Hypothalamic STAT proteins: Regulation of somatostatin neurons by growth hormone via STAT5b

Journal of Neuroendocrinology

Volumn 17, Issue 3, 2005, Pages 186-194

  Bennett, E ^a   McGuinness, L ^b   Gevers, E F ^b   Thomas, G B ^b   Robinson, I C A F ^b   Davey, H W ^c   Luckman, Simon M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c RUAKURA RESEARCH CENTRE   (New Zealand)

Author keywords

Growth hormone; Signal transducers and activators of transcription (STATs); Somatostatin

Indexed keywords

GROWTH HORMONE; MESSENGER RNA; PROLACTIN; STAT PROTEIN; STAT5B PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; FEEDBACK SYSTEM; FEMALE; GROWTH HORMONE RELEASE; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MOUSE STRAIN; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; RAT STRAIN; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SOMATOSTATIN CELL;

ANIMALS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DWARFISM, PITUITARY; FEEDBACK, BIOCHEMICAL; FEMALE; GROWTH HORMONE; HYPOTHALAMUS; MALE; MICE; MICE, KNOCKOUT; MIDLINE THALAMIC NUCLEI; MILK PROTEINS; NEURONS; RATS; RATS, MUTANT STRAINS; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; SOMATOSTATIN; STAT5 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS;

EID: 17544372062     PISSN: 09538194     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2005.01296.x     Document Type: Article

References (54)

