The Immunogenetics of Autoimmune Cholestasis

Clinics in Liver Disease

Volumn 20, Issue 1, 2016, Pages 15-31

  Trivedi, Palak J ^a   Hirschfield, Gideon M ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Autoimmune liver disease; Autoimmunity; Mucosal immunity; Primary biliary cirrhosis; Primary sclerosing cholangitis

Indexed keywords

HLA ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR;

AUTOIMMUNE CHOLESTASIS; CHOLESTASIS; CYTOKINE RESPONSE; DISEASE ACTIVITY; DISEASE ASSOCIATION; EPIGENETICS; GENETIC ASSOCIATION; HUMAN; IMMUNE RESPONSE; IMMUNOGENETICS; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; PROTEIN DETERMINATION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; AUTOIMMUNE DISEASE; BILIARY CIRRHOSIS; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; SCLEROSING CHOLANGITIS;

AUTOIMMUNE DISEASES; CHOLANGITIS, SCLEROSING; EPIGENESIS, GENETIC; HLA ANTIGENS; HUMANS; IMMUNOGENETICS; INTESTINAL MUCOSA; LIVER CIRRHOSIS, BILIARY; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84947703326     PISSN: 10893261     EISSN: 15578224     Source Type: Journal    
DOI: 10.1016/j.cld.2015.08.002     Document Type: Review

References (106)

1. Hirschfield G.M., Chapman R.W., Karlsen T.H., et al. The genetics of complex cholestatic disorders. Gastroenterology 2013, 144(7):1357-1374.
2. Trivedi P.J., Hirschfield G.M. Review article: overlap syndromes and autoimmune liver disease. Aliment Pharmacol Ther 2012, 36(6):517-533.
3. Karlsen T.H., Kaser A. Deciphering the genetic predisposition to primary sclerosing cholangitis. Semin Liver Dis 2011, 31(2):188-207.
4. Folseraas T., Liaskou E., Anderson C.A., et al. Genetics in PSC: what do the "risk genes" teach us?. Clin Rev Allergy Immunol 2014, 48(2-3):154-164.
5. Boonstra K., Beuers U., Ponsioen C.Y. Epidemiology of primary sclerosing cholangitis and primary biliary cirrhosis: a systematic review. J Hepatol 2012, 56(5):1181-1188.
6. Charman S, Copley L, Tovikkai C, et al. UK Liver Transplant Audit (NHS Blood and Transplant). 2012. Available at: . Accessed July 21, 2015. https://www.rcseng.ac.uk/surgeons/research/surgical-research/docs/liver-transplant-audit-report-2012.
7. Arbour L., Rupps R., Field L., et al. Characteristics of primary biliary cirrhosis in British Columbia's First Nations population. Can J Gastroenterol 2005, 19(5):305-310.
8. Selmi C., Mayo M.J., Bach N., et al. Primary biliary cirrhosis in monozygotic and dizygotic twins: genetics, epigenetics, and environment. Gastroenterology 2004, 127(2):485-492.
9. Corpechot C., Chrétien Y., Chazouillères O., et al. Demographic, lifestyle, medical and familial factors associated with primary biliary cirrhosis. J Hepatol 2010, 53(1):162-169.
10. Sood S., Gow P.J., Christie J.M., et al. Epidemiology of primary biliary cirrhosis in Victoria, Australia: high prevalence in migrant populations. Gastroenterology 2004, 127(2):470-475.
11. Watson R.G., Angus P.W., Dewar M., et al. Low prevalence of primary biliary cirrhosis in Victoria, Australia. Melbourne Liver Group. Gut 1995, 36(6):927-930.
12. Trivedi P.J., Cullen S. Etiopathogenesis of primary biliary cirrhosis: an overview of recent developments. Hepatol Int 2013, 7(1):28-47.
13. Bergquist A., Lindberg G., Saarinen S., et al. Increased prevalence of primary sclerosing cholangitis among first-degree relatives. J Hepatol 2005, 42(2):252-256.
