Sex-dependent liver gene expression is extensive and largely dependent upon signal transducer and activator of transcription 5b (STAT5b): STAT5b-dependent activation of male genes and repression of female genes revealed by microarray analysis

Molecular Endocrinology

Volumn 20, Issue 6, 2006, Pages 1333-1351

  Clodfelter, Karl H ^a   Holloway, Minita G ^a   Hodor, Paul ^b   Park, Soo Hee ^a   Ray, William J ^b   Waxman, David J ^a  

^a Boston University   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; STAT5B PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE REPRESSION; GENETIC TRANSCRIPTION; GENOTYPE; HYBRIDIZATION; LIVER; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RNA ISOLATION; SEX DIFFERENCE; UNINDEXED SEQUENCE; UPREGULATION;

ANIMALS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIVER; MALE; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRESSOR PROTEINS; SEX CHARACTERISTICS; STAT5 TRANSCRIPTION FACTOR;

MAMMALIA;

EID: 33744497029     PISSN: 08888809     EISSN: 08888809     Source Type: Journal    
DOI: 10.1210/me.2005-0489     Document Type: Article

References (59)

1. Horvath CM 2000 STAT proteins and transcriptional responses to extracellular signals. Trends Biochem Sci 25:496-502
2. Darnell Jr JE 1997 STATs and gene regulation. Science 277:1630-1635
3. Grimley PM, Dong F, Rui H 1999 Stat5a and Stat5b: fraternal twins of signal transduction and transcriptional activation. Cytokine Growth Factor Rev 10:131-157
4. Frank SJ 2001 Growth hormone signalling and its regulation: preventing too much of a good thing. Growth Horm IGF Res 11:201-212
5. Lin JX, Leonard WJ 2000 The role of Stat5a and Stat5b in signaling by IL-2 family cytokines. Oncogene 19:2566-2576
6. Herrington J, Carter-Su C 2001 Signaling pathways activated by the growth hormone receptor. Trends Endocrinol Metab 12:252-257
7. Veldhuis JD, Anderson SM, Shah N, Bray M, Vick T, Gentili A, Mulligan T, Johnson ML, Weltman A, Evans WS, Iranmanesh A 2001 Neurophysiological regulation and target-tissue impact of the pulsatile mode of growth hormone secretion in the human. Growth Horm IGF Res 11(Suppl A):S25-S37
8. Jansson JO, Eden S, Isaksson O 1985 Sexual dimorphism in the control of growth hormone secretion. Endocr Rev 6:128-150
9. Wiwi CA, Waxman DJ 2004 Role of hepatocyte nuclear factors in growth hormone-regulated, sexually dimorphic expression of liver cytochromes P450. Growth Factors 22:79-88
10. MacLeod JN, Pampori NA, Shapiro BH 1991 Sex differences in the ultradian pattern of plasma growth hormone concentrations in mice. J Endocrinol 131:395-399
11. Legraverend C, Mode A, Westin S, Strom A, Eguchi H, Zaphiropoulos PG, Gustafsson JA 1992 Transcriptional regulation of rat P-450 2C gene subfamily members by the sexually dimorphic pattern of growth hormone secretion. Mol Endocrinol 6:259-266
12. Sundseth SS, Alberta JA, Waxman DJ 1992 Sex-specific, growth hormone-regulated transcription of the cytochrome P450 2C11 and 2C12 genes. J Biol Chem 267:3907-3914
13. Waxman DJ, O'Connor C 16 March 2006 Growth hormone regulation of sex-dependent liver gene expression. Mol Endocrinol doi: 10.1210/me.2006-0007 (http://mend.endojournals.org/cgi/content/abstract/me.2006-0007v1)
14. Waxman DJ, Ram PA, Park SH, Choi HK 1995 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 270:13262-13270
15. Choi HK, Waxman DJ 1999 Growth hormone, but not prolactin, maintains, low-level activation of STAT5a and STAT5b in female rat liver. Endocrinology 140:5126-5135
16. Choi HK, Waxman DJ 2000 Plasma growth hormone pulse activation of hepatic JAK-STAT5 signaling: developmental regulation and role in male-specific liver gene expression. Endocrinology 141:3245-3255
17. Tannenbaum GS, Choi HK, Gurd W, Waxman DJ 2001 Temporal relationship between the sexually dimorphic spontaneous GH secretory profiles and hepatic STAT5 activity. Endocrinology 142:4599-4606
18. Sueyoshi T, Yokomori N, Korach KS, Negishi M 1999 Developmental action of estrogen receptor-α feminizes the growth hormone-Stat5b pathway and expression of Cyp2a4 and Cyp2d9 genes in mouse liver. Mol Pharmacol 56:473-477
