Biliary apotopes and anti-mitochondrial antibodies activate innate immune responses in primary biliary cirrhosis

Hepatology

Volumn 52, Issue 3, 2010, Pages 987-998

  Lleo, Ana ^a,b   Bowlus, Christopher L ^a   Yang, Guo Xiang ^a   Invernizzi, Pietro ^a,b   Podda, Mauro ^b,c   Van De Water, Judy ^a   Ansari, Aftab A ^d   Coppel, Ross L ^e   Worman, Howard J ^f   Gores, Gregory J ^g   Gershwin, M Eric ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MONASH UNIVERSITY   (Australia)

^f New York Presbyterian Columbia University Medical Center   (United States)

^g MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIIDIOTYPIC ANTIBODY; APOPTOSOME; CHOLAGOGUE; CYTOKINE; MITOCHONDRIAL PROTEIN; URSODEOXYCHOLIC ACID;

ADULT; AGED; APOPTOSIS; B LYMPHOCYTE; CASE CONTROL STUDY; CELL CULTURE; DRUG EFFECTS; EPITHELIUM CELL; FEMALE; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; LIVER CIRRHOSIS, BILIARY; MACROPHAGE; METABOLISM; MIDDLE AGED; MITOCHONDRION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RECURRENT DISEASE; T LYMPHOCYTE;

ADULT; AGED; ANTIBODIES, ANTI-IDIOTYPIC; APOPTOSIS; APOPTOSOMES; B-LYMPHOCYTES; CASE-CONTROL STUDIES; CELLS, CULTURED; CHOLAGOGUES AND CHOLERETICS; CYTOKINES; EPITHELIAL CELLS; FEMALE; HUMANS; IMMUNITY, INNATE; LIVER CIRRHOSIS, BILIARY; MACROPHAGES; MIDDLE AGED; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; RECURRENCE; T-LYMPHOCYTES; URSODEOXYCHOLIC ACID;

EID: 77956627699     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.23783     Document Type: Article

References (52)

