Bioactivity studies of rainbow trout (Oncorhynchus mykiss) interleukin-6: Effects on macrophage growth and antimicrobial peptide gene expression

Molecular Immunology

Volumn 48, Issue 15-16, 2011, Pages 1903-1916

  Costa, Maria M ^a,b   Maehr, Tanja ^a   Diaz Rosales, Patricia ^a   Secombes, Christopher J ^a   Wang, Tiehui ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b INSTITUTO DE INVESTIGACIONES MARINAS   (Spain)

Author keywords

Cathelicidin; Hepcidin; Interleukin 6; JAK STAT; SOCS

Indexed keywords

CATHELICIDIN; HEPCIDIN; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 1BETA; IRON; LIPOPOLYSACCHARIDE; POLYPEPTIDE ANTIBIOTIC AGENT; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL GROWTH; CELL PROLIFERATION; DOWN REGULATION; DRUG ACTIVITY; GENE EXPRESSION; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; INFECTION; INFLAMMATION; IRON ABSORPTION; IRON DEFICIENCY; MACROPHAGE FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAINBOW TROUT; SEPSIS;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BLOTTING, WESTERN; CELL LINE; CELL PROLIFERATION; GENE EXPRESSION PROFILING; INTERLEUKIN-6; MACROPHAGES; ONCORHYNCHUS MYKISS; POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

MAMMALIA; ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 80051939266     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2011.05.027     Document Type: Article

References (65)

