Growth hormone STAT5-mediated signaling and its modulation in mice liver during the growth period

Growth Hormone and IGF Research

Volumn 23, Issue 1-2, 2013, Pages 19-28

  Martinez, Carolina S ^a   Piazza, Verónica G ^a   Ratner, Laura D ^b   Matos, Marina N ^a   González, Lorena ^a   Rulli, Susana B ^b   Miquet, Johanna G ^a   Sotelo, Ana I ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

GH signaling; Growth; Liver; Mice; STAT5 modulation

Indexed keywords

GLUCOCORTICOID RECEPTOR; GROWTH FACTOR; HEPATOCYTE NUCLEAR FACTOR 1; JANUS KINASE 2; STAT5 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 2; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL TISSUE; ARTICLE; BODY GROWTH; CONTROLLED STUDY; FEMALE; GENE ACTIVATION; GROWTH CURVE; GROWTH PERIOD; GROWTH RATE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION;

AGE FACTORS; ANIMALS; CELL NUCLEUS; FEMALE; GROWTH AND DEVELOPMENT; GROWTH HORMONE; JANUS KINASE 2; LIVER; MALE; MICE; PHOSPHORYLATION; RECEPTORS, SOMATOTROPIN; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR;

EID: 84875407539     PISSN: 10966374     EISSN: 15322238     Source Type: Journal    
DOI: 10.1016/j.ghir.2012.11.002     Document Type: Article

References (74)

