Molecular characterization and expression analysis of the putative interleukin 6 receptor (IL-6Ralpha and glycoprotein-130) in rainbow trout (Oncorhynchus mykiss): salmonid IL-6Ralpha possesses a polymorphic N-terminal Ig domain with variable numbers of two repeats.
Costa, Maria M.; Wang, Tiehui; Mira Monte, Milenaet al.
[en] Interleukin (IL)-6, the founding member of IL-6 family cytokines, plays non-redundant roles in hematopoiesis and acute phase responses. IL-6 signals via a specific private IL-6Ralpha and a common beta chain gp130. In this study, we have cloned both the IL-6Ralpha and gp130 in rainbow trout. The trout gp130 cDNA encodes 906 aa and is similar in size, extracellular domain structure (D1-D6) and presence of intracellular motifs important for signal transduction to tetrapod gp130s. The trout IL-6Ralpha cDNA encodes for 834 aa and is larger compared to tetrapod IL-6Ralphas, as are other fish IL-6Ralpha molecules due to a large D1 domain. However, the cytokine-binding domain is well conserved across vertebrates, with four conserved cysteine residues in the N-terminal FNIII domain and a WSXWS motif in the C-terminal FNIII domain. Furthermore, a phylogenetic tree analysis confirmed that the reported fish IL-6Ralpha and gp130 molecules are orthologues to their tetrapod counterparts. The extra large D1 domain of the salmonid IL-6Ralpha molecules results partially from the insertions of two repetitive sequences of [TS]-[TF]-VSTTT-[ND]-TTSNG and TTVS-[AT]-IKD-[DG]-S-[KD]-N-[GR], respectively. Furthermore the numbers of repetitions of the two motifs were variable in different individuals and cell lines, and even in the same fish allelic polymorphism exists. Trout IL-6Ralpha was expressed at higher levels than gp130 in a number of tissues examined and the expression of both IL-6Ralpha and gp130 could be modulated by LPS and Poly I:C in the cell lines studied. The expression patterns of the receptors suggest that high level expression of IL-6Ralpha is critical for IL-6 responsiveness.
Molecular characterization and expression analysis of the putative interleukin 6 receptor (IL-6Ralpha and glycoprotein-130) in rainbow trout (Oncorhynchus mykiss): salmonid IL-6Ralpha possesses a polymorphic N-terminal Ig domain with variable numbers of two repeats.
K Abe M Hirai K Mizuno N Higashi T Sekimoto T Miki T Hirano K Nakajima 2001 The YXXQ motif in gp130 is crucial for STAT3 phosphorylation at Ser727 through an H7-sensitive kinase pathway Oncogene 20 3464 3474 11429693 10.1038/sj.onc.1204461 1:CAS:528:DC%2BD3MXkvVals7o%3D
C Ancey E Menet P Corbi S Fredj M Garcia C Rucker-Martin J Bescond F Morel J Wijdenes JC Lecron D Potreau 2003 Human cardiomyocyte hypertrophy induced in vitro by gp130 stimulation Cardiovasc Res 59 78 85 12829178 10.1016/S0008-6363(03)00346-8 1:CAS:528:DC%2BD3sXkvVKisLY%3D
