Distinct from its canonical effects, deletion of IL-12p40 induces cholangitis and fibrosis in interleukin-2Rα-/- mice

Journal of Autoimmunity

Volumn 51, Issue , 2014, Pages 99-108

  Yao, Yuan ^a   Yang, Wei ^a   Yang, Yan Qing ^a   Ma, Hong Di ^a   Lu, Fang Ting ^a   Li, Liang ^a   Tao, Yan Yan ^b   Tsuneyama, Koichi ^c   Zhang, Weici ^d   Friedman, Scott ^e   Gershwin, M Eric ^d   Lian, Zhe Xiong ^a,f  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^c UNIVERSITY OF TOYAMA   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MOUNT SINAI MEDICAL CENTER   (United States)

^f UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

Effector memory cells; Fibrosis; IFN ; IL 12p40; Primary biliary cirrhosis

Indexed keywords

INTERLEUKIN 12P40; INTERLEUKIN 2 RECEPTOR ALPHA; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; BILE DUCT INJURY; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL POPULATION; CHOLANGITIS; COLITIS; CONTROLLED STUDY; DISEASE SEVERITY; FLOW CYTOMETRY; HISTOPATHOLOGY; IMMUNOBIOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOLOGY; INFLAMMATORY CELL; LIVER FIBROSIS; MEMORY CELL; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PHENOTYPE; PORTAL HYPERTENSION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN; TH1 CELL; TH17 CELL; ANIMAL; DISEASE MODEL; FIBROSIS; GENE DELETION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LIVER CIRRHOSIS; METABOLISM; PATHOLOGY; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; AUTOIMMUNE DISEASES; CHOLANGITIS; COLITIS; CYTOKINES; DISEASE MODELS, ANIMAL; FIBROSIS; GENE DELETION; INTERLEUKIN-12 SUBUNIT P40; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LIVER CIRRHOSIS; MICE; MICE, KNOCKOUT; SPLEEN; T-LYMPHOCYTE SUBSETS;

EID: 84901271022     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2014.02.009     Document Type: Article

References (68)