1. Brooks A.J., Waters M.J. The growth hormone receptor: mechanism of activation and clinical implications, nature reviews. Endocrinology 2010, 6:515-525.
2. Lanning N.J., Carter-Su C. Recent advances in growth hormone signaling. Rev. Endocr. Metab. Disord. 2006, 7:225-235.
3. Lichanska A.M., Waters M.J. New insights into growth hormone receptor function and clinical implications. Horm. Res. 2008, 69:138-145.
4. Barclay J.L., Nelson C.N., Ishikawa M., et al. GH-dependent STAT5 signaling plays an important role in hepatic lipid metabolism. Endocrinology 2011, 152:181-192.
5. Teglund S., McKay C., Schuetz E., et al. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 1998, 93:841-850.
6. Udy G.B., Towers R.P., Snell R.G., et al. Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:7239-7244.
7. Rotwein P. Mapping the growth hormone-Stat5b-IGF-I transcriptional circuit. Trends Endocrinol. Metab. 2012, 23:186-193.
8. Croker B.A., Kiu H., Nicholson S.E. SOCS regulation of the JAK/STAT signalling pathway. Semin. Cell Dev. Biol. 2008, 19:414-422.
9. Flores-Morales A., Greenhalgh C.J., Norstedt G., Rico-Bautista E. Negative regulation of growth hormone receptor signaling. Mol. Endocrinol. 2006, 20:241-253.
10. Greenhalgh C.J., Alexander W.S. Suppressors of cytokine signalling and regulation of growth hormone action. Growth Horm. IGF Res. 2004, 14:200-206.
11. Adams T.E., Hansen J.A., Starr R., Nicola N.A., Hilton D.J., Billestrup N. Growth hormone preferentially induces the rapid, transient expression of SOCS-3, a novel inhibitor of cytokine receptor signaling. J. Biol. Chem. 1998, 273:1285-1287.
12. Tollet-Egnell P., Flores-Morales A., Stavreus-Evers A., Sahlin L., Norstedt G. Growth hormone regulation of SOCS-2, SOCS-3, and CIS messenger ribonucleic acid expression in the rat. Endocrinology 1999, 140:3693-3704.
13. Pilecka I., Whatmore A., Hooft van Huijsduijnen R., Destenaves B., Clayton P. Growth hormone signalling: sprouting links between pathways, human genetics and therapeutic options. Trends Endocrinol. Metab. 2007, 18:12-18.
14. Aoki N., Matsuda T. A cytosolic protein-tyrosine phosphatase PTP1B specifically dephosphorylates and deactivates prolactin-activated STAT5a and STAT5b. J. Biol. Chem. 2000, 275:39718-39726.
15. Gu F., Dube N., Kim J.W., et al. Protein tyrosine phosphatase 1B attenuates growth hormone-mediated JAK2-STAT signaling. Mol. Cell. Biol. 2003, 23:3753-3762.
16. Pasquali C., Curchod M.L., Walchli S., et al. Identification of protein tyrosine phosphatases with specificity for the ligand-activated growth hormone receptor. Mol. Endocrinol. 2003, 17:2228-2239.
17. Pilecka I., Patrignani C., Pescini R., et al. Protein-tyrosine phosphatase H1 controls growth hormone receptor signaling and systemic growth. J. Biol. Chem. 2007, 282:35405-35415.
18. Hackett R.H., Wang Y.D., Sweitzer S., Feldman G., Wood W.I., Larner A.C. Mapping of a cytoplasmic domain of the human growth hormone receptor that regulates rates of inactivation of Jak2 and Stat proteins. J. Biol. Chem. 1997, 272:11128-11132.
19. Ram P.A., Waxman D.J. Interaction of growth hormone-activated STATs with SH2-containing phosphotyrosine phosphatase SHP1 and nuclear JAK2 tyrosine kinase. J. Biol. Chem. 1997, 272:17694-17702.
20. Kim S.O., Jiang J., Yi W., Feng G.S., Frank S.J. Involvement of the Src homology 2-containing tyrosine phosphatase SHP2 in growth hormone signaling. J. Biol. Chem. 1998, 273:2344-2354.
21. Stofega M.R., Herrington J., Billestrup N., Carter-Su C. Mutation of the SHP2 binding site in growth hormone (GH) receptor prolongs GH-promoted tyrosyl phosphorylation of GH receptor, JAK2, and STAT5B. Mol. Endocrinol. 2000, 14:1338-1350.
22. Murphy JM T.G., Hilton D.J., Greenhalgh C.J. The negative regulation of JAK/STAT signaling. Handbook of cell signaling 2010.
23. Xu D., Qu C.K. Protein tyrosine phosphatases in the JAK/STAT pathway. Front. Biosci. 2008, 13:4925-4932.
24. Engblom D., Kornfeld J.W., Schwake L., et al. Direct glucocorticoid receptor-Stat5 interaction in hepatocytes controls body size and maturation-related gene expression. Genes Dev. 2007, 21:1157-1162.
25. Tronche F., Opherk C., Moriggl R., et al. Glucocorticoid receptor function in hepatocytes is essential to promote postnatal body growth. Genes Dev. 2004, 18:492-497.
26. Lin W.Y., Hu Y.J., Lee Y.H. Hepatocyte nuclear factor-1alpha regulates glucocorticoid receptor expression to control postnatal body growth. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 295:G542-G551.