1. Darnell JE Jr. STATs and gene regulation. Science 1997; 277: 1630-1635.
2. Gronowski AM, Zhong Z, Wen Z, Thomas MJ, Darnell JE Jr, Rotwein P. In vivo growth hormone treatment rapidly stimulates the tyrosine phosphorylation and activation of Stat3. Mol Endocrinol 1995; 9: 171-177.
3. Waxman DJ, Ram PA, Park SH, Choi HK. 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.
4. Kazansky AV, Raught B, Lindsey SM, Wang YF, Rosen JM. Regulation of mammary gland factor/Stat5a during mammary gland development. Mol Endocrinol 1995; 9: 1598-1609.
5. Miller RJ, Bell GI. JAK/STAT cats the fat. Trends Neurosci 1996; 19: 159-161.
6. Argetsinger LS, Campbell GS, Yang X, Witthuhn BA, Silvennoinen O, Ihle JN, Carter-Su C. Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase. Cell 1993; 74: 237-244.
7. Ram PA, Park SH, Choi HK, Waxman DJ. Growth hormone activation of Stat 1, Stat 3, and Stat 5 in rat liver. Differential kinetics of hormone desensitization and growth hormone stimulation of both tyrosine phosphorylation and serine/threonine phosphorylation. J Biol Chem 1996; 271: 5929-5940.
8. Smit LS, Meyer DJ, Billestrup N, Norstedt G, Schwartz J, Carter-Su C. The role of the growth hormone (GH) receptor and JAK1 and JAK2 kinases in the activation of Stats 1, 3, and 5 by GH. Mol Endocrinol 1996; 10: 519-533.
9. Udy GB, Towers RP, Snell RG, Wilkins RJ, Park SH, Ram PA, Waxman DJ, Davey HW. Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc Natl Acad Sci USA 1997; 94: 7239-7244.
10. Davey HW, Park SH, Grattan DR, McLachlan MJ, Waxman DJ. STAT5b-deficient mice are growth hormone pulse-resistant. Role of STAT5b in sex-specific liver p450 expression. J Biol Chem 1999; 274: 35331-35336.
11. Soldaini E, John S, Moro S, Bollenbacher J, Schindler U, Leonard WJ. DNA binding site selection of dimeric and tetrameric Stat5 proteins reveals a large repertoire of divergent tetrameric Stat5a binding sites. Mol Cell Biol 2000; 20: 389-401.
12. Verdier F, Rabionet R, Gouilleux F, Beisenherz-Huss C, Varlet P, Muller O, Mayeux P, Lacombe C, Gisselbrecht S, Chretien S. A sequence of the CIS gene promoter interacts preferentially with two associated STAT5A dimers. a distinct biochemical difference between STAT5A and STAT5B. Mol Cell Biol 1998; 18: 5852-5860.
13. Yamashita H, Xu J, Erwin RA, Farrar WL, Kirken RA, Rui H. Differential control of the phosphorylation state of proline-juxtaposed serine residues Ser725 of Stat5a and Ser730 of Stat5b in prolactin-sensitive cells. J Biol Chem 1998; 273: 30218-30224.
14. Ripperger JA, Fritz S, Richter K, Hocke GM, Lottspeich F, Fey GH. Transcription factors Stat3 and Stat5b are present in rat liver nuclei late in an acute phase response and bind interleukin-6 response elements. J Biol Chem 1995; 270: 29998-30006.
15. Wang D, Stravopodis D, Teglund S, Kitazawa J, Ihle JN. Naturally occurring dominant negative variants of Stat5. Mol Cell Biol 1996; 16: 6141-6148.
16. Azam M, Lee C, Strehlow I, Schindler C. Functionally distinct isoforms of STAT5 are generated by protein processing. Immunity 1997; 6: 691-701.
17. Wakao H, Gouilleux F, Groner B. Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J 1994; 13: 2182-2191.
18. Liu X, Robinson GW, Wagner KU, Garrett L, Wynshaw-Boris A, Hennighausen L. Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev 1997; 11: 179-186.
19. Teglund S, McKay C, Schuetz E, van Deursen JM, Stravopodis D, Wang D, Brown M, Bodner S, Grosveld G, Ihle JN. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 1998; 93: 841-850.
20. Vaisse C, Halaas JL, Horvath CM, Darnell JE Jr, Stoffel M, Friedman JM. Leptin activation of Stat3 in the hypothalamus of wild-type and ob/ob mice but not db/db mice. Nature Genet 1996; 14: 95-97.
21. Hakansson M, de Lecea L, Sutcliffe JG, Yanagisawa M, Meister B. Leptin receptor- and STAT3-immunoreactivities in hypocretin/orexin neurones of the lateral hypothalamus. J Neuroendocrinol 1999; 11: 653-663.
22. Hakansson ML, Meister B. Transcription factor STAT3 in leptin target neurons of the rat hypothalamus. Neuroendocrinology 1998; 68: 420-427.
23. Jansson JO, Eden S, Isaksson O. Sexual dimorphism in the control of growth hormone secretion. Endocr Rev 1985; 6: 128-150.
24. Plotsky PM, Vale W. Patterns of growth hormone-releasing factor and somatostatin secretion into the hypophysial-portal circulation of the rat. Science 1985; 230: 461-463.
25. Kasting NW, Martin JB, Arnold MA. Pulsatile somatostatin release from the median eminence of the unanesthetized rat and its relationship to plasma growth hormone levels. Endocrinology 1981; 109: 1739-1745.
26. Burton KA, Kabigting EB, Clifton DK, Steiner RA. Growth hormone receptor messenger ribonucleic acid distribution in the adult male rat brain and its colocalization in hypothalamic somatostatin neurons. Endocrinology 1992; 131: 958-963.
27. Chihara K, Minamitani N, Kaji H, Arimura A, Fujita T. Intraventricularly injected growth hormone stimulates somatostatin release into rat hypophysial portal blood. Endocrinology 1981; 109: 2279-2281.
28. Rogers KV, Vician L, Steiner RA, Clifton DK. The effect of hypophysectomy and growth hormone administration on preprosomatostatin messenger ribonucleic acid in the periventricular nucleus of the rat hypothalamus. Endocrinology 1988; 122: 586-591.