1. Hirschfield G.M., Gershwin M.E. The immunobiology and pathophysiology of primary biliary cirrhosis. Annu Rev Pathol 2013, 8:303-330.
2. Gershwin M.E., Mackay I.R., Sturgess A., Coppel R.L. Identification and specificity of a cDNA encoding the 70 kd mitochondrial antigen recognized in primary biliary cirrhosis. JImmunol 1987, 138:3525-3531.
3. Kaplan M.M., Gershwin M.E. Primary biliary cirrhosis. NEngl J Med 2005, 353:1261-1273.
4. Wakabayashi K., Lian Z.X., Moritoki Y., Lan R.Y., Tsuneyama K., Chuang Y.H., et al. IL-2 receptor alpha(-/-) mice and the development of primary biliary cirrhosis. Hepatology 2006, 44:1240-1249.
5. Hsu W., Zhang W., Tsuneyama K., Moritoki Y., Ridgway W.M., Ansari A.A., et al. Differential mechanisms in the pathogenesis of autoimmune cholangitis versus inflammatory bowel disease in interleukin-2Ralpha(-/-) mice. Hepatology 2009, 49:133-140.
6. Lan R.Y., Salunga T.L., Tsuneyama K., Lian Z.X., Yang G.X., Hsu W., et al. Hepatic IL-17 responses in human and murine primary biliary cirrhosis. JAutoimmun 2009, 32:43-51.
7. Hirschfield G.M., Liu X., Xu C., Lu Y., Xie G., Lu Y., et al. Primary biliary cirrhosis associated with HLA, IL12A, and IL12RB2 variants. NEngl J Med 2009, 360:2544-2555.
8. Liu X., Invernizzi P., Lu Y., Kosoy R., Lu Y., Bianchi I., et al. Genome-wide meta-analyses identify three loci associated with primary biliary cirrhosis. Nat Genet 2010, 42:658-660.
9. Vignali D.A., Kuchroo V.K. IL-12 family cytokines: immunological playmakers. Nat Immunol 2012, 13:722-728.
10. Zhu J., Yamane H., Paul W.E. Differentiation of effector CD4 T cell populations (*). Annu Rev Immunol 2010, 28:445-489.
11. Gran B., Zhang G.X., Yu S., Li J., Chen X.H., Ventura E.S., et al. IL-12p35-deficient mice are susceptible to experimental autoimmune encephalomyelitis: evidence for redundancy in the IL-12 system in the induction of central nervous system autoimmune demyelination. JImmunol 2002, 169:7104-7110.
12. Murphy C.A., Langrish C.L., Chen Y., Blumenschein W., McClanahan T., Kastelein R.A., et al. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. JExp Med 2003, 198:1951-1957.
13. Tarrant T.K., Silver P.B., Chan C.C., Wiggert B., Caspi R.R. Endogenous IL-12 is required for induction and expression of experimental autoimmune uveitis. JImmunol 1998, 161:122-127.
14. Kikawada E., Lenda D.M., Kelley V.R. IL-12 deficiency in MRL-Fas(lpr) mice delays nephritis and intrarenal IFN-gamma expression, and diminishes systemic pathology. JImmunol 2003, 170:3915-3925.
15. Eriksson U., Kurrer M.O., Sebald W., Brombacher F., Kopf M. Dual role of the IL-12/IFN-gamma axis in the development of autoimmune myocarditis: induction by IL-12 and protection by IFN-gamma. JImmunol 2001, 167:5464-5469.
16. Tsuda M., Zhang W., Yang G.X., Tsuneyama K., Ando Y., Kawata K., et al. Deletion of interleukin (IL)-12p35 induces liver fibrosis in dominant-negative TGFbeta receptor type II mice. Hepatology 2013, 57:806-816.
17. Yoshida K., Yang G.X., 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.
18. Ando Y., Yang G.X., Tsuda M., Kawata K., Zhang W., Nakajima T., et al. The immunobiology of colitis and cholangitis in interleukin-23p19 and interleukin-17A deleted dominant negative form of transforming growth factor beta receptor type II mice. Hepatology 2012, 56:1418-1426.
19. Kumada T., Tsuneyama K., Hatta H., Ishizawa S., Takano Y. Improved 1-h rapid immunostaining method using intermittent microwave irradiation: practicability based on 5 years application in Toyama Medical and Pharmaceutical University Hospital. Mod Pathol 2004, 17:1141-1149.
20. Jamall I.S., Finelli V.N., Que Hee S.S. Asimple method to determine nanogram levels of 4-hydroxyproline in biological tissues. Anal Biochem 1981, 112:70-75.
21. Zhou R., Wei H., Sun R., Tian Z. Recognition of double-stranded RNA by TLR3 induces severe small intestinal injury in mice. JImmunol 2007, 178:4548-4556.
22. Kullberg M.C., Jankovic D., Feng C.G., Hue S., Gorelick P.L., McKenzie B.S., et al. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. JExp Med 2006, 203:2485-2494.
23. Kobayashi M., Kweon M.N., Kuwata H., Schreiber R.D., Kiyono H., Takeda K., et al. Toll-like receptor-dependent production of IL-12p40 causes chronic enterocolitis in myeloid cell-specific Stat3-deficient mice. JClin Invest 2003, 111:1297-1308.
24. Hue S., Ahern P., Buonocore S., Kullberg M.C., Cua D.J., McKenzie B.S., et al. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. JExp Med 2006, 203:2473-2483.