27. Lupu F., Terwilliger J.D., Lee K., Segre G.V., Efstratiadis A. Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev. Biol. 2001, 229:141-162.
28. Liu J.L., LeRoith D. Insulin-like growth factor I is essential for postnatal growth in response to growth hormone. Endocrinology 1999, 140:5178-5184.
29. Tang Z., Yu R., Lu Y., Parlow A.F., Liu J.L. Age-dependent onset of liver-specific IGF-I gene deficiency and its persistence in old age: implications for postnatal growth and insulin resistance in LID mice. Am. J. Physiol. Endocrinol. Metab. 2005, 289:E288-E295.
30. Zhang Y., Guan R., Jiang J., et al. Growth hormone (GH)-induced dimerization inhibits phorbol ester-stimulated GH receptor proteolysis. J. Biol. Chem. 2001, 276:24565-24573.
31. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
32. Kibbe W.A. OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res. 2007, 35:W43-W46.
33. Gatford K.L., Egan A.R., Clarke I.J., Owens P.C. Sexual dimorphism of the somatotrophic axis. J. Endocrinol. 1998, 157:373-389.
34. Wauthier V., Sugathan A., Meyer R.D., Dombkowski A.A., Waxman D.J. Intrinsic sex differences in the early growth hormone responsiveness of sex-specific genes in mouse liver. Mol. Endocrinol. 2010, 24:667-678.
35. Maes M., De Hertogh R., Watrin-Granger P., Ketelslegers J.M. Ontogeny of liver somatotropic and lactogenic binding sites in male and female rats. Endocrinology 1983, 113:1325-1332.
36. Tiong T.S., Herington A.C. Ontogeny of messenger RNA for the rat growth hormone receptor and serum binding protein. Mol. Cell. Endocrinol. 1992, 83:133-141.
37. Mathews L.S., Enberg B., Norstedt G. Regulation of rat growth hormone receptor gene expression. J. Biol. Chem. 1989, 264:9905-9910.
38. Ram P.A., Waxman D.J. Role of the cytokine-inducible SH2 protein CIS in desensitization of STAT5b signaling by continuous growth hormone. J. Biol. Chem. 2000, 275:39487-39496.
39. Waxman D.J., Ram P.A., Park S.H., Choi H.K. Intermittent plasma growth hormone triggers tyrosine phosphorylation and nuclear translocation of a liver-expressed, Stat 5-related DNA binding protein. Proposed role as an intracellular regulator of male-specific liver gene transcription. J. Biol. Chem. 1995, 270:13262-13270.
40. Thangavel C., Shapiro B.H. A molecular basis for the sexually dimorphic response to growth hormone. Endocrinology 2007, 148:2894-2903.
41. Miquet J.G., Giani J.F., Martinez C.S., et al. Prolonged exposure to GH impairs insulin signaling in the heart. J. Mol. Endocrinol. 2011, 47:167-177.
42. Zhang Y., Laz E.V., Waxman D.J. Dynamic, sex-differential STAT5 and BCL6 binding to sex-biased, growth hormone-regulated genes in adult mouse liver. Mol. Cell. Biol. 2012, 32:880-896.
43. Chia D.J., Varco-Merth B., Rotwein P. Dispersed chromosomal Stat5b-binding elements mediate growth hormone-activated insulin-like growth factor-I gene transcription. J. Biol. Chem. 2010, 285:17636-17647.
44. Paradis V., Dargere D., Vidaud M., et al. Expression of connective tissue growth factor in experimental rat and human liver fibrosis. Hepatology 1999, 30:968-976.
45. Torre C., Benhamouche S., Mitchell C., et al. The transforming growth factor-alpha and cyclin D1 genes are direct targets of beta-catenin signaling in hepatocyte proliferation. J. Hepatol. 2011, 55:86-95.
46. Eden S. Age- and sex-related differences in episodic growth hormone secretion in the rat. Endocrinology 1979, 105:555-560.
47. Mathews L.S., Hammer R.E., Brinster R.L., Palmiter R.D. Expression of insulin-like growth factor I in transgenic mice with elevated levels of growth hormone is correlated with growth. Endocrinology 1988, 123:433-437.
48. Butler A.A., LeRoith D. Minireview: tissue-specific versus generalized gene targeting of the igf1 and igf1r genes and their roles in insulin-like growth factor physiology. Endocrinology 2001, 142:1685-1688.
49. Hyatt M.A., Walker D.A., Stephenson T., Symonds M.E. Ontogeny and nutritional manipulation of the hepatic prolactin-growth hormone-insulin-like growth factor axis in the ovine fetus and in neonate and juvenile sheep. Proc. Nutr. Soc. 2004, 63:127-135.
50. Garcia-Aragon J., Lobie P.E., Muscat G.E., Gobius K.S., Norstedt G., Waters M.J. Prenatal expression of the growth hormone (GH) receptor/binding protein in the rat: a role for GH in embryonic and fetal development?. Development 1992, 114:869-876.
51. Pantaleon M., Whiteside E.J., Harvey M.B., Barnard R.T., Waters M.J., Kaye P.L. Functional growth hormone (GH) receptors and GH are expressed by preimplantation mouse embryos: a role for GH in early embryogenesis?. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:5125-5130.
