Molecular characterization of two suppressor of cytokine signaling 1 genes (SOCS1a and SOCS1b) in chickens
Xue XU, Jiannan ZHANG, Juan LI, Yajun WANG
Molecular characterization of two suppressor of cytokine signaling 1 genes (SOCS1a and SOCS1b) in chickens
Suppressor of cytokine signaling 1 (SOCS1) protein can inhibit the signal transduction triggered by some cytokines or hormones and thus are important in many physiological/pathological processes, including innate and adaptive immunity, inflammation, and development in mammals. However, there is sparse information about their structure, tissue expression, in birds, where their biological functions remain unknown. In this study, we cloned and characterized two SOCS1 genes (named cSOCS1a and cSOCS1b) from chickens. SOCS1a is predicted to encode a 207-amino acid protein, which shares high amino acid sequence identity (64%–67%) with human and mouse SOCS1. Besides SOCS1a, a novel SOCS1b gene was also identified in chickens and other non-mammalian vertebrates including Xenopus tropicalis. Chicken SOCS1b is predicted to encode a 212-amino acid protein, which shares only 30%–32% amino acid sequence identity with human SOCS1 and cSOCS1a. RT-PCR assay revealed that both cSOCS1a and cSOCS1b are widely expressed in all chicken tissues. Using a luciferase reporter assay system, we further demonstrated that transient expression of cSOCS1a and cSOCS1b can significantly inhibit chicken growth hormone (GH)- or prolactin (PRL)-induced luciferase activities of Hep G2 cells expressing cGH receptor (or cPRL receptor), indicating that SOCS1a and SOCS1b proteins can negatively regulate GH/PRL signaling. Taken together, these data suggest that both cSOCS1a and cSOCS1b may function as negative regulators of cytokine/hormone actions, such as modulation of GH/PRL actions in chickens.
chicken / SOCS1a / SOCS1b / growth hormone / prolactin
[1] |
Krebs D L, Hilton D J. SOCS: physiological suppressors of cytokine signaling. Journal of Cell Science, 2000, 113(Pt 16): 2813-2819
Pubmed
|
[2] |
Alexander W S. Suppressors of cytokine signalling (SOCS) in the immune system. Nature Reviews Immunology, 2002, 2(6): 410-416
Pubmed
|
[3] |
Naka T, Narazaki M, Hirata M, Matsumoto T, Minamoto S, Aono A, Nishimoto N, Kajita T, Taga T, Yoshizaki K, Akira S, Kishimoto T. Structure and function of a new STAT-induced STAT inhibitor. Nature, 1997, 387(6636): 924-929
CrossRef
Pubmed
Google scholar
|
[4] |
Endo T A, Masuhara M, Yokouchi M, Suzuki R, Sakamoto H, Mitsui K, Matsumoto A, Tanimura S, Ohtsubo M, Misawa H, Miyazaki T, Leonor N, Taniguchi T, Fujita T, Kanakura Y, Komiya S, Yoshimura A. A new protein containing an SH2 domain that inhibits JAK kinases. Nature, 1997, 387(6636): 921-924
CrossRef
Pubmed
Google scholar
|
[5] |
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(6636): 917-921
CrossRef
Pubmed
Google scholar
|
[6] |
Yasukawa H, Misawa H, Sakamoto H, Masuhara M, Sasaki A, Wakioka T, Ohtsuka S, Imaizumi T, Matsuda T, Ihle J N, Yoshimura A. The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO Journal, 1999, 18(5): 1309-1320
CrossRef
Pubmed
Google scholar
|
[7] |
Nicholson S E, Hilton D J. The SOCS proteins: a new family of negative regulators of signal transduction. Journal of Leukocyte Biology, 1998, 63(6): 665-668
Pubmed
|
[8] |