29. Painson JC, Tannenbaum GS. Sexual dimorphism of somatostatin and growth hormone-releasing factor signaling in the control of pulsatile growth hormone secretion in the rat. Endocrinology 1991; 128: 2858-2866.
30. Sato M, Chihara K, Kita T, Kashio Y, Okimura Y, Kitajima N, Fujita T. Physiological role of somatostatin-mediated autofeedback regulation for growth hormone: importance of growth hormone in triggering somatostatin release during a trough period of pulsatile growth hormone release in conscious male rats. Neuroendocrinology 1989; 50: 139-151.
31. Swanson LW. Brain Maps: Structure of the Rat Brain, 2nd edn. Amsterdam: Elsevier, 1992.
32. Franklin KB, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. London: Academic Press, 1997.
33. Charlton HM, Clark RG, Robinson IC, Goff AE, Cox BS, Bugnon C, Bloch BA. Growth hormone-deficient dwarfism in the rat: a new mutation. J Endocrinol 1988; 119: 51-58.
34. Bennett PA, Levy A, Sophokleous S, Robinson IC, Lightman SL. Hypothalamic GH receptor gene expression in the rat: effects of altered GH status. J Endocrinol 1995; 147: 225-234.
35. Dickson SL, Luckman SM. Induction of c-fos messenger ribonucleic acid in neuropeptide Y and growth hormone (GH)-releasing factor neurons in the rat arcuate nucleus following systemic injection of the GH secretagogue, GH-releasing peptide-6. Endocrinology 1997; 138: 771-777.
36. Silverman AJ, Zimmerman EA. Magnocellular neurosecretory system. Annu Rev Neurosci 1983; 6: 357-380.
37. Wheeler TT, Broadhurst MK, Sadowski HB, Farr VC, Prosser CG. Stat5 phosphorylation status and DNA-binding activity in the bovine and murine mammary glands. Mol Cell Endocrinol 2001; 176: 39-48.
38. Arbogast LA, Voogt JL. Prolactin (PRL) receptors are colocalized in dopaminergic neurons in fetal hypothalamic cell cultures: effect of PRL on tyrosine hydroxylase activity. Endocrinology 1997; 138: 3016-3023.
39. Demarest KT, Riegle GD, Moore KE. Prolactin-induced activation of tuberoinfundibular dopaminergic neurons: evidence for both a rapid 'tonic' and a delayed 'induction' component. Neuroendocrinology 1984; 38: 467-475.
40. Arbogast LA, Voogt JL. Hyperprolactinemia increases and hypoprolactinemia decreases tyrosine hydroxylase messenger ribonucleic acid levels in the arcuate nuclei, but not the substantia nigra or zona incerta. Endocrinology 1991; 128: 997-1005.
41. Choi HK, Waxman DJ. Growth hormone, but not prolactin, maintains, low-level activation of STAT5a and STAT5b in female rat liver. Endocrinology 1999; 140: 5126-5135.
42. Argente J, Chowen JA, Zeitler P, Clifton DK, Steiner RA. Sexual dimorphism of growth hormone-releasing hormone and somatostatin gene expression in the hypothalamus of the rat during development. Endocrinology 1991; 128: 2369-2375.
43. MacLeod JN, Pampori NA, Shapiro BH. Sex differences in the ultradian pattern of plasma growth hormone concentrations in mice. J Endocrinol 1991; 131: 395-399.
44. Legraverend C, Mode A, Wells T, Robinson I, Gustafsson JA. Hepatic steroid hydroxylating enzymes are controlled by the sexually dimorphic pattern of growth hormone secretion in normal and dwarf rats. FASEB J 1992; 6: 711-718.
45. Aguilar RC, Fernandez HN, Dellacha JM, Calandra RS, Bartke A, Ghosh PK, Turyn D. Somatotropic and lactotropic receptors in transgenic mice expressing human or bovine growth hormone genes. Transgenic Res 1992; 1: 221-227.
46. Aguila MC, McCann SM. Growth hormone increases somatostatin release and messenger ribonucleic acid levels in the rat hypothalamus. Brain Res 1993; 623: 89-94.
47. Grattan DR, Xu J, McLachlan MJ, Kokay IC, Bunn SJ, Hovey RC, Davey HW. Feedback regulation of PRL secretion is mediated by the transcription factor, signal transducer, and activator of transcription 5b. Endocrinology 2001; 142: 3935-3940.
48. Montminy M, Brindle P, Arias J, Ferreri K, Armstrong R. Regulation of somatostatin gene transcription by cAMP. Adv Pharmacol 1996; 36: 1-13.
49. Pfitzner E, Jahne R, Wissler M, Stoecklin E, Groner B. p300/CREB-binding protein enhances the prolactin-mediated transcriptional induction through direct interaction with the transactivation domain of Stat5, but does not participate in the Stat5-mediated suppression of the glucocorticoid response. Mol Endocrinol 1998; 12: 1582-1593.
50. Stoecklin E, Wissler M, Schaetzle D, Pfitzner E, Groner B. Interactions in the transcriptional regulation exerted by Stat5 and by members of the steroid hormone receptor family. J Steroid Biochem Mol Biol 1999; 69: 195-204.
51. Jansson JO, Frohman LA. Differential effects of neonatal and adult androgen exposure on the growth hormone secretory pattern in male rats. Endocrinology 1987; 120: 1551-1557.
52. Chowen JA, Argente J, Gonzalez-Parra S, Garcia-Segura LM. Differential effects of the neonatal and adult sex steroid environments on the organization and activation of hypothalamic growth hormone-releasing hormone and somatostatin neurons. Endocrinology 1993; 133: 2792-2802.
53. Herbison AE. Sexually dimorphic expression of androgen receptor immunoreactivity by somatostatin neurones in rat hypothalamic periventricular nucleus and bed nucleus of the stria terminalis. J Neuroendocrinol 1995; 7: 543-553.
54. Park SH, Liu X, Hennighausen L, Davey HW, Waxman DJ. Distinctive roles of STAT5a and STAT5b in sexual dimorphism of hepatic P450 gene expression. Impact of STAT5a gene disruption. J Biol Chem 1999; 274: 7421-7430.