S Aparicio J Chapman E Stupka N Putnam JM Chia P Dehal A Christoffels S Rash S Hoon A Smit MD Gelpke J Roach T Oh IY Ho M Wong C Detter F Verhoef P Predki A Tay S Lucas P Richardson SF Smith MS Clark YJ Edwards N Doggett A Zharkikh SV Tavtigian D Pruss M Barnstead C Evans H Baden J Powell G Glusman L Rowen L Hood YH Tan G Elgar T Hawkins B Venkatesh D Rokhsar S Brenner 2002 Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes Science 297 1301 1310 12142439 10.1126/science.1072104 1:CAS:528: DC%2BD38Xms1ejtr8%3D
E Assier MC Boissier JM Dayer 2010 Interleukin-6: from identification of the cytokine to development of targeted treatments Joint Bone Spine 77 532 536 20869898 10.1016/j.jbspin.2010.07.007 1:CAS:528:DC%2BC3cXhsFCrurbK
H Baumann AJ Symes MR Comeau KK Morella Y Wang D Friend SF Ziegler JS Fink DP Gearing 1994 Multiple regions within the cytoplasmic domains of the leukemia inhibitory factor receptor and gp130 cooperate in signal transduction in hepatic and neuronal cells Mol Cell Biol 14 138 46 8264582 1:CAS:528:DyaK2cXhtVCmt78%3D
CJ Bayne L Gerwick 2001 The acute phase response and innate immunity of fish Dev Comp Immunol 25 725 743 11602193 10.1016/S0145-305X(01)00033-7 1:CAS:528:DC%2BD3MXmsFWkt78%3D
JF Bazan 1990 Structural design and molecular evolution of a cytokine receptor superfamily Proc Natl Acad Sci USA 87 6934 6938 2169613 10.1073/pnas.87.18.6934 1:CAS:528:DyaK3cXlvV2nurc%3D
E Bettelli T Korn VK Kuchroo 2007 Th17: the third member of the effector T cell trilogy Curr Opin Immunol 19 652 657 17766098 10.1016/j.coi.2007.07.020 1:CAS:528:DC%2BD2sXhsVCksb%2FO
Bird S, Zou J, Savan R, Kono T, Sakai M, Woo J, Secombes C (2005) Characterisation and expression analysis of an interleukin 6 homologue in the Japanese pufferfish, Fugu rubripes. Dev Comp Immunol. 29:775-789
MJ Boulanger DC Chow EE Brevnova KC Garcia 2003 Hexameric structure and assembly of the interleukin-6/IL-6 alpha-receptor/gp130 complex Science 300 2101 2114 12829785 10.1126/science.1083901 1:CAS:528:DC%2BD3sXkvVOrtrw%3D
JJ Campanella L Bitincka J Smalley 2003 MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences BMC Bioinform 4 29 10.1186/1471-2105-4-29
Castellana B, Iliev DB, Sepulcre MP, MacKenzie S, Goetz FW, Mulero V, Planas JV (2008) Molecular characterization of interleukin-6 in the gilthead seabream (Sparus aurata). Mol Immunol 45:3363-3370
R Chenna H Sugawara T Koike R Lopez TJ Gibson DG Higgins JD Thompson 2003 Multiple sequence alignment with the Clustal series of programs Nucleic Acids Res 31 3497 3500 12824352 10.1093/nar/gkg500 1:CAS:528:DC%2BD3sXltVWjsrg%3D
P Chomarat J Banchereau J Davoust AK Palucka 2000 IL-6 switches the differentiation of monocytes from dendritic cells to macrophages Nat Immunol 1 510 514 11101873 10.1038/82763 1:CAS:528:DC%2BD3cXoslyru70%3D
AR Cole NE Hall HR Treutlein JS Eddes GE Reid RL Moritz RJ Simpson 1999 Disulfide bond structure and N-glycosylation sites of the extracellular domain of the human interleukin-6 receptor J Biol Chem 274 7207 7215 10066782 10.1074/jbc.274.11.7207 1:CAS:528:DyaK1MXhvFWqtrs%3D
Costa MM, Diaz-Rosales P, Secombes CJ, Wang T (2011) Bioactivity studies of rainbow trout (Oncorhynchus mykiss) interleukin-6: effects on macrophage growth and antimicrobial peptide gene expression.
