Amelioration of non-alcoholic steatohepatitis and glucose intolerance in ob/ob mice by oral immune regulation towards liver-extracted proteins is associated with elevated intrahepatic NKT lymphocytes and serum IL-10 levels

Journal of Pathology

Volumn 208, Issue 1, 2006, Pages 74-81

  Elinav, Eran ^a   Pappo, Orit ^a   Sklair Levy, Miriam ^a   Margalit, Maya ^a   Shibolet, Oren ^a   Gomori, Moshe ^a   Alper, Roslana ^a   Thalenfeld, Barbara ^b   Engelhardt, Dean ^b   Rabbani, Elazar ^b   Ilan, Yaron ^a,c  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b Enzon Incorporated   (United States)

^c HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

NASH; NKT lymphocytes; Ob ob mice; Oral immune regulation

Indexed keywords

INTERLEUKIN 10; LIVER EXTRACT; LIVER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; FAT CONTENT; FLOW CYTOMETRY; GLUCOSE INTOLERANCE; HISTOPATHOLOGY; IMMUNOREGULATION; IMMUNOTHERAPY; LYMPHOCYTE SUBPOPULATION; MALE; MOUSE; NATURAL KILLER CELL; NONALCOHOLIC FATTY LIVER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SIGNAL DETECTION; STATISTICAL SIGNIFICANCE; T LYMPHOCYTE; TH1 CELL; TH2 CELL; WILD TYPE;

ADIPOSE TISSUE; ADMINISTRATION, ORAL; ANIMALS; ANTIGENS; CYTOKINES; FATTY LIVER; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; HEPATITIS; INTERLEUKIN-10; KILLER CELLS, NATURAL; LIVER; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; TRIGLYCERIDES;

EID: 29744447771     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/path.1869     Document Type: Article

References (44)