1. Alessi D.R., Cuenda A., Cohen P., Dudley D.T., Saltiel A.R. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 1995, 270:27489-27494.
2. Barnett S.F., Defeo-Jones D., Fu S., Hancock P.J., Haskell K.M., Jones R.E., Kahana J.A., Kral A.M., Leander K., Lee L.L., Malinowski J., McAvoy E.M., Nahas D.D., Robinson R.G., Huber H.E. Identification and characterization of pleckstrin-homology-domain-dependent and isoenzyme-specific Akt inhibitors. Biochem. J. 2005, 385:399-408.
3. Bird S., Zou J., Savan R., Kono T., Sakai M., Woo J., Secombes C. Characterisation and expression analysis of an interleukin 6 homologue in the Japanese pufferfish, Fugu rubripes. Dev. Comp. Immunol. 2005, 29:775-789.
4. Boshra H., Wang T., Hove-Madsen L., Hansen J., Li J., Matlapudi A., Secombes C.J., Tort L., Sunyer J.O. Characterization of a C3a receptor in rainbow trout and Xenopus: the first identification of C3a receptors in nonmammalian species. J. Immunol. 2005, 175:2427-2437.
5. Breen E.C. Pro- and anti-inflammatory cytokines in human immunodeficiency virus infection and acquired immunodeficiency syndrome. Pharmacol. Ther. 2002, 95:295-304.
6. Casadei E., Wang T., Zou J., Gonzalez Vecino J.L., Wadsworth S., Secombes C.J. Characterization of three novel beta-defensin antimicrobial peptides in rainbow trout (Oncorhynchus mykiss). Mol. Immunol. 2009, 46:3358-3366.
7. Castellana B., Iliev D.B., Sepulcre M.P., MacKenzie S., Goetz F.W., Mulero V., Planas J.V. Molecular characterization of interleukin-6 in the gilthead seabream (Sparus aurata). Mol. Immunol. 2008, 45:3363-3370.
8. Chang C.I., Zhang Y.A., Zou J., Nie P., Secombes C.J. Two cathelicidin genes are present in both rainbow trout (Oncorhynchus mykiss) and atlantic salmon (Salmo salar). Antimicrob. Agents Chemother. 2006, 50:185-195.
9. Chomarat P., Banchereau J., Davoust J., Palucka A.K. IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat. Immunol. 2000, 1:510-514.
10. Chung J., Uchida E., Grammer T.C., Blenis J. STAT3 serine phosphorylation by ERK-dependent and -independent pathways negatively modulates its tyrosine phosphorylation. Mol. Cell. Biol. 1997, 17:6508-6516.
11. Clutterbuck R., Powles R., Millar J., Catovsky D. Interleukin-6 and other gp130-dependent cytokines selectively inhibit proliferation of macrophage-lineage hemopoietic progenitor cells. Exp. Hematol. 2000, 28:1120-1128.
12. Collet B., Hovens G.C., Mazzoni D., Hirono I., Aoki T., Secombes C.J. Cloning and expression analysis of rainbow trout Oncorhynchus mykiss interferon regulatory factor 1 and 2 (IRF-1 and IRF-2). Dev. Comp. Immunol. 2003, 27:111-126.
13. Douglas S.E., Gallant J.W., Liebscher R.S., Dacanay A., Tsoi S.C. Identification and expression analysis of hepcidin-like antimicrobial peptides in bony fish. Dev. Comp. Immunol. 2003, 27:589-601.
14. Drucker C., Gewiese J., Malchow S., Scheller J., Rose-John S. Impact of interleukin-6 classic- and trans-signaling on liver damage and regeneration. J. Autoimmun. 2010, 34:29-37.
15. Ferrajoli A., Faderl S., Van Q., Koch P., Harris D., Liu Z., Hazan-Halevy I., Wang Y., Kantarjian H.M., Priebe W., Estrov Z. WP1066 disrupts Janus kinase-2 and induces caspase-dependent apoptosis in acute, myelogenous leukemia cells. Cancer Res. 2007, 67:11291-11299.
16. Fonseca J.E., Santos M.J., Canhao H., Choy E. Interleukin-6 as a key player in systemic inflammation and joint destruction. Autoimmun. Rev. 2009, 8:538-542.
17. Ganassin R.C., Bols N.C. Development of a monocyte/macrophage-like cell line, RTS11, from rainbow trout spleen. Fish Shellfish Immunol. 1998, 8:457-476.
18. Hanington P.C., Belosevic M. Characterization of the leukemia inhibitory factor receptor in the goldfish (Carassius auratus). Fish Shellfish Immunol. 2005, 18:359-369.
19. Hardie L.J., Laing K.J., Daniels G.D., Grabowski P.S., Cunningham C., Secombes C.J. Isolation of the first piscine transforming growth factor beta gene: analysis reveals tissue specific expression and a potential regulatory sequence in rainbow trout (Oncorhynchus mykiss). Cytokine 1998, 10:555-563.
20. Heinrich P.C., Behrmann I., Haan S., Hermanns H.M., Muller-Newen G., Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 2003, 374:1-20.
21. Hirano T. Interleukin 6 in autoimmune and inflammatory diseases: a personal memoir. Proc. Jpn. Acad. Ser. B. Phys. Biol. Sci. 2010, 86:717-730.
22. Holland J.W., Karim A., Wang T., Alnabulsi A., Scott J., Collet B., Mughal M.S., Secombes C.J., Bird S. Molecular cloning and characterization of interferon regulatory factors 4 and 8 (IRF-4 and IRF-8) in rainbow trout, Oncorhynchus mykiss. Fish Shellfish Immunol. 2010, 29:157-166.