25. Magram J., Connaughton S.E., Warrier R.R., Carvajal D.M., Wu C.Y., Ferrante J., et al. IL-12-deficient mice are defective in IFN gamma production and type 1 cytokine responses. Immunity 1996, 4:471-481.
26. Nicoletti F., Di Marco R., Zaccone P., Salvaggio A., Magro G., Bendtzen K., et al. Murine concanavalin A-induced hepatitis is prevented by interleukin 12 (IL-12) antibody and exacerbated by exogenous IL-12 through an interferon-gamma-dependent mechanism. Hepatology 2000, 32:728-733.
27. Oxenius A., Karrer U., Zinkernagel R.M., Hengartner H. IL-12 is not required for induction of type 1 cytokine responses in viral infections. JImmunol 1999, 162:965-973.
28. Xing Z., Zganiacz A., Wang J., Divangahi M., Nawaz F. IL-12-independent Th1-type immune responses to respiratory viral infection: requirement of IL-18 for IFN-gamma release in the lung but not for the differentiation of viral-reactive Th1-type lymphocytes. JImmunol 2000, 164:2575-2584.
29. Skokos D., Nussenzweig M.C. CD8- DCs induce IL-12-independent Th1 differentiation through delta 4 notch-like ligand in response to bacterial LPS. JExp Med 2007, 204:1525-1531.
30. Soares H., Waechter H., Glaichenhaus N., Mougneau E., Yagita H., Mizenina O., et al. Asubset of dendritic cells induces CD4+ T cells to produce IFN-gamma by an IL-12-independent but CD70-dependent mechanism invivo. JExp Med 2007, 204:1095-1106.
31. Smeltz R.B., Chen J., Shevach E.M. Transforming growth factor-beta1 enhances the interferon-gamma-dependent, interleukin-12-independent pathway of T helper 1 cell differentiation. Immunology 2005, 114:484-492.
32. Ramos H.J., Davis A.M., Cole A.G., Schatzle J.D., Forman J., Farrar J.D. Reciprocal responsiveness to interleukin-12 and interferon-alpha specifies human CD8+ effector versus central memory T-cell fates. Blood 2009, 113:5516-5525.
33. Wilson D.C., Grotenbreg G.M., Liu K., Zhao Y., Frickel E.M., Gubbels M.J., et al. Differential regulation of effector- and central-memory responses to toxoplasma gondii infection by IL-12 revealed by tracking of Tgd057-specific CD8+ T cells. PLoS Pathog 2010, 6:e1000815.
34. Cooper A.M., Khader S.A. IL-12p40: an inherently agonistic cytokine. Trends Immunol 2007, 28:33-38.
35. Yoshimoto T., Wang C.R., Yoneto T., Waki S., Sunaga S., Komagata Y., et al. Reduced T helper 1 responses in IL-12 p40 transgenic mice. JImmunol 1998, 160:588-594.
36. Heinzel F.P., Hujer A.M., Ahmed F.N., Rerko R.M. Invivo production and function of IL-12 p40 homodimers. JImmunol 1997, 158:4381-4388.
37. Brahmachari S., Pahan K. Suppression of regulatory T cells by IL-12p40 homodimer via nitric oxide. JImmunol 2009, 183:2045-2058.
38. Khader S.A., Partida-Sanchez S., Bell G., Jelley-Gibbs D.M., Swain S., Pearl J.E., et al. Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. JExp Med 2006, 203:1805-1815.
39. Huaux F., Arras M., Tomasi D., Barbarin V., Delos M., Coutelier J.P., et al. Aprofibrotic function of IL-12p40 in experimental pulmonary fibrosis. JImmunol 2002, 169:2653-2661.
40. Camoglio L., Juffermans N.P., Peppelenbosch M., Te Velde A.A., Ten Kate F.J., van Deventer S.J., et al. Contrasting roles of IL-12p40 and IL-12p35 in the development of hapten-induced colitis. Eur J Immunol 2002, 32:261-269.
41. Wang R.X., Yu C.R., Mahdi R.M., Egwuagu C.E. Novel IL27p28/IL12p40 cytokine suppressed experimental autoimmune uveitis by inhibiting autoreactive Th1/Th17 cells and promoting expansion of regulatory T cells. JBiol Chem 2012, 287:36012-36021.
42. Stritesky G.L., Yeh N., Kaplan M.H. IL-23 promotes maintenance but not commitment to the Th17 lineage. JImmunol 2008, 181:5948-5955.
43. O'Connor W., Kamanaka M., Booth C.J., Town T., Nakae S., Iwakura Y., et al. Aprotective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol 2009, 10:603-609.
44. Veldhoen M., Hocking R.J., Flavell R.A., Stockinger B. Signals mediated by transforming growth factor-beta initiate autoimmune encephalomyelitis, but chronic inflammation is needed to sustain disease. Nat Immunol 2006, 7:1151-1156.
45. Luthje K., Kallies A., Shimohakamada Y., Belz G.T., Light A., Tarlinton D.M., et al. The development and fate of follicular helper T cells defined by an IL-21 reporter mouse. Nat Immunol 2012, 13:491-498.
46. Ballesteros-Tato A., Leon B., Graf B.A., Moquin A., Adams P.S., Lund F.E., et al. Interleukin-2 inhibits germinal center formation by limiting T follicular helper cell differentiation. Immunity 2012, 36:847-856.