14. Trivedi P.J., Chapman R.W. PSC, AIH and overlap syndrome in inflammatory bowel disease. Clin Res Hepatol Gastroenterol 2012, 36(5):420-436.
15. Bergquist A., Montgomery S.M., Bahmanyar S., et al. Increased risk of primary sclerosing cholangitis and ulcerative colitis in first-degree relatives of patients with primary sclerosing cholangitis. Clin Gastroenterol Hepatol 2008, 6(8):939-943.
16. De Boer Y.S., van Gerven N.M.F., Zwiers A., et al. Genome-wide association study identifies variants associated with autoimmune hepatitis type 1. Gastroenterology 2014, 147(2):443-452.e5.
17. Hirschfield G.M., Liu X., Xu C., et al. Primary biliary cirrhosis associated with HLA, IL12A, and IL12RB2 variants. N Engl J Med 2009, 360(24):2544-2555.
18. Mells G.F., Floyd J.A.B., Morley K.I., et al. Genome-wide association study identifies 12 new susceptibility loci for primary biliary cirrhosis. Nat Genet 2011, 43(4):329-332.
19. Liu X., Invernizzi P., Lu Y., et al. Genome-wide meta-analyses identify three loci associated with primary biliary cirrhosis. Nat Genet 2010, 42(8):658-660.
20. Nakamura M., Nishida N., Kawashima M., et al. Genome-wide association study identifies TNFSF15 and POU2AF1 as susceptibility loci for primary biliary cirrhosis in the Japanese population. Am J Hum Genet 2012, 91(4):721-728.
21. Invernizzi P. Human leukocyte antigen in primary biliary cirrhosis: an old story now reviving. Hepatology 2011, 54(2):714-723.
22. Umemura T., Zen Y., Hamano H., et al. Immunoglobin G4-hepatopathy: association of immunoglobin G4-bearing plasma cells in liver with autoimmune pancreatitis. Hepatology 2007, 46(2):463-471.
23. Lleo A., Bowlus C.L., Yang G.-X., et al. Biliary apotopes and anti-mitochondrial antibodies activate innate immune responses in primary biliary cirrhosis. Hepatology 2010, 52(3):987-998.
24. Lleo A., Selmi C., Invernizzi P., et al. Apotopes and the biliary specificity of primary biliary cirrhosis. Hepatology 2009, 49(3):871-879.
25. Shimoda S., Van de Water J., Ansari A., et al. Identification and precursor frequency analysis of a common T cell epitope motif in mitochondrial autoantigens in primary biliary cirrhosis. J Clin Invest 1998, 102(10):1831-1840.
26. Liu J.Z., Hov J.R., Folseraas T., et al. Dense genotyping of immune-related disease regions identifies nine new risk loci for primary sclerosing cholangitis. Nat Genet 2013, 45(6):670-675.
27. Karlsen T.H., Franke A., Melum E., et al. Genome-wide association analysis in primary sclerosing cholangitis. Gastroenterology 2010, 138(3):1102-1111.
28. Naess S., Björnsson E., Anmarkrud J.A., et al. Small duct primary sclerosing cholangitis without inflammatory bowel disease is genetically different from large duct disease. Liver Int 2014, 34(10):1488-1495.
29. Melum E., Franke A., Schramm C., et al. Genome-wide association analysis in primary sclerosing cholangitis identifies two non-HLA susceptibility loci. Nat Genet 2011, 43(1):17-19.
30. Okada Y., Yamazaki K., Umeno J., et al. HLA-Cw*1202-B*5201-DRB1*1502 haplotype increases risk for ulcerative colitis but reduces risk for Crohn's disease. Gastroenterology 2011, 141(3):864-871.e1-5.
31. Rudolph G., Gotthardt D., Kloeters-Plachky P., et al. PSC with dominant bile duct stenosis, IBD is associated with an increase of carcinomas and reduced survival. J Hepatol 2010, 53(2):313-317.