52. Phornphutkul C., Frick G.P., Goodman H.M., Berry S.A., Gruppuso P.A. Hepatic growth hormone signaling in the late gestation fetal rat. Endocrinology 2000, 141:3527-3533.
53. Choi H.K., Waxman D.J. Plasma growth hormone pulse activation of hepatic JAK-STAT5 signaling: developmental regulation and role in male-specific liver gene expression. Endocrinology 2000, 141:3245-3255.
54. Matsumoto A., Seki Y., Kubo M., et al. Suppression of STAT5 functions in liver, mammary glands, and T cells in cytokine-inducible SH2-containing protein 1 transgenic mice. Mol. Cell. Biol. 1999, 19:6396-6407.
55. Landsman T., Waxman D.J. Role of the cytokine-induced SH2 domain-containing protein CIS in growth hormone receptor internalization. J. Biol. Chem. 2005, 280:37471-37480.
56. Gonzalez L., Miquet J.G., Sotelo A.I., Bartke A., Turyn D. Cytokine-inducible SH2 protein up-regulation is associated with desensitization of GH signaling in GHRH-transgenic mice. Endocrinology 2002, 143:386-394.
57. Miquet J.G., Sotelo A.I., Bartke A., Turyn D. Desensitization of the JAK2/STAT5 GH signaling pathway associated with increased CIS protein content in liver of pregnant mice. Am. J. Physiol. Endocrinol. Metab. 2005, 289:E600-E607.
58. Miquet J.G., Sotelo A.I., Bartke A., Turyn D. Suppression of growth hormone (GH) Janus tyrosine kinase 2/signal transducer and activator of transcription 5 signaling pathway in transgenic mice overexpressing bovine GH. Endocrinology 2004, 145:2824-2832.
59. Greenhalgh C.J., Metcalf D., Thaus A.L., et al. Biological evidence that SOCS-2 can act either as an enhancer or suppressor of growth hormone signaling. J. Biol. Chem. 2002, 277:40181-40184.
60. Metcalf D., Greenhalgh C.J., Viney E., et al. Gigantism in mice lacking suppressor of cytokine signalling-2. Nature 2000, 405:1069-1073.
61. Piessevaux J., Lavens D., Montoye T., et al. Functional cross-modulation between SOCS proteins can stimulate cytokine signaling. J. Biol. Chem. 2006, 281:32953-32966.
62. Tannahill G.M., Elliott J., Barry A.C., Hibbert L., Cacalano N.A., Johnston J.A. SOCS2 can enhance interleukin-2 (IL-2) and IL-3 signaling by accelerating SOCS3 degradation. Mol. Cell. Biol. 2005, 25:9115-9126.
63. Kornfeld J.W., Grebien F., Kerenyi M.A., et al. The different functions of Stat5 and chromatin alteration through Stat5 proteins. Front. Biosci. 2008, 13:6237-6254.
64. Escriva F., Gonzalez-Rodriguez A., Fernandez-Millan E., Rondinone C.M., Alvarez C., Valverde A.M. PTP1B deficiency enhances liver growth during suckling by increasing the expression of insulin-like growth factor-I. J. Cell. Physiol. 2010, 225:214-222.
65. Arrandale J.M., Gore-Willse A., Rocks S., et al. Insulin signaling in mice expressing reduced levels of Syp. J. Biol. Chem. 1996, 271:21353-21358.
66. Elchebly M., Payette P., Michaliszyn E., et al. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 1999, 283:1544-1548.
67. Umeda S., Beamer W.G., Takagi K., et al. Deficiency of SHP1 protein-tyrosine phosphatase activity results in heightened osteoclast function and decreased bone density. Am. J. Pathol. 1999, 155:223-233.
68. Iyer J., Reich N.C. Constitutive nuclear import of latent and activated STAT5a by its coiled coil domain. FASEB J. 2008, 22:391-400.
69. Zeng R., Aoki Y., Yoshida M., Arai K., Watanabe S. Stat5B shuttles between cytoplasm and nucleus in a cytokine-dependent and -independent manner. J. Immunol. 2002, 168:4567-4575.
70. Lee Y.H., Sauer B., Gonzalez F.J. Laron dwarfism and non-insulin-dependent diabetes mellitus in the HNF1alpha knockout mouse. Mol. Cell. Biol. 1998, 18:3059-3068.
71. Eleswarapu S., Jiang H. Growth hormone regulates the expression of hepatocyte nuclear factor-3 gamma and other liver-enriched transcription factors in the bovine liver. J. Endocrinol. 2005, 184:95-105.
72. Kaplan S.A., Cohen P. The somatomedin hypothesis 2007: 50 years later. J. Clin. Endocrinol. Metab. 2007, 92:4529-4535.
73. Klover P., Hennighausen L. Postnatal body growth is dependent on the transcription factors signal transducers and activators of transcription 5a/b in muscle: a role for autocrine/paracrine insulin-like growth factor I. Endocrinology 2007, 148:1489-1497.
74. Fan Y., Menon R.K., Cohen P., et al. Liver-specific deletion of the growth hormone receptor reveals essential role of growth hormone signaling in hepatic lipid metabolism. J. Biol. Chem. 2009, 284:19937-19944.