WS Davidson BF Koop SJ Jones P Iturra R Vidal A Maass I Jonassen S Lien SW Omholt 2010 Sequencing the genome of the Atlantic salmon (Salmo salar) Genome Biol 11 403 20887641
C Drucker J Gewiese S Malchow J Scheller S Rose-John 2010 Impact of interleukin-6 classic- and trans-signaling on liver damage and regeneration J Autoimmun 34 29 37 19717281 10.1016/j.jaut.2009.08.003 1:CAS:528: DC%2BC3cXhtlGjsb0%3D
O Emanuelsson S Brunak G von Heijne H Nielsen 2007 Locating proteins in the cell using TargetP, SignalP and related tools Nat Protoc 2 953 971 17446895 10.1038/nprot.2007.131 1:CAS:528:DC%2BD2sXhtFGnur%2FF
N Fasnacht W Müller 2008 Conditional gp130 deficient mouse mutants Semin Cell Dev Biol 19 379 384 18687405 10.1016/j.semcdb.2008.07.001 1:CAS:528:DC%2BD1cXhtFOrurzF
RD Finn J Mistry J Tate P Coggill A Heger JE Pollington OL Gavin P Gunasekaran G Ceric K Forslund L Holm EL Sonnhammer SR Eddy A Bateman 2010 The Pfam protein families database Nucleic Acids Res 38 D211 222 19920124 10.1093/nar/gkp985 1:CAS:528:DC%2BC3cXktlyhsA%3D%3D Database issue
P Fischer D Hilfiker-Kleiner 2007 Survival pathways in hypertrophy and heart failure: the gp130-STAT axis Basic Res Cardiol 102 393 411 17918316 10.1007/s00395-007-0674-z 1:CAS:528:DC%2BD2sXhtFCgtrvP
S Fredj J Bescond C Louault A Delwail JC Lecron D Potreau 2005 Role of interleukin-6 in cardiomyocyte/cardiac fibroblast interactions during myocyte hypertrophy and fibroblast proliferation J Cell Physiol 204 428 436 15717324 10.1002/jcp.20307 1:CAS:528:DC%2BD2MXlvFCrs7k%3D
K Fujiki M Nakao B Dixon 2003 Molecular cloning and characterisation of a carp (Cyprinus carpio) cytokine-like cDNA that shares sequence similarity with IL-6 subfamily cytokines CNTF, OSM and LIF Dev Comp Immunol 27 127 136 12543126 10.1016/S0145-305X(02)00074-5 1:CAS:528:DC%2BD3sXlt1yjsA%3D%3D
Ganassin RC, Bols NC (1998) Development of a monocyte/macrophage-like cell line, RTS11, from rainbow trout spleen. Fish and Shellfish Immunol 8457-8476.
Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. Protein identification and analysis tools on the ExPASy Server: Humana Press, 2005.
J Gerez J Bonfiglio S Sosa D Giacomini M Acuña AC Nagashima MJ Perone S Silberstein U Renner GK Stalla E Arzt 2007 Molecular transduction mechanisms of cytokine-hormone interactions: role of gp130 cytokines Exp Physiol 92 801 816 17827256 1:CAS:528:DC%2BD2sXhtFGgsLfL
PSE Ghezzi S Sacco C Foddi ML Barbaccia T Mennini 2000 Neurosteroid levels are increased in vivo after LPS treatment and negatively regulate LPS-induced TNF production Eur Cytokine Netw 11 464 469 11022133 1:CAS:528:DC%2BD3cXotFKqtr0%3D
PC Hanington M Belosevic 2005 Characterization of the leukemia inhibitory factor receptor in the goldfish (Carassius auratus) Fish Shellfish Immunol 18 359 369 15683914 10.1016/j.fsi.2004.09.003 1:CAS:528:DC%2BD2MXptlCjtg%3D%3D
PC Hanington M Belosevic 2007 Interleukin-6 family cytokine M17 induces differentiation and nitric oxide response of goldfish (Carassius auratus L.) macrophages Dev Comp Immunol 31 817 829 17250891 10.1016/j.dci.2006.12.001 1:CAS:528:DC%2BD2sXkt1aqt7k%3D