32. Boonstra K., Weersma R.K., van Erpecum K.J., et al. Population-based epidemiology, malignancy risk, and outcome of primary sclerosing cholangitis. Hepatology 2013, 58(6):2045-2055.
33. Mendes F.D., Jorgensen R., Keach J., et al. Elevated serum IgG4 concentration in patients with primary sclerosing cholangitis. Am J Gastroenterol 2006, 101(9):2070-2075.
34. Trivedi P.J., Corpechot C., Pares A., et al. Risk stratification in autoimmune cholestatic liver diseases: Opportunities for clinicians and trialists. Hepatology 2015, [Epub ahead of print].
35. Berntsen N.L., Klingenberg O., Juran B.D., et al. Association between HLA haplotypes and increased serum levels of IgG4 in patients with primary sclerosing cholangitis. Gastroenterology 2015, 148(5):924-927.e2.
36. Katt J., Schwinge D., Schoknecht T., et al. Increased Th17 response to pathogen stimulation in patients with primary sclerosing cholangitis. Hepatology 2013, 58(3):1084-1093.
37. Yang C.-Y., Ma X., Tsuneyama K., et al. IL-12/Th1 and IL-23/Th17 biliary microenvironment in primary biliary cirrhosis: implications for therapy. Hepatology 2014, 59(5):1944-1953.
38. Hudspeth K., Pontarini E., Tentorio P., et al. The role of natural killer cells in autoimmune liver disease: a comprehensive review. J Autoimmun 2013, 46:55-65.
39. Sebode M., Peiseler M., Franke B., et al. Reduced FOXP3(+) regulatory T cells in patients with primary sclerosing cholangitis are associated with IL2RA gene polymorphisms. J Hepatol 2014, 60(5):1010-1016.
40. Rong G., Zhou Y., Xiong Y., et al. Imbalance between T helper type 17 and T regulatory cells in patients with primary biliary cirrhosis: the serum cytokine profile and peripheral cell population. Clin Exp Immunol 2009, 156(2):217-225.
41. Yao Y., Yang W., Yang Y.-Q., et al. Distinct from its canonical effects, deletion of IL-12p40 induces cholangitis and fibrosis in interleukin-2Rα(-/-) mice. J Autoimmun 2014, 51:99-108.
42. Korn T., Bettelli E., Oukka M., et al. IL-17 and Th17 cells. Annu Rev Immunol 2009, 27:485-517.
43. Filipe-Santos O., Bustamante J., Chapgier A., et al. Inborn errors of IL-12/23- and IFN-gamma-mediated immunity: molecular, cellular, and clinical features. Semin Immunol 2006, 18(6):347-361.
44. Barrett J.C., Clayton D.G., Concannon P., et al. Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat Genet 2009, 41(6):703-707.
45. Barrett J.C., Hansoul S., Nicolae D.L., et al. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet 2008, 40(8):955-962.
46. Cordell H.J., Han Y., Mells G.F., et al. International genome-wide meta-analysis identifies new primary biliary cirrhosis risk loci and targetable pathogenic pathways. Nat Commun 2015, in press.
47. Yoshida K., Yang G.-X., Zhang W., et al. Deletion of interleukin-12p40 suppresses autoimmune cholangitis in dominant negative transforming growth factor beta receptor type II mice. Hepatology 2009, 50(5):1494-1500.
48. Carbone M., Mells G.F., Alexander G.J., et al. Calcineurin inhibitors and the IL12A locus influence risk of recurrent primary biliary cirrhosis after liver transplantation. Am J Transplant 2013, 13(4):1110-1111.
49. Juran B.D., Atkinson E.J., Larson J.J., et al. Carriage of a tumor necrosis factor polymorphism amplifies the cytotoxic T-lymphocyte antigen 4 attributed risk of primary biliary cirrhosis: evidence for a gene-gene interaction. Hepatology 2010, 52(1):223-229.