Hilton D J, Richardson R T, Alexander W S, Viney E M, Willson T A, Sprigg N S, Starr R, Nicholson S E, Metcalf D, Nicola N A. Twenty proteins containing a C-terminal SOCS box form five structural classes. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(1): 114-119
CrossRef
Pubmed
Google scholar
|
[9] |
Zhang J G, Metcalf D, Rakar S, Asimakis M, Greenhalgh C J, Willson T A, Starr R, Nicholson S E, Carter W, Alexander W S, Hilton D J, Nicola N A. The SOCS box of suppressor of cytokine signaling-1 is important for inhibition of cytokine action in vivo. Proceedings of the National Academy of Sciences of the United States of America, 2001, 98(23): 13261-13265
CrossRef
Pubmed
Google scholar
|
[10] |
Kamura T, Maenaka K, Kotoshiba S, Matsumoto M, Kohda D, Conaway R C, Conaway J W, Nakayama K I. VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes & Development, 2004, 18(24): 3055-3065
CrossRef
Pubmed
Google scholar
|
[11] |
Yoshimura A, Naka T, Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nature Reviews Immunology, 2007, 7(6): 454-465
CrossRef
Pubmed
Google scholar
|
[12] |
Marine J C, Topham D J, McKay C, Wang D, Parganas E, Stravopodis D, Yoshimura A, Ihle J N. SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell, 1999, 98(5): 609-616
CrossRef
Pubmed
Google scholar
|
[13] |
Naka T, Matsumoto T, Narazaki M, Fujimoto M, Morita Y, Ohsawa Y, Saito H, Nagasawa T, Uchiyama Y, Kishimoto T. Accelerated apoptosis of lymphocytes by augmented induction of Bax in SSI-1 (STAT-induced STAT inhibitor-1) deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(26): 15577-15582
CrossRef
Pubmed
Google scholar
|
[14] |
Starr R, Metcalf D, Elefanty A G, Brysha M, Willson T A, Nicola N A, Hilton D J, Alexander W S. Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(24): 14395-14399
CrossRef
Pubmed
Google scholar
|
[15] |
Hansen J A, Lindberg K, Hilton D J, Nielsen J H, Billestrup N. Mechanism of inhibition of growth hormone receptor signaling by suppressor of cytokine signaling proteins. Molecular Endocrinology, 1999, 13(11): 1832-1843
CrossRef
Pubmed
Google scholar
|
[16] |
Pezet A, Favre H, Kelly P A, Edery M. Inhibition and restoration of prolactin signal transduction by suppressors of cytokine signaling. The Journal of Biological Chemistry, 1999, 274(35): 24497-24502
CrossRef
Pubmed
Google scholar
|
[17] |
Huang G, He C, Meng F, Li J, Zhang J, Wang Y. Glucagon-like peptide (GCGL) is a novel potential TSH-releasing factor (TRF) in Chickens: I) Evidence for its potent and specific action on stimulating TSH mRNA expression and secretion in the pituitary. Endocrinology, 2014, 155(11): 4568-4580
CrossRef
Pubmed
Google scholar
|
[18] |
Jin H J, Xiang L X, Shao J Z. Identification and characterization of suppressor of cytokine signaling 1 (SOCS-1) homologues in teleost fish. Immunogenetics, 2007, 59(8): 673-686
CrossRef
Pubmed
Google scholar
|
[19] |
Jin H J, Shao J Z, Xiang L X, Wang H, Sun L L. Global identification and comparative analysis of SOCS genes in fish: insights into the molecular evolution of SOCS family. Molecular Immunology, 2008, 45(5): 1258-1268
CrossRef
Pubmed
Google scholar
|
[20] |
Nie L, Xiong R, Zhang Y S, Zhu L Y, Shao J Z, Xiang L X. Conserved inhibitory role of teleost SOCS-1s in IFN signaling pathways. Developmental and Comparative Immunology, 2014, 43(1): 23-29
CrossRef
Pubmed
Google scholar
|
[21] |
