Role of STAT5a in regulation of sex-specific gene expression in female but not male mouse liver revealed by microarray analysis

Physiological Genomics

Volumn 31, Issue 1, 2007, Pages 63-74

  Clodfelter, Karl H ^a   Miles, Gregory D ^a   Wauthier, Valerie ^a   Holloway, Minita G ^a   Zhang, Xiaohua ^b   Hodor, Paul ^b   Ray, William J ^b   Waxman, David J ^a  

^a Boston University   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Growth hormone action; Knockout; Liver sexual dimorphism; Signal transducer and activator of transcription 5a; Strain dependent gene expression

Indexed keywords

STAT5A PROTEIN; STAT5B PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; FEMALE; GENE CONTROL; GENE EXPRESSION; LIVER; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RNA ANALYSIS; SEX DIFFERENCE; UNINDEXED SEQUENCE; WILD TYPE;

ANIMALS; CROSSES, GENETIC; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TECHNIQUES; GROWTH HORMONE; LIVER; MALE; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEX FACTORS; STAT5 TRANSCRIPTION FACTOR;

MAMMALIA; MUS;

EID: 34548813862     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00055.2007     Document Type: Article

References (38)

1. Ahluwalia A, Clodfelter KH, Waxman DJ. Sexual dimorphism of rat liver gene expression: regulatory role of growth hormone revealed by deoxyribonucleic acid microarray analysis. Mol Endocrinol 18: 747-760, 2004.
2. Aida K, Negishi M. A trans-acting locus regulates transcriptional repression of the female-specific steroid 15 alpha-hydroxylase gene in male mice. J Mol Endocrinol 11: 213-222, 1993.
3. Choi HK, Waxman DJ. Growth hormone, but not prolactin, maintains low-level activation of STAT5a and STAT5b in female rat liver. Endocrinology 140: 5126-5135, 1999.
4. Choi HK, Waxman DJ. Plasma growth hormone pulse activation of hepatic JAK-STAT5 signaling: developmental regulation and role in male-specific liver gene expression. Endocrinology 141: 3245-3255, 2000.
5. Clodfelter KH, Holloway MG, Hodor P, Park SH, Ray WJ, Waxman DJ. 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. Mol Endocrinol 20: 1333-1351, 2006.
6. Darnell JE Jr. STATs and gene regulation. Science 277: 1630-1635, 1997.
7. Grimley PM, Dong F, Rui H. Stat5a and Stat5b: fraternal twins of signal transduction and transcriptional activation. Cytokine Growth Factor Rev 10: 131-157, 1999.
8. He YD, Dai H, Schadt EE, Cavet G, Edwards SW, Stepaniants SB, Duenwald S, Kleinhanz R, Jones AR, Shoemaker DD, Stoughton RB. Microarray standard data set and figures of merit for comparing data processing methods and experiment designs. Bioinformatics 19: 956-965, 2003.
9. Herrington J, Carter-Su C. Signaling pathways activated by the growth hormone receptor. Trends Endocrinol Metab 12: 252-257, 2001.
10. Holloway MG, Cui Y, Laz EV, Hosui A, Hennighausen L, Waxman DJ. Loss of sexually dimorphic liver gene expression upon hepatocyte-specific deletion of Stat5a-Stat5b locus. Endocrinology 148: 1977-1986, 2007.
11. Holloway MG, Laz EV, Waxman DJ. Codependence of growth hormone-responsive, sexually dimorphic hepatic gene expression on signal transducer and activator of transcription 5b and hepatic nuclear factor 4alpha. Mol Endocrinol 20: 647-660, 2006.
12. Horvath CM. STAT proteins and transcriptional responses to extracellular signals. Trends Biochem Sci 25: 496-502, 2000.
13. Hughes TR, Mao M, Jones AR, Burchard J, Marton MJ, Shannon KW, Lefkowitz SM, Ziman M, Schelter JM, Meyer MR, Kobayashi S, Davis C, Dai H, He YD, Stephaniants SB, Cavet G, Walker WL, West A, Coffey E, Shoemaker DD, Stoughton R, Blanchard AP, Friend SH, Linsley PS. Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer. Nat Biotechnol 19: 342-347, 2001.
