Growth impairment in IL-6-overexpressing transgenic mice is associated with induction of SOCS3 mRNA

Growth Hormone and IGF Research

Volumn 13, Issue 1, 2003, Pages 26-35

  Lieskovska, Jaroslava ^b   Guo, Donglin ^a,b   Derman, Eva ^b  

^a AMGEN INC   (United States)

^b PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Dwarfism; Growth hormone; IL 6; SOCS3; STAT3; STAT5; Transgenic mice

Indexed keywords

CYTOKINE; GROWTH HORMONE; INTERLEUKIN 6; MESSENGER RNA; STAT3 PROTEIN; STAT5 PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BRAIN; CELL PROLIFERATION; CONTROLLED STUDY; GENE INDUCTION; GENE LOCATION; GENE OVEREXPRESSION; GROWTH HORMONE BLOOD LEVEL; GROWTH RETARDATION; HORMONAL REGULATION; LIVER; LUNG; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SUPPRESSOR GENE; TRANSGENIC MOUSE;

EID: 0037292517     PISSN: 10966374     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1096-6374(02)00135-1     Document Type: Article

References (66)

1. K. Shahan, M. Gilmartin, E. Derman, Nucleotide sequences of liver, lachrymal, and submaxillary gland mouse major urinary protein mRNAs: mosaic structure and construction of panels of gene-specific synthetic oligonucleotide probes, Mol. Cell. Biol. 7 (1987) 1938-1946.
2. H.J. Son, K. Shahan, M. Rodriguez, E. Derman, F. Costantini, Identification of an enhancer required for the expression of a mouse major urinary protein gene in the submaxillary gland, Mol. Cell. Biol. 11 (1991) 4244-4252.
3. J. Lieskovska, D. Guo, E. Derman, IL-6 overexpression brings about growth impairment through perturbations of growth hormone (GH) signaling that includes a GH receptor defect, Growth Horm. IGF Res. 12 (2002) 388-398.
4. A. Efstratiadis, Genetics of mouse growth, Int. J. Dev. Biol. 42 (1998) 955-976.
5. Y. Zhou, B.C. Xu, H.G. Maheshwari, L. He, M. Reed, M. Lozykowski, S. Okada, L. Cataldo, K. Coschigamo, T.E. Wagner, G. Baumann, J.J. Kopchick, A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse), Proc. Natl. Acad. Sci. USA 94 (1997) 13215-13220.
6. J.C. Chow, P.R. Ling, Z. Qu, L. Laviola, A. Ciccarone, B.R. Bistrian, R.J. Smith, Growth hormone stimulates tyrosine phosphorylation of JAK2 and STAT5, but not insulin receptor substrate-1 or SHC proteins in liver and skeletal muscle of normal rats in vivo, Endocrinology 137 (1996) 2880-2886.
7. C. Carter-Su, L.S. Smit, Signaling via JAK tyrosine kinases: growth hormone receptor as a model system, Recent Prog. Horm. Res. 53 (1998) 61-82.
8. S. John, U. Vinkemeier, E. Soldaini, J.E. Darnell Jr., W.J. Leonard, The significance of tetramerization in promoter recruitment by Stat5, Mol. Cell. Biol. 19 (1999) 1910-1918.
9. H. Yasukawa, A. Sasaki, A. Yoshimura, Negative regulation of cytokine signaling pathways, Annu. Rev. Immunol. 18 (2000) 143-164.
10. X.P. Chen, J.A. Losman, P. Rothman, SOCS proteins, regulators of intracellular signaling, Immunity 13 (2000) 287-290.
11. C. Carter-Su, L. Rui, M.R. Stofega, SH2-B and SIRP: JAK2 binding proteins that modulate the actions of growth hormone, Recent Prog. Horm. Res. 55 (2000) 293-311.
12. D.J. Hilton, R.T. Richardson, W.S. Alexander, E.M. Viney, T.A. Willson, N.S. Sprigg, R. Starr, S.E. Nicholson, D. Metcalf, N.A. Nicola, Twenty proteins containing a C-terminal SOCS box form five structural classes, Proc. Natl. Acad. Sci. USA 95 (1998) 114- 119.
13. R. Starr, T.A. Willson, E.M. Viney, L.J. Murray, J.R. Rayner, B.J. Jenkins, T.J. Gonda, W.S. Alexander, D. Metcalf, N.A. Nicola, D.J. Hilton, A family of cytokine-inducible inhibitors of signalling, Nature 387 (1997) 917-921.
14. T. Naka, M. Narazaki, M. Hirata, T. Matsumoto, S. Minamoto, A. Aono, N. Nishimoto, T. Kajita, T. Taga, K. Yoshizaki, S. Akira, T. Kishimoto, Structure and function of a new STAT-induced STAT inhibitor, Nature 387 (1997) 924-929.
