Sequential activation of genetic programs in mouse mammary epithelium during pregnancy depends on STAT5A/B concentration

Nucleic Acids Research

Volumn 41, Issue 3, 2013, Pages 1622-1636

  Yamaji, Daisuke ^a   Kang, Keunsoo ^a   Robinson, Gertraud W ^a   Hennighausen, Lothar ^a,b  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b Dankook University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE II; STAT5A PROTEIN; STAT5B PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BREAST DEVELOPMENT; BREAST EPITHELIUM; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENOTYPING TECHNIQUE; HISTOLOGY; IN VIVO STUDY; LACTATION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCER AND ACTIVATOR OF TRANSCRIPTION 5A GENE; SIGNAL TRANSDUCER AND ACTIVATOR OF TRANSCRIPTION 5B GENE; TISSUE LEVEL;

ANIMALS; BINDING SITES; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; MICE, KNOCKOUT; MICE, NUDE; PREGNANCY; RNA POLYMERASE II; STAT5 TRANSCRIPTION FACTOR;

EID: 84873637249     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1310     Document Type: Article

References (47)

1. Wakao,H., Gouilleux,F. and Groner,B. (1995) Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J., 14, 854-855.
2. Hennighausen,L. and Robinson,G.W. (2005) Information networks in the mammary gland. Nat. Rev. Mol. Cell. Biol., 6, 715-725.
3. Cui,Y., Riedlinger,G., Miyoshi,K., Tang,W., Li,C., Deng,C.X., Robinson,G.W. and Hennighausen,L. (2004) Inactivation of Stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol. Cell. Biol., 24, 8037-8047.
4. Yamaji,D., Na,R., Feuermann,Y., Pechhold,S., Chen,W., Robinson,G.W. and Hennighausen,L. (2009) Development of mammary luminal progenitor cells is controlled by the transcription factor STAT5A. Genes Dev., 23, 2382-2387.
5. Liu,X., Robinson,G.W. and Hennighausen,L. (1996) Activation of Stat5a and Stat5b by tyrosine phosphorylation is tightly linked to mammary gland differentiation. Mol. Endocrinol., 10, 1496-1506.
6. Liu,X., Robinson,G.W., Wagner,K.U., Garrett,L., Wynshaw-Boris,A. and Hennighausen,L. (1997) Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev., 11, 179-186.
7. Udy,G.B., Towers,R.P., Snell,R.G., Wilkins,R.J., Park,S.H., Ram,P.A., Waxman,D.J. and Davey,H.W. (1997) Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc. Natl Acad. Sci. USA, 94, 7239-7244.
8. Liu,X., Robinson,G.W., Gouilleux,F., Groner,B. and Hennighausen,L. (1995) Cloning and expression of Stat5 and an additional homologue (Stat5b) involved in prolactin signal transduction in mouse mammary tissue. Proc. Natl Acad. Sci. USA, 92, 8831-8835.
9. Meyer,R.D., Laz,E.V., Su,T. and Waxman,D.J. (2009) Male-specific hepatic Bcl6: growth hormone-induced block of transcription elongation in females and binding to target genes inversely coordinated with STAT5. Mol. Endocrinol., 23, 1914-1926.
10. Chia,D.J. and Rotwein,P. (2010) Defining the epigenetic actions of growth hormone: acute chromatin changes accompany GH-activated gene transcription. Mol. Endocrinol., 24, 2038-2049.
11. Chia,D.J., Varco-Merth,B. and Rotwein,P. (2010) Dispersed Chromosomal Stat5b-binding elements mediate growth hormone-activated insulin-like growth factor-I gene transcription. J. Biol. Chem., 285, 17636-17647.