23. Hong S., Zou J., Crampe M., Peddie S., Scapigliati G., Bols N., Cunningham C., Secombes C.J. The production and bioactivity of rainbow trout (Oncorhynchus mykiss) recombinant IL-1 beta. Vet. Immunol. Immunopathol. 2001, 81:1-14.
24. Iliev D.B., Castellana B., Mackenzie S., Planas J.V., Goetz F.W. Cloning and expression analysis of an IL-6 homolog in rainbow trout (Oncorhynchus mykiss). Mol. Immunol. 2007, 44:1803-1807.
25. Inoue Y., Kamota S., Ito K., Yoshiura Y., Ototake M., Moritomo T., Nakanishi T. Molecular cloning and expression analysis of rainbow trout (Oncorhynchus mykiss) interleukin-10 cDNAs. Fish Shellfish Immunol. 2005, 18:335-344.
26. Into T., Inomata M., Shibata K., Murakami Y. Effect of the antimicrobial peptide LL-37 on Toll-like receptors 2-, 3- and 4-triggered expression of IL-6, IL-8 and CXCL10 in human gingival fibroblasts. Cell. Immunol. 2010, 264:104-109.
27. Jansen J.H., Kluin-Nelemans J.C., Van Damme J., Wientjens G.J., Willemze R., Fibbe W.E. Interleukin 6 is a permissive factor for monocytic colony formation by human hematopoietic progenitor cells. J. Exp. Med. 1992, 175:1151-1154.
28. Jenkins B.J., Grail D., Inglese M., Quilici C., Bozinovski S., Wong P., Ernst M. Imbalanced gp130-dependent signaling in macrophages alters macrophage colony-stimulating factor responsiveness via regulation of c-fms expression. Mol. Cell. Biol. 2004, 24:1453-1463.
29. Kishimoto T. Interleukin-6: from basic science to medicine-40 years in immunology. Annu. Rev. Immunol. 2005, 23:1-21.
30. Laing K.J., Wang T., Zou J., Holland J., Hong S., Bols N., Hirono I., Aoki T., Secombes C.J. Cloning and expression analysis of rainbow trout Oncorhynchus mykiss tumour necrosis factor-alpha. Eur. J. Biochem. 2001, 268:1315-1322.
31. Laing K.J., Bols N., Secombes C.J. A CXC chemokine sequence isolated from the rainbow trout Oncorhynchus mykiss resembles the closely related interferon-gamma-inducible chemokines CXCL9, CXCL10 and CXCL11. Eur. Cytokine Netw. 2002, 13:462-473.
32. Laing K.J., Zou J.J., Wang T., Bols N., Hirono I., Aoki T., Secombes C.J. Identification and analysis of an interleukin 8-like molecule in rainbow trout Oncorhynchus mykiss. Dev. Comp. Immunol. 2002, 26:433-444.
33. Lou D.Q., Lesbordes J.C., Nicolas G., Viatte L., Bennoun M., Van Rooijen N., Kahn A., Renia L., Vaulont S. Iron- and inflammation-induced hepcidin gene expression in mice is not mediated by Kupffer cells in vivo. Hepatology 2005, 41:1056-1064.
34. Mitani Y., Takaoka A., Kim S.H., Kato Y., Yokochi T., Tanaka N., Taniguchi T. Cross talk of the interferon-alpha/beta signalling complex with gp130 for effective interleukin-6 signalling. Genes Cells 2001, 6:631-640.
35. Nam B.H., Byon J.Y., Kim Y.O., Park E.M., Cho Y.C., Cheong J. Molecular cloning and characterisation of the flounder (Paralichthys olivaceus) interleukin-6 gene. Fish Shellfish Immunol. 2007, 23:231-236.
36. Nemeth E., Rivera S., Gabayan V., Keller C., Taudorf S., Pedersen B.K., Ganz T. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J. Clin. Invest. 2004, 113:1271-1276.
37. Nishimoto N., Kishimoto T. Interleukin 6: from bench to bedside. Nat. Clin. Pract. Rheumatol. 2006, 2:619-626.
38. Satriotomo I., Bowen K.K., Vemuganti R. JAK2 and STAT3 activation contributes to neuronal damage following transient focal cerebral ischemia. J. Neurochem. 2006, 98:1353-1368.
39. Savitsky D., Tamura T., Yanai H., Taniguchi T. Regulation of immunity and oncogenesis by the IRF transcription factor family. Cancer Immunol. Immunother. 2010, 59:489-510.
40. Schust J., Sperl B., Hollis A., Mayer T.U., Berg T. Stattic: a small-molecule inhibitor of STAT3 activation and dimerization. Chem. Biol. 2006, 13:1235-1242.
41. Sims N.A. gp130 signaling in bone cell biology: multiple roles revealed by analysis of genetically altered mice. Mol. Cell. Endocrinol. 2009, 310:30-39.
42. Sow F.B., Florence W.C., Satoskar A.R., Schlesinger L.S., Zwilling B.S., Lafuse W.P. Expression and localization of hepcidin in macrophages: a role in host defense against tuberculosis. J. Leukoc. Biol. 2007, 82:934-945.
43. Starr R., Willson T.A., Viney E.M., Murray L.J., Rayner J.R., Jenkins B.J., Gonda T.J., Alexander W.S., Metcalf D., Nicola N.A., Hilton D.J. A family of cytokine-inducible inhibitors of signalling. Nature 1997, 387:917-921.
44. Suh H.N., Lee S.H., Lee M.Y., Lee Y.J., Lee J.H., Han H.J. Role of interleukin-6 in the control of DNA synthesis of hepatocytes: involvement of PKC, p44/42 MAPKs, and PPARdelta. Cell. Physiol. Biochem. 2008, 22:673-684.
45. Wang T., Secombes C.J. Complete sequencing and expression of three complement components, C1r, C4 and C1 inhibitor, of the classical activation pathway of the complement system in rainbow trout Oncorhynchus mykiss. Immunogenetics 2003, 55:615-628.
