First characterization of a teleost Epstein-Barr virus-induced gene 3 (EBI3) reveals a regulatory effect of EBI3 on the innate immune response of peripheral blood leukocytes

Developmental and Comparative Immunology

Volumn 41, Issue 4, 2013, Pages 514-522

  Li, Mo fei ^a,b   Sun, Bo guang ^a   Xiao, Zhi zhong ^a   Sun, Li ^a  

^a INSTITUTE OF OCEANOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Cynoglossus semilaevis; Epstein Barr virus induced gene 3; Immunoregulation; Interleukin 27

Indexed keywords

CD28 ANTIGEN; CHEMOKINE; EBI3 PROTEIN; FIBRONECTIN; FIBRONECTIN TYPE 3 PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 8; MUTANT PROTEIN; MYELOID DIFFERENTIATION FACTOR 88; RECOMBINANT EBI3 PROTEIN; RECOMBINANT PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIAL INFECTION; BIOLOGICAL ACTIVITY; CD28 GENE; CELL RESPIRATION; CONTROLLED STUDY; CYNOGLOSSUS SEMILAEVIS; EBI3 GENE; EXTRACELLULAR SPACE; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HOST RESISTANCE; IL 8 GENE; IMMUNOREGULATION; INNATE IMMUNITY; INTERFERON INDUCED GENE 15; INTERLEUKIN 1BETA GENE; LEUKOCYTE; LEUKOCYTE ACTIVATION; MYD88 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN SECRETION; TELEOST; UPREGULATION; VERTEBRATE; VIRUS INFECTION;

BACTERIA (MICROORGANISMS); CYNOGLOSSIDAE; CYNOGLOSSUS SEMILAEVIS; HUMAN HERPESVIRUS 4; MAMMALIA; TELEOSTEI; VERTEBRATA;

CYNOGLOSSUS SEMILAEVIS; EPSTEIN-BARR VIRUS-INDUCED GENE 3; IMMUNOREGULATION; INTERLEUKIN-27;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; BACTERIAL INFECTIONS; BASE SEQUENCE; FISH DISEASES; FISH PROTEINS; FLATFISHES; GENE EXPRESSION; IMMUNITY, INNATE; LEUKOCYTES; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84883317847     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.07.022     Document Type: Article

References (44)