15. S. Diehl, J. Anguita, A. Hoffmeyer, T. Zapton, J.N. Ihle, E. Fikrig, M. Rincon, Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1, Immunity 13 (2000) 805-815.
16. S. Ito, P. Ansari, M. Sakatsume, H. Dickensheets, N. Vazquez, R.P. Donnelly, A.C. Larner, D.S. Finbloom, Interleukin-10 inhibits expression of both interferon α- and interferon γ-induced genes by suppressing tyrosine phosphorylation of STAT1, Blood 93 (1999) 1456-1463.
17. Y.R. Boisclair, J. Wang, J. Shi, K.R. Hurst, G.T. Ooi, Role of the suppressor of cytokine signaling-3 in mediating the inhibitory effects of interleukin-1β on the growth hormone-dependent transcription of the acid-labile subunit gene in liver cells, J. Biol. Chem. 275 (2000) 3841-3847.
18. C.J. Auernhammer, C. Bousquet, S. Melmed, Autoregulation of pituitary corticotroph SOCS-3 expression: characterization of the murine SOCS-3 promoter, Proc. Natl. Acad. Sci. USA 96 (1999) 6964-6969.
19. S. Teglund, C. McKay, E. Schuetz, J.M. van Deursen, D. Stravopodis, D. Wang, M. Brown, S. Bodner, G. Grosveld, J.N. Ihle, Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses, Cell 93 (1998) 841-850.
20. G.B. Udy, R.P. Towers, R.G. Snell, R.J. Wilkins, S.H. Park, P.A. Ram, D.J. Waxman, H.W. Davey, Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression, Proc. Natl. Acad. Sci. USA 94 (1997) 7239-7244.
21. N.A. Sims, P. Clement-Lacroix, F. Da Ponte, Y. Bouali, N. Binart, R. Moriggl, V. Goffin, K. Coschigano, M. Gaillard-Kelly, J. Kopchick, R. Baron, P.A. Kelly, Bone homeostasis in growth hormone receptor-null mice is restored by IGF-I but independent of Stat5, J. Clin. Invest. 106 (2000) 1095-1103.
22. C. Auffray, F. Rougeon, Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA, Eur. J. Biochem. 107 (1980) 303-314.
23. A. Matsumoto, Y. Seki, M. Kubo, S. Ohtsuka, A. Suzuki, I. Hayashi, K. Tsuji, T. Nakahata, M. Okabe, S. Yamada, A. Yoshimura, Suppression of STAT5 functions in liver, mammary glands, and T cells in cytokine-inducible SH2-containing protein 1 transgenic mice, Mol. Cell. Biol. 19 (1999) 6396-6407.
24. H.B. Sadowski, K. Shuai, J.E. Darnell Jr., M.Z. Gilman, A common nuclear signal transduction pathway activated by growth factor and cytokine receptors [see comments], Science 261 (1993) 1739-1744.
25. Z. Zhong, Z. Wen, J.E. Darnell Jr., Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6, Science 264 (1994) 95-98.
26. U.M. Wegenka, C. Lutticken, J. Buschmann, J. Yuan, F. Lottspeich, W. Muller-Esterl, C. Schindler, E. Roeb, P.C. Heinrich, F. Horn, The interleukin-6-activated acute-phase response factor is antigenically and functionally related to members of the signal transducer and activator of transcription (STAT) family, Mol. Cell. Biol. 14 (1994) 3186-3196.
27. S. Akira, Y. Nishio, M. Inoue, X.J. Wang, S. Wei, T. Matsusaka, K. Yoshida, T. Sudo, M. Naruto, T. Kishimoto, Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p9l-related transcription factor involved in the gp130-mediated signaling pathway, Cell 77 (1994) 63-71.
28. S. Akira, H. Isshiki, T. Sugita, O. Tanabe, S. Kinoshita, Y. Nishio, T. Nakajima, T. Hirano, T. Kishimoto, A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family, EMBO J. 9 (1990) 1897-1906.
29. V. Poli, F.P. Mancini, R. Cortese, IL-6DBP, a nuclear protein involved in interleukin-6 signal transduction, defines a new family of leucine zipper proteins related to C/EBP, Cell 63 (1990) 643-653.
30. R. Pine, Convergence of TNFα and IFNγ signalling pathways through synergistic induction of IRF-I/ISGF-2 is mediated by a composite GAS/κB promoter element, Nucleic Acids Res. 25 (1997) 4346-4354.