46. Wang T., Johnson N., Zou J., Bols N., Secombes C.J. Sequencing and expression of the second allele of the interleukin-1beta1 gene in rainbow trout (Oncorhynchus mykiss): identification of a novel SINE in the third intron. Fish Shellfish Immunol. 2004, 16:335-358.
47. Wang T., Holland J.W., Bols N., Secombes C.J. Cloning and expression of the first nonmammalian interleukin-11 gene in rainbow trout Oncorhynchus mykiss. FEBS J. 2005, 272:1136-1147.
48. Wang T., Holland J.W., Carrington A., Zou J., Secombes C.J. Molecular and functional characterization of IL-15 in rainbow trout Oncorhynchus mykiss: a potent inducer of IFN-gamma expression in spleen leukocytes. J. Immunol. 2007, 179:1475-1488.
49. Wang T., Secombes C.J. Rainbow trout suppressor of cytokine signalling (SOCS)-1, 2 and 3: molecular identification, expression and modulation. Mol. Immunol. 2008, 45:1449-1457.
50. Wang T., Secombes C.J. Identification and expression analysis of two fish-specific IL-6 cytokine family members, the ciliary neurotrophic factor (CNTF)-like and M17 genes, in rainbow trout Oncorhynchus mykiss. Mol. Immunol. 2009, 46:2290-2298.
51. Wang T., Bird S., Koussounadis A., Holland J.W., Carrington A., Zou J., Secombes C.J. Identification of a novel IL-1 cytokine family member in teleost fish. J. Immunol. 2009, 183:962-974.
52. Wang T., Gao Q., Nie P., Secombes C.J. Identification of suppressor of cytokine signalling (SOCS) 6, 7, 9 and CISH in rainbow trout Oncorhynchus mykiss and analysis of their expression in relation to other known trout SOCS. Fish Shellfish Immunol. 2010, 29:656-667.
53. Wang T., Martin S.A., Secombes C.J. Two interleukin-17C-like genes exist in rainbow trout Oncorhynchus mykiss that are differentially expressed and modulated. Dev. Comp. Immunol. 2010, 34:491-500.
54. Wang T., Diaz-Rosales P., Martin S.A., Secombes C.J. Cloning of a novel interleukin (IL)-20-like gene in rainbow trout Oncorhynchus mykiss gives an insight into the evolution of the IL-10 family. Dev. Comp. Immunol. 2010, 34:158-167.
55. Wang T., Diaz-Rosales P., Costa M.M., Campbell S., Snow M., Collet B., Martin S.A., Secombes C.J. Functional characterization of a nonmammalian IL-21: rainbow trout Oncorhynchus mykiss IL-21 upregulates the expression of the Th cell signature cytokines IFN-gamma, IL-10, and IL-22. J. Immunol. 2011, 186:708-721.
56. Wang T., Huang W., Costa M.M., Martin S.A., Secombes C.J. Two copies of the genes encoding the subunits of putative interleukin (IL)-4/IL-13 receptors, IL-4Rα, IL-13Rα1 and IL-13Rα2, have been identified in rainbow trout (Oncorhynchus mykiss) and have complex patterns of expression and modulation. Immunogenetics 2011, 63:235-253.
57. Wessling-Resnick M. Iron homeostasis and the inflammatory response. Annu. Rev. Nutr. 2010, 30:105-122.
58. Wolvekamp M.C., Marquet R.L. Interleukin-6: historical background, genetics and biological significance. Immunol. Lett. 1990, 24:1-9.
59. Wrighting D.M., Andrews N.C. Interleukin-6 induces hepcidin expression through STAT3. Blood 2006, 108:3204-3209.
60. Wu H., Zhang G., Minton J.E., Ross C.R., Blecha F. Regulation of cathelicidin gene expression: induction by lipopolysaccharide, interleukin-6, retinoic acid, and Salmonella enterica serovar typhimurium infection. Infect. Immun. 2000, 68:5552-5558.
61. Wymann M.P., Bulgarelli-Leva G., Zvelebil M.J., Pirola L., Vanhaesebroeck B., Waterfield M.D., Panayotou G. Wortmannin inactivates phosphoinositide 3-kinase by covalent modification of Lys-802, a residue involved in the phosphate transfer reaction. Mol. Cell. Biol. 1996, 16:1722-1733.
62. Zhang Y.A., Zou J., Chang C.I., Secombes C.J. Discovery and characterization of two types of liver-expressed antimicrobial peptide 2 (LEAP-2) genes in rainbow trout. Vet. Immunol. Immunopathol. 2004, 101:259-269.
63. Zou J., Bird S., Truckle J., Bols N., Horne M., Secombes C. Identification and expression analysis of an IL-18 homologue and its alternatively spliced form in rainbow trout (Oncorhynchus mykiss). Eur. J. Biochem. 2004, 271:1913-1923.
64. Zou J., Peddie S., Scapigliati G., Zhang Y., Bols N.C., Ellis A.E., Secombes C.J. Functional characterisation of the recombinant tumor necrosis factors in rainbow trout, Oncorhynchus mykiss. Dev. Comp. Immunol. 2003, 27:813-822.
65. Zou J., Wang T., Hirono I., Aoki T., Inagawa H., Honda T., Soma G.I., Ototake M., Nakanishi T., Ellis A.E., Secombes C.J. Differential expression of two tumor necrosis factor genes in rainbow trout, Oncorhynchus mykiss. Dev. Comp. Immunol. 2002, 26:161-172.