1. Aida Y., Pabst M.J. Removal of endotoxin from protein solutions by phase separation using Triton X-114. J. Immunol. Methods 1990, 132:191-195.
2. Baker B.J., Park K.W., Qin H., Ma X., Benveniste E.N. IL-27 inhibits OSM mediated TNF-alpha and iNOS gene expression in microglia. Glia 2010, 58:1082-1093.
3. Chung S., Secombes C.J. Analysis of events occurring within teleost macrophages during the respiratory burst. Comp. Biochem. Physiol. 1988, 89:539-544.
4. Collison L.W., Vignali D.A. Interleukin-35: odd one out or part of the family?. Immunol. Rev. 2008, 226:248-262.
5. Collison L.W., Workman C.J., Kuo T.T., Boyd K., Wang Y., Vignali K.M., Cross R., David S., Blumberg R., Vignali1 D. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 2007, 450:566-569.
6. Devergne O., Birkenbach M., Kieff E. Epstein-Barr virus-induced gene 3 and the p35 subunit of interleukin 12 form a novel heterodimeric hematopoietin. Proc. Natl. Acad. Sci. 1997, 94:12041-12046.
7. Devergne O., Hummel M., Koeppen H., Le-Beau M.M., Nathanson E.C., Kieff E., Birkenbach M. A novel interleukin-12 p40-related protein induced by latent Epstein-Barr virus infection in B lymphocytes. J. Virol. 1996, 70:1143-1153.
8. Hu Y.H., Liu C.S., Hou J.H., Sun L. Identification, characterization, and molecular application of a virulence associated autotransporter from a pathogenic Pseudomonas fluorescens strain. Appl. Environ. Microbiol. 2009, 75:4333-4340.
9. Hu Y.H., Sun B., Deng T., Sun L. Molecular characterization of Cynoglossus semilaevis CD28. Fish Shellfish Immunol. 2012, 32:934-938.
10. Igawa T., Nakashima H., Sadanaga A., Masutani K., Miyake K., Shimizu S., Takeda A., Hamano S., Yoshida H. Deficiency in EBV-induced gene 3 (EBI3) in MRL/lpr mice results in pathological alteration of autoimmune glomerulonephritis and sialadenitis. Mod. Rheumatol. 2009, 19:33-41.
11. Larousserie F., Bardel E., Pflanz S., Arnulf B., Lome-Maldonado C., Hermine O., Brégeaud L., Perennec M., Brousse N., Kastelein R., Devergne O. Analysis of interleukin-27 (EBI3/p28) expression in Epstein-Barr virus- and human T-cell leukemia virus type 1-associated lymphomas: heterogeneous expression of EBI3 subunit by tumoral cells. Am. J. Pathol. 2005, 166:1217-1228.
12. Larousserie F., Charlot P., Bardel E., Froger J., Kastelein R.A., Devergne O. Differential effects of IL-27 on human B cell subsets. J. Immunol. 2006, 176:5890-5897.
13. Larousserie F., Pflanz S., Coulomb-L'Herminé A., Brousse N., Kastelein R., Devergne O. Expression of IL-27 in human Th1-associated granulomatous diseases. J. Pathol. 2004, 202:164-171.
14. Li H.Y., Zhang D.L., Ge J., Zhou H., Qi A.P., Ma L., Xue F., Zhou Z.P., Yang R.C. Elevated interleukin-27 enhances the polarization of Th1/Tc1 cells and the production of proinflammatory cytokines in primary immune thrombocytopenia. Hum. Immunol. 2012, 73:240-247.
15. Li Y.X., Hu Y.H., Sun J.S., Sun L. CsCXCe1: a novel Cynoglossus semilaevis CXC chemokine that functions as a chemoattractant and an immunomodulator for peripheral blood leukocytes. Dev. Comp. Immunol. 2012, 37:54-64.
16. Li Y.X., Sun J., Sun L. An inflammatory CC chemokine of Cynoglossus semilaevis is involved in immune defense against bacterial infection. Fish Shellfish Immunol. 2011, 31:446-452.
17. Liu C.S., Sun Y., Zhang M., Sun L. Identification and analysis of a Sciaenops ocellatus ISG15 homologue that is involved in host immune defense against bacterial infection. Fish Shellfish Immunol. 2010, 29:167-174.
18. Liu J.Q., Liu Z., Zhang X., Shi Y., Talebian F., Carl J.W., Yu C., Shi F.D., Whitacre C.C., Trgovcich J., Bai X.F. Increased Th17 and regulatory T cell responses in EBV induced gene 3-deficient mice lead to marginally enhanced development of autoimmune encephalomyelitis. J. Immunol. 2012, 188:3099-3106.
19. Lucas S., Ghilardi N., Li J., de-Sauvage F.J. IL-27 regulates IL-12 responsiveness of naive CD4+ T cells through Stat1-dependent and -independent mechanisms. Proc. Natl. Acad. Sci. USA 2003, 100:15047-15052.
20. Morishima N., Mizoguchi I., Okumura M., Chiba Y., Xu M., Shimizu M., Matsui M., Mizuguchi J., Yoshimoto T. A pivotal role for interleukin-27 in CD8+ T cell functions and generation of cytotoxic T lymphocytes. J. Biomed. Biotechnol. 2010, 201:1-10.
21. Murugaiyan G., Mittal A., Lopez-Diego R., Maier L.M., Anderson D.E., Weiner H.L. IL-27 is a key regulator of IL-10 and IL-17 production by human CD4+ T cells. J. Immunol. 2009, 183:2435-2443.
22. Niedbala W., Wei X.Q., Cai B., Hueber A.J., Leung B.P., McInnes I.B., Liew F.Y. IL-35 is a novel cytokine with therapeutic effects against collagen-induced arthritis through the expansion of regulatory T cells and suppression of Th17 cells. Eur. J. Immunol. 2007, 37:3021-3029.