T Hirano 2010 Interleukin 6 in autoimmune and inflammatory diseases: a personal memoir Proc Jpn Acad Ser B Phys Biol Sci 86 717 30 20689230 10.2183/pjab.86.717 1:CAS:528:DC%2BC3cXhtFGms7%2FJ
MO Huising CP Kruiswijk JE van Schijndel HF Savelkoul G Flik BM Verburg-van Kemenade 2005 Multiple and highly divergent IL-11 genes in teleost fish Immunogenetics 57 432 443 16003467 10.1007/s00251-005-0012-2 1:CAS:528:DC%2BD2MXhtVektrnF
MO Huising CP Kruiswijk G Flik 2006 Phylogeny and evolution of class-I helical cytokines J Endocrinol 189 1 25 16614377 10.1677/joe.1.06591 1:CAS:528:DC%2BD28Xkslaqsb0%3D
JY Hwang MD Santos H Kondo I Hirono T Aoki 2007 Identification, characterization and expression of a novel cytokine M17 homologue (MSH) in fish Fish Shellfish Immunol 23 1256 1265 17950621 10.1016/j.fsi.2007.06.009 1:CAS:528:DC%2BD2sXht12htb3J
Iliev DB, Castellana B, Mackenzie S, Planas JV, Goetz FW (2007) Cloning and expression analysis of an IL-6 homolog in rainbow trout (Oncorhynchus mykiss). Mol Immunol. 44:1803-1807
O Jaillon JM Aury F Brunet JL Petit N Stange-Thomann E Mauceli L Bouneau C Fischer C Ozouf-Costaz A Bernot S Nicaud D Jaffe S Fisher G Lutfalla C Dossat B Segurens C Dasilva M Salanoubat M Levy N Boudet S Castellano V Anthouard C Jubin V Castelli M Katinka B Vacherie C Biémont Z Skalli L Cattolico J Poulain V De Berardinis C Cruaud S Duprat P Brottier JP Coutanceau J Gouzy G Parra G Lardier C Chapple KJ McKernan P McEwan S Bosak M Kellis JN Volff R Guigó MC Zody J Mesirov K Lindblad-Toh B Birren C Nusbaum D Kahn M Robinson-Rechavi V Laudet V Schachter F Quétier W Saurin C Scarpelli P Wincker ES Lander J Weissenbach H Roest Crollius 2004 Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype Nature 431 946 957 15496914 10.1038/nature03025
Kawashima T, Hojyo S, Nishimichi N, Sato M, Aosasa M, Horiuchi H, Furusawa S, Matsuda H (2005) Characterization and expression analysis of the chicken interleukin-11 receptor alpha chain. Dev Comp Immunol. 29:349-359
CF Lai J Ripperger KK Morella Y Wang DP Gearing GH Fey H Baumann 1995 Separate signaling mechanisms are involved in the control of STAT protein activation and gene regulation via the interleukin 6 response element by the box 3 motif of gp130 J Biol Chem 270 14847 14850 7797460 10.1074/jbc.270.25.14847 1:CAS:528:DyaK2MXmsFKqsr0%3D
LE Lee JH Clemons DG Bechtel SJ Caldwell KB Han M Pasitschniak-Arts DD Mosser NC Bols 1993 Development and characterization of a rainbow trout liver cell line expressing cytochrome P450-dependent monooxygenase activity Cell Biol Toxicol 9 279 294 8299006 10.1007/BF00755606 1:CAS:528:DyaK2cXhvVCrtbY%3D
JS Leong SG Jantzen KR von Schalburg GA Cooper AM Messmer NY Liao S Munro R Moore RA Holt SJ Jones WS Davidson BF Koop 2010 Salmo salar and Esox lucius full-length cDNA sequences reveal changes in evolutionary pressures on a post-tetraploidization genome BMC Genomics 11 279 20433749 10.1186/1471-2164-11- 279
C Liongue AC Ward 2007 Evolution of class I cytokine receptors BMC Evol Biol 7 120 17640376 10.1186/1471-2148-7-120
RL Moritz NE Hall LM Connolly RJ Simpson 2001 Determination of the disulfide structure and N-glycosylation sites of the extracellular domain of the human signal transducer gp130 J Biol Chem 276 8244 8253 11098061 10.1074/jbc.M009979200 1:CAS:528:DC%2BD3MXitFKgsbo%3D