19. Waxman DJ 2000 Growth hormone pulse-activated STAT5 signalling: a unique regulatory mechanism governing sexual dimorphism of liver gene expression. Novartis Found Symp 227:61-74; discussion 75-81
20. Holloway MG, Laz EV, Waxman DJ 2006 Codependence of GH-responsive, sexually dimorphic hepatic gene expression on signal transducer and activator of transcription 5b and hepatic nuclear factor 4α. Mol Endocrinol 20:647-660
21. Teglund S, McKay C, Schuetz E, van Deursen JM, Stravopodis D, Wang D, Brown M, Bodner S, Grosveld G, Ihle JN 1998 Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 93:841-850
22. Udy GB, Towers RP, Snell RG, Wilkins RJ, Park SH, Ram PA, Waxman DJ, Davey HW 1997 Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc Natl Acad Sci USA 94:7239-7244
23. Flores-Morales A, Stahlberg N, Tollet-Egnell P, Lundeberg J, Malek RL, Quackenbush J, Lee NH, Norstedt G 2001 Microarray analysis of the in vivo effects of hypophysectomy and growth hormone treatment on gene expression in the rat. Endocrinology 142:3163-3176
24. Gardmo C, Swerdlow H, Mode A 2002 Growth hormone regulation of rat liver gene expression assessed by SSH and microarray. Mol Cell Endocrinol 190:125-133
25. Lu C, Kasik J, Stephan DA, Yang S, Sperling MA, Menon RK 2001 Grtp1, a novel gene regulated by growth hormone. Endocrinology 142:4568-4571
26. Olsson B, Bohlooly YM, Brusehed O, Isaksson OG, Ahren B, Olofsson SO, Oscarsson J, Tornell J 2003 Bovine growth hormone-transgenic mice have major alterations in hepatic expression of metabolic genes. Am J Physiol Endocrinol Metab 285:E504-E511
27. Amador-Noguez D, Zimmerman J, Venable S, Darlington G 2005 Gender-specific alterations in gene expression and loss of liver sexual dimorphism in the long-lived Ames dwarf mice. Biochem Biophys Res Commun 332:1086-1100
28. Amador-Noguez D, Yagi K, Venable S, Darlington G 2004 Gene expression profile of long-lived Ames dwarf mice and Little mice. Aging Cell 3:423-441
29. Ahluwalia A, Clodfelter KH, Waxman DJ 2004 Sexual dimorphism of rat liver gene expression: regulatory role of growth hormone revealed by deoxyribonucleic acid microarray analysis. Mol Endocrinol 18:747-760
30. Stahlberg N, Merino R, Hernandez LH, Fernandez-Perez L, Sandelin A, Engstrom P, Tollet-Egnell P, Lenhard B, Flores-Morales A 2005 Exploring hepatic hormone actions using a compilation of gene expression profiles. BMC Physiol 5:8
31. Thompson BJ, Shang CA, Waters MJ 2000 Identification of genes induced by growth hormone in rat liver using cDNA arrays. Endocrinology 141:4321-4324
32. Laz EV, Wiwi CA, Waxman DJ 2004 Sexual dimorphism of rat liver nuclear proteins: regulatory role of growth hormone. Mol Cell Proteomics 3:1170-1180
33. Shahan K, Denaro M, Gilmartin M, Shi Y, Derman E 1987 Expression of six mouse major urinary protein genes in the mammary, parotid, sublingual, submaxillary, and lachrymal glands and in the liver. Mol Cell Biol 7:1947-1954
34. Held WA, Gallagher JF, Hohman CM, Kuhn NJ, Sampsell BM, Hughes Jr RG 1987 Identification and characterization of functional genes encoding the mouse major urinary proteins. Mol Cell Biol 7:3705-3712
35. Clark AJ, Chave-Cox A, Ma X, Bishop JO 1985 Analysis of mouse major urinary protein genes: variation between the exonic sequences of group 1 genes and a comparison with an active gene out with group 1 both suggest that gene conversion has occurred between MUP genes. EMBO J 4:3167-3171
36. Wiwi CA, Gupte M, Waxman DJ 2004 Sexually dimorphic P450 gene expression in liver-specific hepatocyte nuclear factor 4α-deficient mice. Mol Endocrinol 18:1975-1987
37. Lakso M, Masaki R, Noshiro M, Negishi M 1991 Structures and characterization of sex-specific mouse cytochrome P-450 genes as members within a large family. Duplication boundary and evolution. Eur J Biochem 195:477-486
38. Akinola LA, Poutanen M, Vihko R 1996 Cloning of rat 17β- hydroxysteroid dehydrogenase type 2 and characterization of tissue distribution and catalytic activity of rat type 1 and type 2 enzymes. Endocrinology 137:1572-1579