23. Nieuwenhuis E.E., Neurath M.F., Corazza N., Iijima H., Trgovcich J., Wirtz S., Glickman J., Bailey D., Yoshida M., Galle R.P., Kronenberg M., Birkenbach M., Blumberg R.S. Disruption of T helper 2-immune responses in Epstein-Barr virus-induced gene 3-deficient mice. Proc. Natl. Acad. Sci. 2002, 99:16951-16956.
24. Pflanz S., Hibbert L., Mattson J., Rosales R., Vaisberg E., Bazan J.F., Phillips J.H., McClanahan T.K., Malefyt R.D., Kastelein R.A. WSX-1 and glycoprotein 130 constitute a signaltransducing receptor for IL-27. J. Immunol. 2004, 172:2225-2231.
25. Pflanz S., Timans J.C., Cheung J., Rosales R., Kanzler H., Gilbert J., Hibbert L., Churakova T., Travis M., Vaisberg E., Blumenschein W.M., Mattson J.D., Wagner J.L., To W., Zurawski S., McClanahan T.K., Gorman D.M., Bazan J.F., Malefyt R.D., Rennick D., Kastelein R.A. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 2002, 16:779-790.
26. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 3rd ed.
27. Shimizu M., Ogura K., Mizoguchi I., Chiba Y., Higuchi K., Ohtsuka H., Mizuguchi J., Yoshimoto T. IL-27 promotes nitric oxide production induced by LPS through STAT1, NF-κB and MAPKs. Immunobiology 2013, 218:628-634.
28. Stumhofer J.S., Hunter C.A. Advances in understanding the anti-inflammatory properties of IL-27. Immunol. Lett. 2008, 117:123-130.
29. Sun Y., Zheng W.J., Hu Y.H., Sun B.G., Sun L. Edwardsiella tarda et al., an in vivo induced antigen that is involved in host infection. Infect. Immun. 2012, 80:2948-2955.
30. Tong H., Miyazaki Y., Yamazaki M., Hara H., Waldmann H., Hori S., Yoshida H. Exacerbation of delayed-type hypersensitivity responses in EBV-induced gene-3 (EBI-3)-deficient mice. Immunol. Lett. 2010, 128:108-115.
31. Wang H.R., Hu Y.H., Zhang W.W., Sun L. Construction of an attenuated Pseudomonas fluorescens strain and evaluation of its potential as a cross protective vaccine. Vaccine 2009, 27:4047-4055.
32. Wong H.R., Cvijanovich N.Z., Hall M., Allen G.L., Thomas N.J., Freishtat R.J., Anas N., Meyer K., Checchia P.A., Lin R., Bigham M.T., Sen A., Nowak J., Quasney M., Henricksen J.W., Chopra A., Banschbach S., Beckman E., Harmon K., Lahni P., Shanley T.P. Interleukin-27 is a novel candidate diagnostic biomarker for bacterial infection in critically ill children. Crit. Care 2012, 16:213.
33. Yang J., Yang M., Htut T.M., Ouyang X., Hanidu A., Li X., Sellati R., Jiang H., Zhang S., Li H., Zhao J., Ting A.T., Mayer L., Unkeless J.C., Labadia M.E., Hodge M., Li J., Xiong H. Epstein-Barr virus-induced gene 3 negatively regulates IL-17, IL-22 and RORgamma t. Eur. J. Immunol. 2008, 38:1204-1214.
34. Yoshida H., Miyazaki Y. Regulation of immune responses by interleukin-27. Immunol. Rev. 2008, 226:234-247.
35. Yoshida H., Nakaya M., Miyazaki Y. Interleukin 27: a double-edged sword for offense and defense. J. Leukoc. Biol. 2009, 86:1295-1303.
36. Wang W., Zhang M., Sun L. Ferritin M of Cynoglossus semilaevis: an iron binding protein and a broad spectrum antimicrobial that depends on the integrity of the ferroxidase center and nucleation center for biological activity. Fish Shellfish Immunol. 2011, 31:269-274.
37. Wang W., Zhang M., Xiao Z., Sun L. Cynoglossus semilaevis ISG15: a secreted cytokine-like protein that stimulates antiviral immune response in a LRGG motif-dependent manner. PLoS ONE 2012, 7:44884.
38. Wojno E.D., Hunter C.A. New directions in the basic and translational biology of interleukin-27. Trends Immunol. 2012, 33:91-97.
39. Zahn S., Wirtz S., Birkenbach M., Blumberg R.S., Neurath M.F., von-Stebut E. Impaired Th1 responses in mice deficient in Epstein-Barr virus-induced gene 3 and challenged with physiological doses of Leishmania major. Eur. J. Immunol. 2005, 35:1106-1112.
40. Zhang M., Sun K., Sun L. Regulation of autoinducer 2 production and luxS expression in a pathogenic Edwardsiella tarda strain. Microbiology 2008, 154:2060-2069.
41. Zhang M., Xiao Z., Hu Y.H., Sun L. Characterization of a megalocytivirus from cultured rock bream, Oplegnathus fasciatus (Temminck & Schlege) in China. Aquac. Res. 2012, 43:556-564.
42. Zhang M., Xiao Z., Sun L. Overexpression of NF-B inhibitor alpha in Cynoglossus semilaevis impairs pathogen-induced immune response. Dev. Comp. Immunol. 2012, 36:253-257.
43. Zheng W.J., Hu Y., Sun L. The two Dps of Edwardsiella tarda are involved in resistance against oxidative stress and host infection. Fish Shellfish Immunol. 2011, 31:985-992.
44. Zheng W.J., Sun L. Evaluation of housekeeping genes as references for quantitative real time RT-PCR analysis of gene expression in Japanese flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 2011, 30:638-645.