50. Liaskou E., Jeffery L.E., Trivedi P.J., et al. Loss of CD28 expression by liver-infiltrating T cells contributes to pathogenesis of primary sclerosing cholangitis. Gastroenterology 2014, 147(1):221-232.e7.
51. Tacke F., Luedde T., Trautwein C. Inflammatory pathways in liver homeostasis and liver injury. Clin Rev Allergy Immunol 2009, 36(1):4-12.
52. Kar S.P., Seldin M.F., Chen W., et al. Pathway-based analysis of primary biliary cirrhosis genome-wide association studies. Genes Immun 2013, 14(3):179-186.
53. Neuman M., Angulo P., Malkiewicz I., et al. Tumor necrosis factor-alpha and transforming growth factor-beta reflect severity of liver damage in primary biliary cirrhosis. J Gastroenterol Hepatol 2002, 17(2):196-202.
54. Liaskou E., Karikoski M., Reynolds G.M., et al. Regulation of mucosal addressin cell adhesion molecule 1 expression in human and mice by vascular adhesion protein 1 amine oxidase activity. Hepatology 2011, 53(2):661-672.
55. Steinberg M.W., Shui J.-W., Ware C.F., et al. Regulating the mucosal immune system: the contrasting roles of LIGHT, HVEM, and their various partners. Semin Immunopathol 2009, 31(2):207-221.
56. Atarashi K., Nishimura J., Shima T., et al. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008, 455(7214):808-812.
57. Puel A., Döffinger R., Natividad A., et al. Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J Exp Med 2010, 207(2):291-297.
58. Esplugues E., Huber S., Gagliani N., et al. Control of TH17 cells occurs in the small intestine. Nature 2011, 475(7357):514-518.
59. Trivedi P.J., Adams D.H. Mucosal immunity in liver autoimmunity: a comprehensive review. J Autoimmun 2013, 46:97-111.
60. Marchesi F., Martin A.P., Thirunarayanan N., et al. CXCL13 expression in the gut promotes accumulation of IL-22-producing lymphoid tissue-inducer cells, and formation of isolated lymphoid follicles. Mucosal Immunol 2009, 2(6):486-494.
61. Wang L., Sun Y., Zhang Z., et al. CXCR5+ CD4+ T follicular helper cells participate in the pathogenesis of primary biliary cirrhosis. Hepatology 2015, 61(2):627-638.
62. Zhang W., Sharma R., Ju S.-T., et al. Deficiency in regulatory T cells results in development of antimitochondrial antibodies and autoimmune cholangitis. Hepatology 2009, 49(2):545-552.
63. Oertelt S., Lian Z.-X., Cheng C.-M., et al. Anti-mitochondrial antibodies and primary biliary cirrhosis in TGF-beta receptor II dominant-negative mice. J Immunol 2006, 177(3):1655-1660.
64. Cimbro R., Vassena L., Arthos J., et al. IL-7 induces expression and activation of integrin α4β7 promoting naive T-cell homing to the intestinal mucosa. Blood 2012, 120(13):2610-2619.
65. Tsuda M., Ambrosini Y.M., Zhang W., et al. Fine phenotypic and functional characterization of effector cluster of differentiation 8 positive T cells in human patients with primary biliary cirrhosis. Hepatology 2011, 54(4):1293-1302.
66. Wakabayashi K., Lian Z.-X., Moritoki Y., et al. IL-2 receptor alpha(-/-) mice and the development of primary biliary cirrhosis. Hepatology 2006, 44(5):1240-1249.
67. Bo X., Broome U., Remberger M., et al. Tumour necrosis factor alpha impairs function of liver derived T lymphocytes and natural killer cells in patients with primary sclerosing cholangitis. Gut 2001, 49(1):131-141.
68. Moran C.J., Walters T.D., Guo C.-H., et al. IL-10R polymorphisms are associated with very-early-onset ulcerative colitis. Inflamm Bowel Dis 2013, 19(1):115-123.
