. Shimizu, T. Katsumoto, T. Kitamura, M. Taniguchi, H. Koseki, and T. Nakayama. 2001. Regulation of Th2 cell differentiation by mel-18, a mammalian polycomb group gene. Immunity 15: 275-287. (Pubitemid 32816876)
32. Yamashita, M., M. Kimura, M. Kubo, C. Shimizu, T. Tada, R. M. Perlmutter, and T. Nakayama. 1999. T cell antigen receptor-mediated activation of the Ras/ mitogen-activated protein kinase pathway controls interleukin 4 receptor function and type-2 helper T cell differentiation. Proc. Natl. Acad. Sci. USA 96: 1024-1029.
33. Ajuebor, M. N., C. M. Hogaboam, T. Le, A. E. Proudfoot, and M. G. Swain. 2004. CCL3/MIP-1alpha is pro-inflammatory in murine T cell-mediated hepatitis by recruiting CCR1-expressing CD4(+) T cells to the liver. Eur. J. Immunol. 34: 2907-2918.
34. Leifeld, L., F. L. Dumoulin, I. Purr, K. Janberg, C. Trautwein, M. Wolff, M. P. Manns, T. Sauerbruch, and U. Spengler. 2003. Early up-regulation of chemokine expression in fulminant hepatic failure. J. Pathol. 199: 335-344. (Pubitemid 36266856)
35. Gantner, F., M. Leist, A. W. Lohse, P. G. Germann, and G. Tiegs. 1995. Concanavalin A-induced T-cell-mediated hepatic injury in mice: the role of tumor necrosis factor. Hepatology 21: 190-198.
36. Tagawa, Y., K. Sekikawa, and Y. Iwakura. 1997. Suppression of concanavalin A-induced hepatitis in IFN-gamma(-/-) mice, but not in TNF-alpha(-/-) mice: role for IFN-gamma in activating apoptosis of hepatocytes. J. Immunol. 159: 1418-1428. (Pubitemid 127484121)
37. Kano, A., T. Haruyama, T. Akaike, and Y. Watanabe. 1999. IRF-1 is an essential mediator in IFN-gamma-induced cell cycle arrest and apoptosis of primary cultured hepatocytes. Biochem. Biophys. Res. Commun. 257: 672-677.
38. Bonder, C. S., M. N. Ajuebor, L. D. Zbytnuik, P. Kubes, and M. G. Swain. 2004. Essential role for neutrophil recruitment to the liver in concanavalin A-induced hepatitis. J. Immunol. 172: 45-53.
39. Gantner, F., M. Leist, S. Küsters, K. Vogt, H. D. Volk, and G. Tiegs. 1996. T cell stimulus-induced crosstalk between lymphocytes and liver macrophages results in augmented cytokine release. Exp. Cell Res. 229: 137-146.
40. Bournazou, I., J. D. Pound, R. Duffin, S. Bournazos, L. A. Melville, S. B. Brown, A. G. Rossi, and C. D. Gregory. 2009. Apoptotic human cells inhibit migration of granulocytes via release of lactoferrin. J. Clin. Invest. 119: 20-32.
41. Nagata, T., L. McKinley, J. J. Peschon, J. F. Alcorn, S. J. Aujla, and J. K. Kolls. 2008. Requirement of IL-17RA in Con A induced hepatitis and negative regulation of IL-17 production in mouse T cells. J. Immunol. 181: 7473-7479.
42. Narumi, S., Y. Tominaga, M. Tamaru, S. Shimai, H. Okumura, K. Nishioji, Y. Itoh, and T. Okanoue. 1997. Expression of IFN-inducible protein-10 in chronic hepatitis. J. Immunol. 158: 5536-5544. (Pubitemid 127681264)
43. Shields, P. L., C. M. Morland, M. Salmon, S. Qin, S. G. Hubscher, and D. H. Adams. 1999. Chemokine and chemokine receptor interactions provide a mechanism for selective T cell recruitment to specific liver compartments within hepatitis C-infected liver. J. Immunol. 163: 6236-6243.
44. Kusano, F., Y. Tanaka, F. Marumo, and C. Sato. 2000. Expression of C-C chemokines is associated with portal and periportal inflammation in the liver of patients with chronic hepatitis C. Lab. Invest. 80: 415-422.
45. Afford, S. C., N. C. Fisher, D. A. Neil, J. Fear, P. Brun, S. G. Hubscher, and D. H. Adams. 1998. Distinct patterns of chemokine expression are associated with leukocyte recruitment in alcoholic hepatitis and alcoholic cirrhosis. J. Pathol. 186: 82-89.
46. Adams, D. H., S. Hubscher, J. Fear, J. Johnston, S. Shaw, and S. Afford. 1996. Hepatic expression of macrophage inflammatory protein-1 alpha and macrophage inflammatory protein-1 beta after liver transplantation. Transplantation 61: 817-825. (Pubitemid 26097246)
47. Schenk, M., A. Zipfel, C. Schulz, H. D. Becker, and R. Viebahn. 2000. RANTES in the postoperative course after liver transplantation. Transpl. Int. 13(Suppl. 1): S147-S149.
48. Ajuebor, M. N., A. I. Aspinall, F. Zhou, T. Le, Y. Yang, S. J. Urbanski, S. Sidobre, M. Kronenberg, C. M. Hogaboam, and M. G. Swain. 2005. Lack of chemokine receptor CCR5 promotes murine fulminant liver failure by preventing the apoptosis of activated CD1d-restricted NKT cells. J. Immunol. 174: 8027-8037.
49. Diao, H., S. Kon, K. Iwabuchi, C. Kimura, J. Morimoto, D. Ito, T. Segawa, M. Maeda, J. Hamuro, T. Nakayama, et al. 2004. Osteopontin as a mediator of NKT cell function in T cell-mediated liver diseases. Immunity 21: 539-550. (Pubitemid 39370509)
50. Rooney, J. W., T. Hoey, and L. H. Glimcher. 1995. Coordinate and cooperative roles for NF-AT and AP-1 in the regulation of the murine IL-4 gene. Immunity 2: 473-483.
51. Kopp, E. B., and S. Ghosh. 1995. NF-kappa B and rel proteins in innate immunity. Adv. Immunol. 58: 1-27.
52. Rao, A. 1994. NF-ATp: a transcription factor required for the co-ordinate induction of several cytokine genes. Immunol. Today 15: 274-281. (Pubitemid 24170521)
53. Rao, A., C. Luo, and P. G. Hogan. 1997. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15: 707-747.
54. Czaja, A. J., and H. A. Carpenter. 2004. Decreased fibrosis during corticosteroid therapy of autoimmune hepatitis. J. Hepatol. 40: 646-652.
55. Jones, E. A., and N. V. Bergasa. 1993. Immunosuppressive treatment of chronic liver disease. Ann. N. Y. Acad. Sci. 696: 319-327.