M Murakami M Narazaki M Hibi H Yawata K Yasukawa M Hamaguchi T Taga T Kishimoto 1991 Critical cytoplasmic region of the interleukin 6 signal transducer gp130 is conserved in the cytokine receptor family Proc Natl Acad Sci USA 88 11349 11353 1662392 10.1073/pnas.88.24.11349 1:CAS:528: DyaK38XhtVCjurY%3D
Murray PJ (2007) The JAK-STAT signaling pathway: input and output integration. J Immunol 178:2623-2629
Nam BH, Byon JY, Kim YO, Park EM, Cho YC, Cheong J (2007) Molecular cloning and characterisation of the flounder (Paralichthys olivaceus) interleukin-6 gene Fish Shellfish Immunol 23:231-236
N Nishimichi T Kawashima S Hojyo H Horiuchi S Furusawa H Matsuda 2006 Characterization and expression analysis of a chicken interleukin-6 receptor alpha Dev Comp Immunol 30 419 429 16153708 10.1016/j.dci.2005.05.007 1:CAS:528:DC%2BD28XksFWr
N Nishimoto T Kishimoto 2006 Interleukin 6: from bench to bedside Nat Clin Pract Rheumatol 2 619 626 17075601 10.1038/ncprheum0338 1:CAS:528:DC%2BD28Xht1emtLnI
PC Heinrich I Behrmann G Müller-Newen F Schaper L Graeve 1998 Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway Biochem J 334 297 314 9716487 1:CAS:528:DyaK1cXmtFOls7c%3D
JW Oh M Revel J Chebath 1996 A soluble interleukin 6 receptor isolated from conditioned medium of human breast cancer cells is encoded by a differentially spliced mRNA Cytokine 8 401 409 8726669 10.1006/cyto.1996.0055 1:CAS:528:DyaK28XjtFOmtL4%3D
S Radtke S Wüller XP Yang BE Lippok B Mütze C Mais HS de Leur JG Bode M Gaestel PC Heinrich I Behrmann F Schaper HM Hermanns 2010 Cross-regulation of cytokine signalling: pro-inflammatory cytokines restrict IL-6 signalling through receptor internalisation and degradation J Cell Sci 1 23 947 959 10.1242/jcs.065326
M Saito K Yoshida M Hibi T Taga T Kishimoto 1992 Molecular cloning of a murine IL-6 receptor-associated signal transducer, gp130, and its regulated expression in vivo J Immunol 148 4066 4071 1602143 1:CAS:528:DyaK3sXitFWjtrY%3D
MD Santos M Yasuike H Kondo I Hirono T Aoki 2007 A novel type-1 cytokine receptor from fish involved in the Janus kinase/signal transducers and activators of transcription (Jak/STAT) signal pathway Mol Immunol 44 3355 3363 17383728 10.1016/j.molimm.2007.02.018 1:CAS:528:DC%2BD2sXkvFWntro%3D
MD Santos M Yasuike H Kondo I Hirono T Aoki 2008 Teleostean IL11b exhibits complementing function to IL11a and expansive involvement in antibacterial and antiviral responses Mol Immunol 45 3494 34501 18538848 10.1016/j.molimm.2008.02.004 1:CAS:528:DC%2BD1cXntFGnur4%3D
K Schirmer AG Chan BM Greenberg DG Dixon NC Bols 1998 Ability of 16 priority PAHs to be photocytotoxic to a cell line from the rainbow trout gill Toxicology 127 143 155 9699801 10.1016/S0300-483X(98)00031-6 1:CAS:528:DyaK1cXks1Omtrc%3D
JS Silver CA Hunter 2010 gp130 at the nexus of inflammation, autoimmunity and cancer J Leukoc Biol 88 1145 56 20610800 10.1189/jlb.0410217 1:CAS:528:DC%2BC3cXhsFGgtL3M
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution. doi: 10.1093/molbev/msr121