31. T.E. Adams, J.A. Hansen, R. Starr, N.A. Nicola, D.J. Hilton, N. Billestrup, Growth hormone preferentially induces the rapid, transient expression of SOCS-3, a novel inhibitor of cytokine receptor signaling, J. Biol. Chem. 273 (1998) 1285-1287.
32. J.A. Hansen, K. Lindberg, D.J. Hilton, J.H. Nielsen, N. Billestrup, Mechanism of inhibition of growth hormone receptor signaling by suppressor of cytokine signaling proteins, Mol. Endocrinol. 13 (1999) 1832-1843.
33. D.J. Waxman, P.A. Ram, S.H. Park, H.K. Choi, Intermittent plasma growth hormone triggers tyrosine phosphorylation and nuclear translocation of a liver-expressed, Stat5-related DNA binding protein. Proposed role as an intracellular regulator of male- specific liver gene transcription, J. Biol. Chem. 270 (1995) 13262-13270.
34. S.H. Park, X. Liu, L. Hennighausen, H.W. Davey, D.J. Waxman, Distinctive roles of STAT5a and STAT5b in sexual dimorphism of hepatic P450 gene expression. Impact of STAT5a gene disruption, J. Biol. Chem. 274 (1999) 7421-7430.
35. P.A. Ram, D.J. Waxman, SOCS/CIS protein inhibition of growth hormone-stimulated STAT5 signaling by multiple mechanisms, J. Biol. Chem. 274 (1999) 35553-35561.
36. K. Shahan, M. Denaro, M. Gilmartin, Y. Shi, E. Derman, Expression of six mouse major urinary protein genes in the mammary, parotid, sublingual, submaxillary, and lachrymal glands and in the liver, Mol. Cell. Biol. 7 (1987) 1947-1954,
37. E. Derman, Isolation of a cDNA clone for mouse urinary proteins: age- and sex-related expression of mouse urinary protein genes is transcriptionally controlled, Proc. Natl. Acad. Sci. USA 78 (1981) 5425-5429.
38. P.H. Shaw, W.A. Held, N.D. Hastie, The gene family for major urinary proteins: expression in several secretory tissues of the mouse, Cell 32 (1983) 755-761.
39. G. Norstedt, R. Palmiter, Secretory rhythm of growth hormone regulates sexual differentiation of mouse liver, Cell 4 (1984) 805-812.
40. P. Rotwein, Human growth disorders: molecular genetics of the growth hormone insulin-like growth factor I axis, Acta Paediatr. Suppl. 88 (1999) 148-151, discussion 152.
41. F. De Benedetti, T. Alonzi, A. Moretta, D. Lazzaro, P. Costa, V. Poli, A. Martini, G. Ciliberto, E. Fattori, Interleukin 6 causes growth impairment in transgenic mice through a decrease in insulin-like growth factor-I. A model for stunted growth in children with chronic inflammation, J. Clin. Invest. 99 (1997) 643-650.
42. A.G. Thomas, J.M. Holly, F. Taylor, V. Miller, Insulin like growth factor-I, insulin like growth factor binding protein-1, and insulin in childhood Crohn's disease, Gut 34 (1993) 944-947.
43. R.K. Menon, S. Arslanian, B. May, W.S. Cutfield, M.A. Sperling, Diminished growth hormone-binding protein in children with insulin-dependent diabetes mellitus, Clin. Endocrinol. Metab. 74 (1991) 934.
44. E.M. Hodson, A.S. Brown, L.P. Roy, A.R. Rosenberg, Insulin-like growth factor-1, growth hormone-dependent insulin-like growth factor-binding protein and growth in children with chronic renal failure, Pediatr. Nephrol. 6 (1992) 433-438.
45. A. Suzuki, T. Hanada, K. Mitsuyama, T. Yoshida, S. Kamizono, T. Hoshino, M. Kubo, A. Yamashita, M. Okabe, K. Takeda, S. Akira, S. Matsumoto, A. Toyonaga, M. Sata, A. Yoshimura, CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation, J. Exp. Med. 193 (2001) 471-481.
46. J.C. Marine, C. McKay, D. Wang, D.J. Topham, E. Parganas, H. Nakajima, H. Pendeville, H. Yasukawa, A. Sasaki, A. Yoshimura, J.N. Ihle, SOCS3 is essential in the regulation of fetal liver erythropoiesis, Cell 98 (1999) 617-627.
47. S. Moutoussamy, P.A. Kelly, J. Finidori, Growth-hormone-receptor and cytokine-receptor-family signaling, Eur. J. Biochem. 255 (1998) 1-11.