14. Ihle JN. The Stat family in cytokine signaling. Curr Opin Cell Biol 13: 211-217, 2001.
15. Jansson JO, Eden S, Isaksson O. Sexual dimorphism in the control of growth hormone secretion. Endocr Rev 6: 128-150, 1985.
16. Krebs CJ, Larkins LK, Khan SM, Robins DM. Expansion and diversification of KRAB zinc-finger genes within a cluster including regulator of sex-limitation 1 and 2. Genomics 85: 752-761, 2005.
17. Krebs CJ, Larkins LK, Price R, Tullis KM, Miller RD, Robins DM. 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, 2003.
18. Laz EV, Holloway MG, Chen CS, Waxman DJ. Characterization of three growth hormone-responsive transcription factors preferentially expressed in adult female liver. Endocrinology. 148:3327-3337, 2007.
19. 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 11: 179-186, 1997.
20. MacLeod JN, Pampori NA, Shapiro BH. Sex differences in the ultradian pattern of plasma growth hormone concentrations in mice. J Endocrinol 131: 395-399, 1991.
21. Mode A, Gustafsson JA. Sex and the liver - a journey through five decades. Drug Metab Rev 38: 197-207, 2006.
22. Mori S, Nishikawa SI, Yokota Y. Lactation defect in mice lacking the helix-loop-helix inhibitor Id2. EMBO J 19: 5772-5781, 2000.
23. Noshiro M, Serabjit-Singh CJ, Bend JR, Negishi M. Female-predominant expression of testosterone 16 alpha-hydroxylase ("I"-P-450(16) alpha) and its repression in strain 129/J. Arch Biochem Biophys 244: 857-864, 1986.
24. 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 274: 7421-7430, 1999.
25. Schwartz J, Huo JS, Piwien-Pilipuk G. Growth hormone regulated gene expression. Minerva Endocrinol 27: 231-241, 2002.
26. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods 31: 265-273, 2003.
27. 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 20: 389-401, 2000.
28. 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 93: 841-850, 1998.
29. Tullis KM, Krebs CJ, Leung JY, Robins DM. The regulator of sex-limitation gene, rsl, enforces male-specific liver gene expression by negative regulation. Endocrinology 144: 1854-1860, 2003.
30. 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 94: 7239-7244, 1997.
31. Veldhuis JD, Anderson SM, Shah N, Bray M, Vick T, Gentili A, Mulligan T, Johnson ML, Weltman A, Evans WS, Iranmanesh A. Neurophysiological regulation and target-tissue impact of the pulsatile mode of growth hormone secretion in the human. Growth Horm IGF Res11, Suppl A: S25-S37, 2001.
32. Waxman DJ. 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, 2000.
33. Waxman DJ, Celenza JL. Sexual dimorphism of hepatic gene expression: novel biological role of KRAB zinc finger repressors revealed. Genes Dev 17: 2607-2613, 2003.
34. Waxman DJ, O'Connor C. Growth hormone regulation of sex-dependent liver gene expression. Mol Endocrinol 20: 2613-2629, 2006.
35. 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 270: 13262-13270, 1995.
36. Weng L, Dai H, Zhan Y, He Y, Stepaniants SB, Bassett DE. Rosetta error model for gene expression analysis. Bioinformatics 22: 1111-1121, 2006.
37. Wiwi CA, Waxman DJ. Role of hepatocyte nuclear factors in growth hormone-regulated, sexually dimorphic expression of liver cytochromes P450. Growth Factors 22: 79-88, 2004.
38. Yang X, Schadt EE, Wang S, Wang H, Arnold AP, Ingram-Drake L, Drake TA, Lusis AJ. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 16: 995-1004, 2006.