WCM Thabard MP Mellerin D Puthier S Barillé R Bataille M Amiot 2001 IL-6 upregulates its own receptor on some human myeloma cell lines Cytokine 14 352 356 11497497 10.1006/cyto.2001.0911 1:CAS:528:DC%2BD3MXlvVWgtrs%3D
JN Varghese RL Moritz MZ Lou A Van Donkelaar H Ji N Ivancic KM Branson NE Hall RJ Simpson 2002 Structure of the extracellular domains of the human interleukin-6 receptor alpha-chain Proc Natl Acad Sci USA 99 15959 15964 12461182 10.1073/pnas.232432399 1:CAS:528:DC%2BD38Xps1egu78%3D
P Vollmer B Oppmann N Voltz M Fischer S Rose-John 1999 A role for the immunoglobulin-like domain of the human IL-6 receptor. Intracellular protein transport and shedding Eur J Biochem 263 438 446 10406952 10.1046/j.1432-1327. 1999.00511.x 1:CAS:528:DyaK1MXltVert7g%3D
GH Waetzig A Chalaris P Rosenstiel J Suthaus C Holland N Karl L Vallés Uriarte A Till J Scheller J Grötzinger S Schreiber S Rose-John D Seegert 2010 N-linked glycosylation is essential for the stability but not the signalling function of the interleukin-6 signal transducer glycoprotein 130 J Biol Chem 285 1781 1789 19915009 10.1074/jbc.M109.075952 1:CAS:528:DC%2BC3cXjsVSlsA%3D%3D
T Wang JW Holland N Bols CJ Secombes 2005 Cloning and expression of the first nonmammalian interleukin-11 gene in rainbow trout Oncorhynchus mykiss Febs J272 1136 1147
Wang T, Holland JW, Carrington A, Zou J, Secombes CJ (2007) Molecular and functional characterization of IL-15 in rainbow trout Oncorhynchus mykiss: a potent inducer of IFN-gamma expression in spleen leukocytes. J Immunol. 179:1475-1488
Wang T, Hanington PC, Belosevic M, Secombes CJ (2008) Two macrophage colony-stimulating factor genes exist in fish that differ in gene organization and are differentially expressed. J Immunol 181: 3310-3322
Wang T, Diaz-Rosales P, Costa MM, Campbell S, Snow M, Collet B, Martin SAM, Secombes CJ (2011a) The first functional characterisation of a non-mammalian interleukin (IL)-21: Rainbow trout Oncorhynchus mykiss IL-21 up-regulates the expression of the T helper cell signature cytokines interferon-γ, IL-10 and IL-22. J Immunol. 186:708-721
Wang T, Huang W, Costa MM, Martin SA, Secombes C (2011b). 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 63:235-253
T Wang CJ Secombes 2009 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 46 2290 2298 19419770 10.1016/j.molimm.2009.04.003 1:CAS:528:DC%2BD1MXntFyns7g%3D
KQM Wolf 1962 Established eurythermic line of fish cells in vitro Science 135 1065 1066 14007940 10.1126/science.135.3508.1065 1:STN:280: DyaF387pvFymsg%3D%3D
YKN Xu CS Luo P Soo MJ Pocock PE Czabotar DJ Hilton NA Nicola TP Garrett JG Zhang 2010 Crystal structure of the entire ectodomain of gp130: insights into the molecular assembly of the tall cytokine receptor complexes J Biol Chem 285 21214 21218 20489211 10.1074/jbc.C110.129502 1:CAS:528:DC%2BC3cXos1WrsLw%3D
XG Zhang JJ Gu ZY Lu K Yasukawa GD Yancopoulos K Turner, et al. 1994 Ciliary neurotropic factor, interleukin 11, leukemia inhibitory factor, and oncostatin M are growth factors for human myeloma cell lines using the interleukin 6 signal transducer gp130 J Exp Med 179 1337 1342 8145045 10.1084/jem.179.4.1337 1:CAS:528:DyaK2cXhs1Wgt78%3D