1. Kaplan MM, Gershwin ME. Primary biliary cirrhosis. N Engl J Med 2005;353:1261-1273.
2. Kawano A, Shimoda S, Kamihira T, Ishikawa F, Niiro H, Soejima Y, et al. Peripheral tolerance and the qualitative characteristics of autoreactive T cell clones in primary biliary cirrhosis. J Immunol 2007;179:3315-3324.
3. Shimoda S, Nakamura M, Ishibashi H, Hayashida K, Niho Y. HLA DRB4 0101-restricted immunodominant T cell autoepitope of pyruvate dehydrogenase complex in primary biliary cirrhosis: evidence of molecular mimicry in human autoimmune diseases. J Exp Med 1995;181:1835-1845.
4. Shimoda S, Miyakawa H, Nakamura M, Ishibashi H, Kikuchi K, Kita H, et al. CD4 T-cell autoreactivity to the mitochondrial autoantigen PDC-E2 in AMA-negative primary biliary cirrhosis. J Autoimmun 2008;31:110-115.
5. Yang GX, Lian ZX, Chuang YH, Moritoki Y, Lan RY, Wakabayashi K, et al. Adoptive transfer of CD8(+) T cells from transforming growth factor beta receptor type II (dominant negative form) induces autoimmune cholangitis in mice. HEPATOLOGY 2008;47:1974-1982.
6. Migliaccio C, Nishio A, Van deWater J, Ansari AA, Leung PS, Nakanuma Y, et al. Monoclonal antibodies to mitochondrial E2 components define autoepitopes in primary biliary cirrhosis. J Immunol 1998;161:5157-5163.
7. Mattalia A, Quaranta S, Leung PS, Bauducci M, Van de Water J, Calvo PL, et al. Characterization of antimitochondrial antibodies in health adults. HEPATOLOGY 1998;27:656-661. (Pubitemid 28103538)
8. Gershwin ME, Mackay IR, Sturgess A, Coppel RL. Identification and specificity of a cDNA encoding the 70 kd mitochondrial antigen recognized in primary biliary cirrhosis. J Immunol 1987;138:3525-3531.
9. Van de Water J, Gershwin ME, Leung P, Ansari A, Coppel RL. The autoepitope of the 74-kD mitochondrial autoantigen of primary biliary cirrhosis corresponds to the functional site of dihydrolipoamide acetyl-transferase. J Exp Med 1988;167:1791-1799.
10. Selmi C, Mayo MJ, Bach N, Ishibashi H, Invernizzi P, Gish RG, et al. Primary biliary cirrhosis in monozygotic and dizygotic twins: genetics, epigenetics, and environment. Gastroenterology 2004;127:485-492.
11. Gershwin ME, Selmi C, Worman HJ, Gold EB, Watnik M, Utts J, et al. Risk factors and comorbidities in primary biliary cirrhosis: a controlled interview-based study of 1032 patients. HEPATOLOGY 2005;42:1194-1202.
12. Wakabayashi K, Lian ZX, Leung PS, Moritoki Y, Tsuneyama K, Kurth MJ, et al. Loss of tolerance in C57BL/6 mice to the autoantigen E2 subunit of pyruvate dehydrogenase by a xenobiotic with ensuing biliary ductular disease. HEPATOLOGY 2008;48:531-540.
13. Savill J, Dransfield I, Gregory C, Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2002;2:965-975. (Pubitemid 37323217)
14. Ravichandran KS, Lorenz U. Engulfment of apoptotic cells: signals for a good meal. Nat Rev Immunol 2007;7:964-974.
15. Nagata S, Hanayama R, Kawane K. Autoimmunity and the clearance of dead cells. Cell 2010;140:619-630.
16. Lleo A, Selmi C, Invernizzi P, Podda M, Coppel RL, Mackay IR, et al. Apotopes and the biliary specificity of primary biliary cirrhosis. HEPATOLOGY 2009;49:871-879.
17. Reed JH, Jackson MW, Gordon TP. A B cell apotope of Ro 60 in systemic lupus erythematosus. Arthritis Rheum 2008;58:1125-1129.
18. Reed JH, Jackson MW, Gordon TP. B cell apotopes of the 60-kDa Ro/SSA and La/SSB autoantigens. J Autoimmun 2008;31:263-267.
19. Van de Water J, Gerson LB, Ferrell LD, Lake JR, Coppel RL, Batts KP, et al. Immunohistochemical evidence of disease recurrence after liver transplantation for primary biliary cirrhosis. HEPATOLOGY 1996;24:1079-1084.
20. Silveira MG, Lindor KD. Treatment of primary biliary cirrhosis: therapy with choleretic and immunosuppressive agents. Clin Liver Dis 2008;12:425-443. (Pubitemid 351626672)
21. Chamulitrat W, Burhenne J, Rehlen T, Pathil A, Stremmel W. Bile salt-phospholipid conjugate ursodeoxycholyl lysophosphatidylethanolamide as a hepatoprotective agent. HEPATOLOGY 2009;50:143-154.
22. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997;40:1725.
23. Chapman RW, Arborgh BA, Rhodes JM, Summerfield JA, Dick R, Scheuer PJ, et al. Primary sclerosing cholangitis: a review of its clinical features, cholangiography, and hepatic histology. Gut 1980;21:870-877.
24. Menke J, Rabacal WA, Byrne KT, Iwata Y, Schwartz MM, Stanley ER, et al. Circulating CSF-1 promotes monocyte and macrophage phenotypes that enhance lupus nephritis. J Am Soc Nephrol 2009;20:2581-2592.
25. Ancuta P, Liu KY, Misra V, Wacleche VS, Gosselin A, Zhou X, et al. Transcriptional profiling reveals developmental relationship and distinct biological functions of CD16+ and CD16- monocyte subsets. BMC Genomics 2009;10:403.
26. Grage-Griebenow E, Flad HD, Ernst M. Heterogeneity of human peripheral blood monocyte subsets. J Leukoc Biol 2001;69:11-20.
27. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005;5:953-964.