39. Crabb DW, Roepke J 1987 Loss of growth hormone-dependent characteristics of rat hepatocytes in culture. In Vitro Cell Dev Biol 23:303-307
40. Robertson JA, Haldosen LA, Wood TJ, Steed MK, Gustafsson JA 1990 Growth hormone pretranslationally regulates the sexually dimorphic expression of the prolactin receptor gene in rat liver. Mol Endocrinol 4:1235-1239
41. Klaassen CD, Liu L, Dunn II RT 1998 Regulation of sulfotransferase mRNA expression in male and female rats of various ages. Chem Biol Interact 109:299-313
42. McLellan LI, Hayes JD 1987 Sex-specific constitutive expression of the pre-neoplastic marker glutathione S-transferase, YfYf, in mouse liver. Biochem J 245:399-406
43. Heng YM, Kuo CS, Jones PS, Savory R, Schulz RM, Tomlinson SR, Gray TJ, Bell DR 1997 A novel murine P-450 gene, Cyp4a14, is part of a cluster of Cyp4a and Cyp4b, but not of CYP4F, genes in mouse and humans. Biochem J 325:741-749
44. Li-Hawkins J, Lund EG, Bronson AD, Russell DW 2000 Expression cloning of an oxysterol 7α-hydroxylase selective for 24-hydroxycholesterol. J Biol Chem 275:16543-16549
45. Bergad PL, Shih HM, Towle HC, Schwarzenberg SJ, Berry SA 1995 Growth hormone induction of hepatic serine protease inhibitor 2.1 transcription is mediated by a Stat5-related factor binding synergistically to two γ-activated sites. J Biol Chem 270:24903-24910
46. Krebs CJ, Larkins LK, Price R, Tullis KM, Miller RD, Robins DM 2003 Regulator of sex-limitation (Rsl) encodes a pair of KRAB zinc-finger genes that control sexually dimorphic liver gene expression. Genes Dev 17:2664-2674
47. Tullis KM, Krebs CJ, Leung JY, Robins DM 2003 The regulator of sex-limitation gene, rsl, enforces male-specific liver gene expression by negative regulation. Endocrinology 144:1854-1860
48. Waxman DJ, Celenza JL 2003 Sexual dimorphism of hepatic gene expression: novel biological role of KRAB zinc finger repressors revealed. Genes Dev 17:2607-2613
49. Davey HW, Xie T, McLachlan MJ, Wilkins RJ, Waxman DJ, Grattan DR 2001 STAT5b is required for GH-induced liver IGF-I gene expression. Endocrinology 142:3836-3841
50. Woelfle J, Chia DJ, Rotwein P 2003 Mechanisms of growth hormone (GH) action. Identification of conserved Stat5 binding sites that mediate GH-induced insulin-like growth factor-I gene activation. J Biol Chem 278:51261-51266
51. Woelfle J, Rotwein P 2004 In vivo regulation of growth hormone-stimulated gene transcription by STAT5b. Am J Physiol Endocrinol Metab 286:E393-E401
52. Nakajima H, Brindle PK, Handa M, Ihle JN 2001 Functional interaction of STAT5 and nuclear receptor co-repressor SMRT: implications in negative regulation of STAT5-dependent transcription. EMBO J 20:6836-6844
53. Luo G, Yu-Lee L 2000 Stat5b inhibits NFκB-mediated signaling. Mol Endocrinol 14:114-123
54. Zhou YC, Waxman DJ 1999 Cross-talk between janus kinase-signal transducer and activator of transcription (JAK-STAT) and peroxisome proliferator-activated receptor-α (PPARα) signaling pathways. Growth hormone inhibition of PPARα transcriptional activity mediated by stat5b. J Biol Chem 274:2672-2681
55. Bennett E, McGuinness L, Gevers EF, Thomas GB, Robinson IC, Davey HW, Luckman SM 2005 Hypothalamic STAT proteins: regulation of somatostatin neurones by growth hormone via STAT5b. J Neuroendocrinol 17:186-194
56. Davey HW, Park SH, Grattan DR, McLachlan MJ, Waxman DJ 1999 STAT5b-deficient mice are growth hormone pulse-resistant. Role of STAT5b in sex-specific liver p450 expression. J Biol Chem 274:35331-35336
57. Park SH, Liu X, Hennighausen L, Davey HW, Waxman DJ 1999 Distinctive roles of STAT5a and STAT5b in sexual dimorphism of hepatic P450 gene expression. Impact of STAT5a gene disruption. J Biol Chem 274:7421-7430
58. Jaffe CA, Turgeon DK, Lown K, Demott-Friberg R, Watkins PB 2002 Growth hormone secretion pattern is an independent regulator of growth hormone actions in humans. Am J Physiol Endocrinol Metab 283:E1008-E1015
59. Cheung C, Yu A-M, Chen C-S, Krausz KW, Byrd LG, Feigenbaum L, Edwards RJ, Waxman DJ, Gonzalez FJ 2006 Growth hormone determines sexual dimorphism of hepatic cytochrome P450 3A4 expression in transgenic mice. J Pharmacol Exp Ther 316:1328-1334