47. Zeng R., Spolski R., Finkelstein S.E., Oh S., Kovanen P.E., Hinrichs C.S., et al. Synergy of IL-21 and IL-15 in regulating CD8+ T cell expansion and function. JExp Med 2005, 201:139-148.
48. Strengell M., Sareneva T., Foster D., Julkunen I., Matikainen S. IL-21 up-regulates the expression of genes associated with innate immunity and Th1 response. JImmunol 2002, 169:3600-3605.
49. Pflanz S., Timans J.C., Cheung J., Rosales R., Kanzler H., Gilbert J., et al. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 2002, 16:779-790.
50. Awasthi A., Carrier Y., Peron J.P., Bettelli E., Kamanaka M., Flavell R.A., et al. Adominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat Immunol 2007, 8:1380-1389.
51. Pot C., Jin H., Awasthi A., Liu S.M., Lai C.Y., Madan R., et al. Cutting edge: IL-27 induces the transcription factor c-Maf, cytokine IL-21, and the costimulatory receptor ICOS that coordinately act together to promote differentiation of IL-10-producing Tr1 cells. JImmunol 2009, 183:797-801.
52. Diveu C., McGeachy M.J., Boniface K., Stumhofer J.S., Sathe M., Joyce-Shaikh B., et al. IL-27 blocks RORc expression to inhibit lineage commitment of Th17 cells. JImmunol 2009, 182:5748-5756.
53. Fantuzzi G., Reed D.A., Dinarello C.A. IL-12-induced IFN-gamma is dependent on caspase-1 processing of the IL-18 precursor. JClin Invest 1999, 104:761-767.
54. Ma A., Koka R., Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 2006, 24:657-679.
55. Lindor K.D., Gershwin M.E., Poupon R., Kaplan M., Bergasa N.V., Heathcote E.J., et al. Primary biliary cirrhosis. Hepatology 2009, 50:291-308.
56. Sakamoto H., Zhao L.H., Jain F., Kradin R. IL-12p40(-/-) mice treated with intratracheal bleomycin exhibit decreased pulmonary inflammation and increased fibrosis. Exp Mol Pathol 2002, 72:1-9.
57. Mentink-Kane M.M., Cheever A.W., Wilson M.S., Madala S.K., Beers L.M., Ramalingam T.R., et al. Accelerated and progressive and lethal liver fibrosis in mice that lack interleukin (IL)-10, IL-12p40, and IL-13Ralpha2. Gastroenterology 2011, 141:2200-2209.
58. Meng F., Wang K., Aoyama T., Grivennikov S.I., Paik Y., Scholten D., et al. Interleukin-17 signaling in inflammatory, Kupffer cells, and hepatic stellate cells exacerbates liver fibrosis in mice. Gastroenterology 2012, 143:765-776. e1-3.
59. Jeong W.I., Park O., Radaeva S., Gao B. STAT1 inhibits liver fibrosis in mice by inhibiting stellate cell proliferation and stimulating NK cell cytotoxicity. Hepatology 2006, 44:1441-1451.
60. Bansal R., Prakash J., Post E., Beljaars L., Schuppan D., Poelstra K. Novel engineered targeted interferon-gamma blocks hepatic fibrogenesis in mice. Hepatology 2011, 54:586-596.
61. Simeonova P.P., Gallucci R.M., Hulderman T., Wilson R., Kommineni C., Rao M., et al. The role of tumor necrosis factor-alpha in liver toxicity, inflammation, and fibrosis induced by carbon tetrachloride. Toxicol Appl Pharmacol 2001, 177:112-120.
62. Connolly M.K., Bedrosian A.S., Mallen-St Clair J., Mitchell A.P., Ibrahim J., Stroud A., et al. In liver fibrosis, dendritic cells govern hepatic inflammation in mice via TNF-alpha. JClin Invest 2009, 119:3213-3225.
63. Loffreda S., Rai R., Yang S.Q., Lin H.Z., Diehl A.M. Bile ducts and portal and central veins are major producers of tumor necrosis factor alpha in regenerating rat liver. Gastroenterology 1997, 112:2089-2098.
64. Harada K., Chiba M., Okamura A., Hsu M., Sato Y., Igarashi S., et al. Monocyte chemoattractant protein-1 derived from biliary innate immunity contributes to hepatic fibrogenesis. JClin Pathol 2011, 64:660-665.
65. Kruglov E.A., Nathanson R.A., Nguyen T., Dranoff J.A. Secretion of MCP-1/CCL2 by bile duct epithelia induces myofibroblastic transdifferentiation of portal fibroblasts. Am J Physiol Gastrointest Liver Physiol 2006, 290:G765-G771.
66. Kawata K., Tsuda M., Yang G.X., Zhang W., Tanaka H., Tsuneyama K., et al. Identification of potential cytokine pathways for therapeutic intervention in murine primary biliary cirrhosis. PLoS One 2013, 8:e74225.
67. Rong G.H., Yang G.X., Ando Y., Zhang W., He X.S., Leung P.S., et al. Human intrahepatic biliary epithelial cells engulf blebs from their apoptotic peers. Clin Exp Immunol 2013, 172:95-103.
68. Ando Y., Yang G.X., Kenny T.P., Kawata K., Zhang W., Huang W., et al. Overexpression of microRNA-21 is associated with elevated pro-inflammatory cytokines in dominant-negative TGF-beta receptor type II mouse. JAutoimmun 2013, 41:111-119.