1. Pelleymounter MA, Cullen MF, Baker MB, Hecht R, Winters D, Boone T, Collins F. Effects of the obese gene product on body weight regulation in Ob/Ob mice. Science 1995;269(5223):540-543.
2. Cohen B, Novick D, Rubinstein M. Modulation of insulin activities by leptin. Science 1996;274(5290):1185-1188.
3. Howard JK, Lord GM, Matarese G, Vendetti S, Chatei A, Ritter MA, et al. Leptin protects mice from starvation induced lymphoid atrophy and increases thymic cellularity in Ob/Ob mice. J Clin Invest 1999;104(8):1051-1059.
4. Lord GM, Matarese G, Howard KJ, Baker RJ, Bloom SR, Lechler RI. Leptin modulates the T cell immune response and reverses starvation-induced immunosuppression. Nature 1998;394(6696):897-901.
5. Guebre-Xabier M, Yang SQ, Lin HZ, Schwenk R, Krytch U, Diehl AM. Altered hepatic lymphocyte subpopulations in obesity-related fatty livers. Hepatology 2000;31(3):633-640.
6. Lee FJ, Li Y, Yang EK, Yang SQ, Lin HZ, Trush MA, et al. Phenotypic abnormalities in macrophages from leptin-deficient obese mice. Am J Physiol 1999;276(2):c386-c394.
7. Loffreda S, Yang SQ, Lin HZ, Karp CL, Brengman M, Wang DG, et al. Leptin regulates proinflammatory immune responses. FASEB J 1998;12(1):57-65.
8. Li Z, Lin H, Yang S, Diehl AM. Murine leptin deficiency alters Kupffer cell production of cytokines that regulate the innate immune system. Gastroenterology 2002;123(4):1304-1310.
9. Tilg H, Diehl AM. Cytokines in alcoholic and non-alcoholic steatohepatitis. N Eng J Med 2000;343(20):1467-1476.
10. Yang SQ, Lin HZ, Lane MD, Clemens M, Diehl AM. Obesity increases sensitivity to endotoxin liver injury: implications for pathogenesis of steatohepatitis. Proc Natl Acad Sci USA 1997;94(6):2557-2562.
11. Faggioni R, Fantuzzi G, Gabay C, Moser A, Dinarello CA, Feingold KR, Grunfeld C. Leptin deficiency enhances sensitivity to endotoxin-induced lethality. Am J Physiol 1999;276(1):R136-R142.
12. Faggioni R, Jones-Carson J, Reed DA, Dinarello CA, Feingold KR, Grunfeld C, Fantuzzi G. Leptin-deficient (Ob/Ob) mice are protected from T cell-mediated hepatotoxicity: role of tumor necrosis factor-α and IL-18. Proc Natl Acad Sci USA 2000;97(5):2367-2372.
13. Kugelmas M, Hill DB, Vivian B, Marsano L, McClain CJ. Cytokines and NASH: a pilot study of the effects of lifestyle modification and vitamin E. Hepatology 2003;38(2):413-419.
14. Friedman A, Weiner H. Induction of anergy or active suppression following oral tolerance is determined by antigen dosage. Proc Natl Acad Sci USA 1994;91(14):6688-6692.
15. Mitchell DG, Kim I, Chang TS, et al. Chemical shift phase-difference and suppression magnetic resonance imaging techniques in animals, phantoms and humans: fatty liver. Invest Radiol 1991;26(12):1041-1052.
16. Mitchell DG, Crovello M, Matteucci T, Petersen RO, Miettinen MM. Benign adrenocortical masses: diagnosis with chemical shift MR imaging. Radiology 1992;185(2):345-351.
17. Mayo-Smith WW, Lee MJ, McNicholas MMJ, Hahn PF, Boland GW, Saini S. Characterization of adrenal masses (<5 cm) by use of chemical shift MR imaging: observer performance versus quantitative measures. Am J Roentgenol 1995;165(1):91-95.
18. Namimoto T, Yamashita Y, Mitsuzaki K, Nakayama Y, Makita O, Kadota M, Takahashi M. Adrenal masses: quantification of fat content with double-echo chemical shift in-phase and opposed-phase FLASH MR images for differentiation of adrenal adenomas. Radiology 2001;218(3):642-646.
19. Brunt EM. Nonalcoholic steatohepatitis: definition and pathology. Semin Liv Dis 2001;21(1):3-16.
20. Trop S, Samsonov D, Gotsman I, Alper R, Diment J, Ilan Y. Liver-associated lymphocytes expressing NK1.1 are essential for oral tolerance induction in a murine model. Hepatology 1999;29(3):746-755.
21. Bendelac A, Rivera MN, Park SH, Roark JH. Mouse CD1-specific NK 1.1 T cells: development, specificity, and function. Annu Rev Immunol 1997;15:532-562.
22. Bendelac A. Selection and adaptation of cells expressing major histocompatibility complex class-I specific receptors of the natural killer complex. J Exp Med 1997;186(3):349-351.
23. Godfrey DJ, Hammond KJ, Poulon LD, Smyth MJ, Baxter AG. NKT cells: facts, functions and fallacies. Immunol Today 2000;21:573-583.
24. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K, et al. CD1d-restricted and TCR-mediated activation of α14 NKT cells by glycosylceramides. Science 1997;28(5342):1626-1629.
25. Bendelac A, Fearon DT. Innate pathways that control acquired immunity. Curr Opin Immunol 1997;9(1):1-3.
26. Baxter AG, Kinder SJ, Hammond KJL, Scollay R, Godfrey DI. Association between abTCR + CD4-CD8-T cell deficiency and IDDM in NOD/Lt mice. Diabetes 1997;46:572-582.
27. Hammond KJL, Poulton LD, Palmisano LJ, Silveira PA, Godfrey DI, Baxter AG. α/β-T cell receptor (TCR) + CD4-CD8-(NKT) thymocytes prevent insulin-dependent diabetes mellitus in non-obese diabetic (NOD)/Lt mice by the influence of interleukin (IL)-4 and/or IL-10. J Exp Med 1998;187:1047-1056.
28. Miyamoto K, Miyake S, Yamamura T. A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing Th2 bias of natural killer T cells. Nature 2001;413:531-534.
29. Takeda K, Dennert G. The development of autoimmunity in C57BL/6 lpr mice correlates with the disappearance of natural killer type-1 positive cells: evidence of their suppressive action on one marrow stem cell proliferation, B cell immunoglobulin secretion, and autoimmune symptoms. J Exp Med 1993;177:155-164.
30. + cells in oral immunoregulation of experimental colitis. Inflamm Bowel Dis 2003;9(2):75-86.
31. Wilson SB, Kent SC, Patton KT, et al. Extreme Th1 bias of invariant Vα24-JαQ T cells in type 1 diabetes. Nature 1998; 291:177-181.
32. Illes Z, Kondo T, Newcombe J, Oka N, Tabira T, Yamamura T. Differential expression of NK T cell Vα24JαQ invariant TCR chain in the lesions of multiple sclerosis and chronic inflammatory demyelination polyneuropathy. J Immunol 2000;164:4375-4381.
33. + T helper cells in humans augment the production of pathogenic anti-DNA autoantibodies associated with lupus nephritis. J Immunol 1989;143:103-112.
34. + double-negative regulatory natural killer T cells in autoimmune diseases. Arthritis Rheum 2001;44:1127-1138.
35. Kennedy MK, Glaccum M, Brown SN, Burz EA, Viney JL, Embers M, et al. Reversible defects in natural killer and memory CD8 T cell lineage in interleukin 15-deficient mice. J Exp Med 2000;191(5):771-780.
36. Takeda K, Hayakawa Y, Van Kaer L, Matsuda H, Yagita H, Okumura K. Critical contribution of liver natural killer T cells to a murine model of hepatitis. Proc Natl Acad Sci USA 2000;97(10):5498-5503.
37. Yuan M, Konstantopoulos N, Lee J, Hansen L, Li ZW, Karin M, Shoelson SE. Reversal of obesity and diet induced insulin resistance with salicylates or targeted disruption of IKK β. Science 2001;293(5535):1673-1677.
38. Shibolet O, Alper R, Avraham Y, Berry EM, Ilan Y. Immunomodulation of experimental colitis via caloric restriction: role of NK 1.1 T cells. Clin Immunol 2002;105(1):48-56.
39. Carvalho CR, Verdolin BA, Vaz NM. Indirect effects of oral tolerance cannot be ascribed to bystander suppression. Scand J Immunol 1997;45(3):276-281.
40. Stephens JM, Pekala PH. Transcriptional repression of the GLUT 4 and the C/ERB genes in 3T3-L1 adipocytes by tumor necrosis factor alpha. J Biol Chem 1991;266(32):21 839-21 845.
41. Koteish A, Diehl AM. Animal models of steatosis. Semin Liver Dis 2001;21(1):89-104.
42. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Protection from obesity-induced insulin resistance in mice lacking TNFα function. Nature 1997;389(665):610-614.
43. Solomon SS, Mishra SK, Cwik C, Rajanna B, Postlethwaite AE. Pioglitazone and metformin reverse insulin resistance induced by tumor necrosis factor alpha in liver cells. Horm Metab Res 1997;29(8):390-382.
44. Day CP, James OF. Steatohepatitis: a tale of two hits? Gastroenterology 1998;114(4):842-845.