28. Schutze S, Tchikov V, Schneider-Brachert W. Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat Rev Mol Cell Biol 2008;9:655-662.
29. Takeda K, Kojima Y, Ikejima K, Harada K, Yamashina S, Okumura K, et al. Death receptor 5 mediated-apoptosis contributes to cholestatic liver disease. Proc Natl Acad Sci U S A 2008;105:10895-10900.
30. Odin JA, Huebert RC, Casciola-Rosen L, LaRusso NF, Rosen A. Bcl-2-dependent oxidation of pyruvate dehydrogenase-E2, a primary biliary cirrhosis autoantigen, during apoptosis. J Clin Invest 2001;108:223-232. (Pubitemid 32656246)
31. Kita H, Lian ZX, Van de Water J, He XS, Matsumura S, Kaplan M, et al. Identification of HLA-A2-restricted CD8(+) cytotoxic T cell responses in primary biliary cirrhosis: T cell activation is augmented by immune complexes cross-presented by dendritic cells. J Exp Med 2002;195:113-123.
32. Leung DY, Bloom JW. Update on glucocorticoid action and resistance. J Allergy Clin Immunol 2003;111:3-22.
33. Clancy RM, Buyon JP, Ikeda K, Nozawa K, Argyle DA, Friedman DM, et al. Maternal antibody responses to the 52-kd SSA/RO p200 peptide and the development of fetal conduction defects. Arthritis Rheum 2005;52:3079-3086.
34. Miranda-Carus ME, Askanase AD, Clancy RM, Di Donato F, Chou TM, Libera MR, et al. Anti-SSA/Ro and anti-SSB/La autoantibodies bind the surface of apoptotic fetal cardiocytes and promote secretion of TNF-alpha by macrophages. J Immunol 2000;165:5345-5351.
35. Karnabi E, Qu Y, Wadgaonkar R, Mancarella S, Yue Y, Chahine M, et al. Congenital heart block: identification of autoantibody binding site on the extracellular loop (domain I, S5-S6) of alpha(1D) L-type Ca channel. J Autoimmun 2010;34:80-86.
36. Neufing PJ, Clancy RM, Jackson MW, Tran HB, Buyon JP, Gordon TP. Exposure and binding of selected immunodominant La/SSB epitopes on human apoptotic cells. Arthritis Rheum 2005;52:3934-3942.
37. Clancy RM, Kapur RP, Molad Y, Askanase AD, Buyon JP. Immunohistologic evidence supports apoptosis, IgG deposition, and novel macrophage/fibroblast crosstalk in the pathologic cascade leading to congenital heart block. Arthritis Rheum 2004;50:173-182.
38. Clancy RM, Neufing PJ, Zheng P, O'Mahony M, Nimmerjahn F, Gordon TP, et al. Impaired clearance of apoptotic cardiocytes is linked to anti-SSA/Ro and -SSB/La antibodies in the pathogenesis of congenital heart block. J Clin Invest 2006;116:2413-2422.
39. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008;8:958-969.
40. Mantovani A, Locati M. Orchestration of macrophage polarization. Blood 2009;114:3135-3136.
41. Mao TK, Lian ZX, Selmi C, Ichiki Y, Ashwood P, Ansari AA, et al. Altered monocyte responses to defined TLR ligands in patients with primary biliary cirrhosis. HEPATOLOGY 2005;42:802-808. (Pubitemid 41401117)
42. Chuang YH, Lian ZX, Tsuneyama K, Chiang BL, Ansari AA, Coppel RL, et al. Increased killing activity and decreased cytokine production in NK cells in patients with primary biliary cirrhosis. J Autoimmun 2006;26:232-240. (Pubitemid 44177425)
43. Dardalhon V, Korn T, Kuchroo VK, Anderson AC. Role of Th1 and Th17 cells in organ-specific autoimmunity. J Autoimmun 2008;31:252-256.
44. Nagano T, Yamamoto K, Matsumoto S, Okamoto R, Tagashira M, Ibuki N, et al. Cytokine profile in the liver of primary biliary cirrhosis. J Clin Immunol 1999;19:422-427.
45. Oertelt S, Rieger R, Selmi C, Invernizzi P, Ansari AA, Coppel RL, et al. A sensitive bead assay for antimitochondrial antibodies: chipping away at AMA-negative primary biliary cirrhosis. HEPATOLOGY 2007;45:659-665.
46. Hirschfield GM, Liu X, Xu C, Lu Y, Xie G, Gu X, et al. Primary biliary cirrhosis associated with HLA, IL12A, and IL12RB2 variants. N Engl J Med 2009;360:2544-2555.
47. Yoshida K, Yang GX, Zhang W, Tsuda M, Tsuneyama K, Moritoki Y, et al. Deletion of interleukin-12p40 suppresses autoimmune cholangitis in dominant negative transforming growth factor beta receptor type II mice. HEPATOLOGY 2009;50:1494-1500.
48. Boruchov AM, Heller G, Veri MC, Bonvini E, Ravetch JV, Young JW. Activating and inhibitory IgG Fc receptors on human DCs mediate opposing functions. J Clin Invest 2005;115:2914-2923.
49. Tamir I, Stolpa JC, Helgason CD, Nakamura K, Bruhns P, Daeron M, et al. The RasGAP-binding protein p62dok is a mediator of inhibitory FcgammaRIIB signals in B cells. Immunity 2000;12:347-358.
50. Takai T. Roles of Fc receptors in autoimmunity. Nat Rev Immunol 2002;2:580-592.
51. Frisoni L, McPhie L, Colonna L, Sriram U, Monestier M, Gallucci S, et al. Nuclear autoantigen translocation and autoantibody opsonization lead to increased dendritic cell phagocytosis and presentation of nuclear antigens: a novel pathogenic pathway for autoimmunity? J Immunol 2005;175:2692-2701.
52. Higuchi H, Grambihler A, Canbay A, Bronk SF, Gores GJ. Bile acids up-regulate death receptor 5/TRAIL-receptor 2 expression via a c-Jun N-terminal kinase-dependent pathway involving Sp 1. J Biol Chem 2004;279:51-60. (Pubitemid 38044798)