Skjesol A, Liebe T, Iliev D B, Thomassen E I, Tollersrud L G, Sobhkhez M, Lindenskov Joensen L, Secombes C J, Jørgensen J B. Functional conservation of suppressors of cytokine signaling proteins between teleosts and mammals: Atlantic salmon SOCS1 binds to JAK/STAT family members and suppresses type I and II IFN signaling. Developmental and Comparative Immunology, 2014, 45(1): 177-189
CrossRef
Pubmed
Google scholar
|
[22] |
Bu G, Ying Wang C, Cai G, Leung F C, Xu M, Wang H, Huang G, Li J, Wang Y. Molecular characterization of prolactin receptor (cPRLR) gene in chickens: gene structure, tissue expression, promoter analysis, and its interaction with chicken prolactin (cPRL) and prolactin-like protein (cPRL-L). Molecular and Cellular Endocrinology, 2013, 370(1-2): 149-162
CrossRef
Pubmed
Google scholar
|
[23] |
Cocolakis E, Dai M, Drevet L, Ho J, Haines E, Ali S, Lebrun J J. Smad signaling antagonizes STAT5-mediated gene transcription and mammary epithelial cell differentiation. The Journal of Biological Chemistry, 2008, 283(3): 1293-1307
CrossRef
Pubmed
Google scholar
|
[24] |
Bu G, Huang G, Fu H, Li J, Huang S, Wang Y. Characterization of the novel duplicated PRLR gene at the late-feathering K locus in Lohmann chickens. Journal of Molecular Endocrinology, 2013, 51(2): 261-276
CrossRef
Pubmed
Google scholar
|
[25] |
Frantsve J, Schwaller J, Sternberg D W, Kutok J, Gilliland D G. Socs-1 inhibits TEL-JAK2-mediated transformation of hematopoietic cells through inhibition of JAK2 kinase activity and induction of proteasome-mediated degradation. Molecular and Cellular Biology, 2001, 21(10): 3547-3557
CrossRef
Pubmed
Google scholar
|
[26] |
Waiboci L W, Ahmed C M, Mujtaba M G, Flowers L O, Martin J P, Haider M I, Johnson H M. Both the suppressor of cytokine signaling 1 (SOCS-1) kinase inhibitory region and SOCS-1 mimetic bind to JAK2 autophosphorylation site: implications for the development of a SOCS-1 antagonist. Journal of Immunology, 2007, 178(8): 5058-5068
CrossRef
Pubmed
Google scholar
|
[27] |
Bullock A N, Debreczeni J E, Edwards A M, Sundström M, Knapp S. Crystal structure of the SOCS2-elongin C-elongin B complex defines a prototypical SOCS box ubiquitin ligase. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(20): 7637-7642
CrossRef
Pubmed
Google scholar
|
[28] |
Van de Peer Y, Maere S, Meyer A. The evolutionary significance of ancient genome duplications. Nature Reviews Genetics, 2009, 10(10): 725-732
CrossRef
Pubmed
Google scholar
|
[29] |
Meyer A, Van de Peer Y. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology. 2005, 27(9): 937-45
|
[30] |
Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly P A. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocrine Reviews, 1998, 19(3): 225-268
CrossRef
Pubmed
Google scholar
|
[31] |
Harvey S, Gineste C, Gaylinn B D. Growth hormone (GH)-releasing activity of chicken GH-releasing hormone (GHRH) in chickens. General and Comparative Endocrinology, 2014, 204: 261-266
CrossRef
Pubmed
Google scholar
|
[32] |
Studzinski A L, Almeida D V, Lanes C F, Figueiredo M A, Marins L F. SOCS1 and SOCS3 are the main negative modulators of the somatotrophic axis in liver of homozygous GH-transgenic zebrafish (Danio rerio). General and Comparative Endocrinology, 2009, 161(1): 67-72
CrossRef
Pubmed
Google scholar
|
/
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