69. Devkota S., Wang Y., Musch M.W., et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 2012, 487(7405):104-108.
70. Reizis B. Regulation of plasmacytoid dendritic cell development. Curr Opin Immunol 2010, 22(2):206-211.
71. Hara H., Saito T. CARD9 versus CARMA1 in innate and adaptive immunity. Trends Immunol 2009, 30(5):234-242.
72. Sokol H., Conway K.L., Zhang M., et al. Card9 mediates intestinal epithelial cell restitution, T-helper 17 responses, and control of bacterial infection in mice. Gastroenterology 2013, 145(3):591-601.e3.
73. Raab M., Wang H., Lu Y., et al. T cell receptor "inside-out" pathway via signaling module SKAP1-RapL regulates T cell motility and interactions in lymph nodes. Immunity 2010, 32(4):541-556.
74. Katagiri K., Katakai T., Ebisuno Y., et al. Mst1 controls lymphocyte trafficking and interstitial motility within lymph nodes. EMBO J 2009, 28(9):1319-1331.
75. Häuser F., Deyle C., Berard D., et al. Macrophage-stimulating protein polymorphism rs3197999 is associated with a gain of function: implications for inflammatory bowel disease. Genes Immun 2012, 13(4):321-327.
76. Lee D.-H., Esworthy R.S., Chu C., et al. Mutation accumulation in the intestine and colon of mice deficient in two intracellular glutathione peroxidases. Cancer Res 2006, 66(20):9845-9851.
77. Folseraas T., Melum E., Rausch P., et al. Extended analysis of a genome-wide association study in primary sclerosing cholangitis detects multiple novel risk loci. J Hepatol 2012, 57(2):366-375.
78. Rausch P., Rehman A., Künzel S., et al. Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (secretor) genotype. Proc Natl Acad Sci U S A 2011, 108(47):19030-19035.
79. Rupp C., Friedrich K., Folseraas T., et al. Fut2 genotype is a risk factor for dominant stenosis and biliary candida infections in primary sclerosing cholangitis. Aliment Pharmacol Ther 2014, 39(8):873-882.
80. Gaj P., Maryan N., Hennig E.E., et al. Pooled sample-based GWAS: a cost-effective alternative for identifying colorectal and prostate cancer risk variants in the polish population. PLoS One 2012, 7(4):e35307.
81. Nakagawa H., Hikiba Y., Hirata Y., et al. Loss of liver E-cadherin induces sclerosing cholangitis and promotes carcinogenesis. Proc Natl Acad Sci U S A 2014, 111(3):1090-1095.
82. Invernizzi P., Miozzo M., Battezzati P.M., et al. Frequency of monosomy X in women with primary biliary cirrhosis. Lancet 2004, 363(9408):533-535.
83. Miozzo M., Selmi C., Gentilin B., et al. Preferential X chromosome loss but random inactivation characterize primary biliary cirrhosis. Hepatology 2007, 46(2):456-462.
84. Lleo A., Oertelt-Prigione S., Bianchi I., et al. Y chromosome loss in male patients with primary biliary cirrhosis. J Autoimmun 2013, 41:87-91.
85. Lleo A., Zhang W., Zhao M., et al. DNA methylation profiling of the X chromosome reveals an aberrant demethylation on CXCR3 promoter in primary biliary cirrhosis. Clin Epigenetics 2015, 7(1):61.
86. Chuang Y.-H., Lian Z.-X., Cheng C.-M., et al. Increased levels of chemokine receptor CXCR3 and chemokines IP-10 and MIG in patients with primary biliary cirrhosis and their first degree relatives. J Autoimmun 2005, 25(2):126-132.
87. Lleo A., Liao J., Invernizzi P., et al. Immunoglobulin M levels inversely correlate with CD40 ligand promoter methylation in patients with primary biliary cirrhosis. Hepatology 2012, 55(1):153-160.
88. Goules A., Tzioufas A.G., Manousakis M.N., et al. Elevated levels of soluble CD40 ligand (sCD40L) in serum of patients with systemic autoimmune diseases. J Autoimmun 2006, 26(3):165-171.