48. C. Bjorbak, H.J. Lavery, S.H. Bates, R.K. Olson, S.M. Davis, J.S. Flier, M.G. Myers Jr., SOCS3 mediates feedback inhibition of the leptin receptor via Tyr985, J. Biol. Chem. 275 (2000) 40649-40657.
49. S.E. Nicholson, D. De Souza, L.J. Fabri, J. Corbin, T.A. Willson, J.G. Zhang, A. Silva, M. Asimakis, A. Farley, A.D. Nash, D. Metcalf, D.J. Hilton, N.A. Nicola, M. Baca, Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130, Proc. Natl. Acad. Sci. USA 97 (2000) 6493-6498.
50. C.L. Yu, Y.J. Jin, S.J. Burakoff, Cytosolic tyrosine dephosphorylation of STAT5. Potential role of SHP-2 in STAT5 regulation, J. Biol. Chem. 275 (2000) 599-604.
51. M.R. Stofega, J. Herrington, N. Billestrup, C. Carter-Su, Mutation of the SHP-2 binding site in growth hormone (GH) receptor prolongs GH-promoted tyrosyl phosphorylation of GH receptor, JAK2, and STAT5B, Mol. Endocrinol. 14 (2000) 1338-1350.
52. T. Fukada, M. Hibi, Y. Yamanaka, M. Takahashi-Tezuka, Y. Fujitani, T. Yamaguchi, K. Nakajima, T. Hirano, Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: involvement of STAT3 in anti-apoptosis, Immunity 5 (1996) 449-460.
53. S.O. Kim, J. Jiang, W. Yi, G.S. Feng, S.J. Frank, Involvement of the Src homology 2-containing tyrosine phosphatase SHP-2 in growth hormone signaling, J. Biol. Chem. 273 (1998) 2344-2354.
54. R. Garcia, R. Jove, Activation of STAT transcription factors in oncogenic tyrosine kinase signaling, J. Biomed. Sci. 5 (1998) 79-85.
55. R.M. Weber-Nordt, R. Mertelsmann, J. Finke, The JAK-STAT pathway: signal transduction involved in proliferation, differentiation and transformation, Leuk. Lymphoma 28 (1998) 459-467.
56. J.F. Bromberg, M.H. Wrzeszczynska, G. Devgan, Y. Zhao, R.G. Pestell, C. Albanese, J.E. Darnell Jr., Stat3 as an oncogene, [published erratum appears in Cell1999 Oct 15;99(2):239,] Cell 98 (1999) 295-303.
57. B.F. DiCosmo, G.P. Geba, D. Picarella, J.A. Elias, J.A. Rankin, B.R. Stripp, J.A. Whitsett, R.A. Flavell, Airway epithelial cell expression of interleukin-6 in transgenic mice. Uncoupling of airway inflammation and bronchial hyperreactivity, J. Clin. Invest. 94 (1994) 2028-2035.
58. G. Luo, L. Yu-Lee, Stat5b inhibits NFκB-mediated signaling, Mol. Endocrinol. 14 (2000) 114-123.
59. S.A. Keller, E.J. Schattner, E. Cesarman, Inhibition of NF-κB induces apoptosis of KSHV-infected primary effusion lymphoma cells, Blood 96 (2000) 2537-2542.
60. S. Jeay, G.E. Sonenshein, P.A. Kelly, M.C. Postel-Vinay, E. Baixeras, Growth hormone exerts antiapoptotic and proliferative effects through two different pathways involving nuclear factor-κB and phosphatidylinositol 3-kinase, Endocrinology 142 (2001) 147-156.
61. B. Emanuelli, P. Peraldi, C. Filloux, D. Sawka-Verhelle, D. Hilton, E. Van Obberghen, SOCS-3 is an insulin-induced negative regulator of insulin signaling, J. Biol. Chem. 275 (2000) 15985-15991.
62. B.R. Dey, S.L. Spence, P. Nissley, R.W. Furlanetto, Interaction of human suppressor of cytokine signaling (SOCS)-2 with the insulin-like growth factor-I receptor, J. Biol. Chem. 273 (1998) 24095-24101.
63. L. Rui, M. Yuan, D. Frantz, S. Shoelson, M.F. White, SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2, J. Biol. Chem. (2002).
64. J. Baker, J.P. Liu, E.J. Robertson, A. Efstratiadis, Role of insulin-like growth factors in embryonic and postnatal growth, Cell 75 (1993) 73-82.
65. J.L. Liu, A. Grinberg, H. Westphal, B. Sauer, D. Accili, M. Karas, D. LeRoith, Insulin-like growth factor-I affects perinatal lethality and postnatal development in a gene dosage-dependent manner: manipulation using the Cre/loxP system in transgenic mice, Mol. Endocrinol. 12 (1998) 1452-1462.
66. J.L. Liu, D. LeRoith, Insulin-like growth factor I is essential for postnatal growth in response to growth hormone, Endocrinology 140 (1999) 5178-5184.