89. Kawamura T., Kanai T., Dohi T., et al. Ectopic CD40 ligand expression on B cells triggers intestinal inflammation. J Immunol 2004, 172(10):6388-6397.
90. Armstrong M.J., Hegade V.S., Robins G. Advances in coeliac disease. Curr Opin Gastroenterol 2012, 28(2):104-112.
91. Lee J.C., Lyons P.A., McKinney E.F., et al. Gene expression profiling of CD8+ T cells predicts prognosis in patients with Crohn disease and ulcerative colitis. J Clin Invest 2011, 121(10):4170-4179.
92. Hirschfield G.M., Siminovitch K.A. Genetics in PBC: what do the "risk genes" teach us?. Clin Rev Allergy Immunol 2014, 48(2-3):176-181.
93. Teng M.W.L., Bowman E.P., McElwee J.J., et al. IL-12 and IL-23 cytokines: from discovery to targeted therapies for immune-mediated inflammatory diseases. Nat Med 2015, 21(7):719-729.
94. Zhang H., Bernuzzi F., Lleo A., et al. Therapeutic potential of IL-17-mediated signaling pathway in autoimmune liver diseases. Mediators Inflamm 2015, 2015:436450.
95. Heninger A.-K., Wentrup S., Al-Saeedi M., et al. Immunomodulation of human intestinal T cells by the synthetic CD80 antagonist RhuDex®. Immun Inflamm Dis 2014, 2(3):166-180.
96. Lobatón T., Vermeire S., Van Assche G., et al. Review article: anti-adhesion therapies for inflammatory bowel disease. Aliment Pharmacol Ther 2014, 39(6):579-594.
97. Hart B.A., Hintzen R.Q., Laman J.D. Preclinical assessment of therapeutic antibodies against human CD40 and human interleukin-12/23p40 in a nonhuman primate model of multiple sclerosis. Neurodegener Dis 2008, 5(1):38-52.
98. Hassan S.B., Sørensen J.F., Olsen B.N., et al. Anti-CD40-mediated cancer immunotherapy: an update of recent and ongoing clinical trials. Immunopharmacol Immunotoxicol 2014, 36(2):96-104.
99. Yellin M., Paliienko I., Balanescu A., et al. A phase II, randomized, double-blind, placebo-controlled study evaluating the efficacy and safety of MDX-1100, a fully human anti-CXCL10 monoclonal antibody, in combination with methotrexate in patients with rheumatoid arthritis. Arthritis Rheum 2012, 64(6):1730-1739.
100. Klimatcheva E., Pandina T., Reilly C., et al. CXCL13 antibody for the treatment of autoimmune disorders. BMC Immunol 2015, 16:6.
101. Ha S.G., Ge X.N., Bahaie N.S., et al. ORMDL3 promotes eosinophil trafficking and activation via regulation of integrins and CD48. Nat Commun 2013, 4:2479.
102. Berce V., Kozmus C.E.P., Potočnik U. Association among ORMDL3 gene expression, 17q21 polymorphism and response to treatment with inhaled corticosteroids in children with asthma. Pharmacogenomics J 2013, 13(6):523-529.
103. Fallarini S., Magliulo L., Paoletti T., et al. Expression of functional GPR35 in human iNKT cells. Biochem Biophys Res Commun 2010, 398(3):420-425.
104. Imielinski M., Baldassano R.N., Griffiths A., et al. Common variants at five new loci associated with early-onset inflammatory bowel disease. Nat Genet 2009, 41(12):1335-1340.
105. Jenkins L., Harries N., Lappin J.E., et al. Antagonists of GPR35 display high species ortholog selectivity and varying modes of action. J Pharmacol Exp Ther 2012, 343(3):683-695.
106. Harikumar K.B., Kunnumakkara A.B., Ochi N., et al. A novel small-molecule inhibitor of protein kinase D blocks pancreatic cancer growth in vitro and in vivo. Mol Cancer Ther 2010, 9(5):1136-1146.