12. Lin,J.X., Li,P., Liu,D., Jin,H.T., He,J., Ata Ur Rasheed,M., Rochman,Y., Wang,L., Cui,K., Liu,C. et al. (2012) Critical Role of STAT5 transcription factor tetramerization for cytokine responses and normal immune function. Immunity, 36, 586-599.
13. Rotwein,P. (2012) Mapping the growth hormone-Stat5b-IGF-I transcriptional circuit. Trends Endocrinol. Metab., 23, 186-193.
14. Zhang,Y., Laz,E.V. and Waxman,D.J. (2012) Dynamic, sex-differential STAT5 and BCL6 binding to sex-biased, growth hormone-regulated genes in adult mouse liver. Mol. Cell. Biol., 32, 880-896.
15. Wagner,K.U., Wall,R.J., St-Onge,L., Gruss,P., Wynshaw-Boris,A., Garrett,L., Li,M., Furth,P.A. and Hennighausen,L. (1997) Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res., 25, 4323-4330.
16. Trapnell,C., Pachter,L. and Salzberg,S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
17. Trapnell,C. and Salzberg,S.L. (2009) How to map billions of short reads onto genomes. Nat. Biotechnol., 27, 455-457.
18. Mortazavi,A., Williams,B.A., McCue,K., Schaeffer,L. and Wold,B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 621-628.
19. Bolstad,B.M., Irizarry,R.A., Astrand,M. and Speed,T.P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics, 19, 185-193.
20. de Hoon,M.J., Imoto,S., Nolan,J. and Miyano,S. (2004) Open source clustering software. Bioinformatics, 20, 1453-1454.
21. Li,H. and Durbin,R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
22. North,B.V., Curtis,D. and Sham,P.C. (2002) A note on the calculation of empirical P values from Monte Carlo procedures. Am. J. Hum. Genet., 71, 439-441.
23. Yao,Z., Cui,Y., Watford,W.T., Bream,J.H., Yamaoka,K., Hissong,B.D., Li,D., Durum,S.K., Jiang,Q., Bhandoola,A. et al. (2006) Stat5a/b are essential for normal lymphoid development and differentiation. Proc. Natl Acad. Sci. USA, 103, 1000-1005.
24. Shillingford,J.M., Miyoshi,K., Robinson,G.W., Bierie,B., Cao,Y., Karin,M. and Hennighausen,L. (2003) Proteotyping of mammary tissue from transgenic and gene knockout mice with immunohistochemical markers: a tool to define developmental lesions. J. Histochem. Cytochem., 51, 555-565.
25. Robinson,G.W., McKnight,R.A., Smith,G.H. and Hennighausen,L. (1995) Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development, 121, 2079-2090.
26. Ormandy,C.J., Camus,A., Barra,J., Damotte,D., Lucas,B., Buteau,H., Edery,M., Brousse,N., Babinet,C., Binart,N. et al. (1997) Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev., 11, 167-178.
27. Zhou,J., Chehab,R., Tkalcevic,J., Naylor,M.J., Harris,J., Wilson,T.J., Tsao,S., Tellis,I., Zavarsek,S., Xu,D. et al. (2005) Elf5 is essential for early embryogenesis and mammary gland development during pregnancy and lactation. EMBO J., 24, 635-644.
28. Harris,J., Stanford,P.M., Sutherland,K., Oakes,S.R., Naylor,M.J., Robertson,F.G., Blazek,K.D., Kazlauskas,M., Hilton,H.N., Wittlin,S. et al. (2006) Socs2 and elf5 mediate prolactin-induced mammary gland development. Mol. Endocrinol., 20, 1177-1187.
29. Naylor,M.J., Oakes,S.R., Gardiner-Garden,M., Harris,J., Blazek,K., Ho,T.W., Li,F.C., Wynick,D., Walker,A.M. and Ormandy,C.J. (2005) Transcriptional changes underlying the secretory activation phase of mammary gland development. Mol. Endocrinol., 19, 1868-1883.
30. Oakes,S.R., Naylor,M.J., Asselin-Labat,M.L., Blazek,K.D., Gardiner-Garden,M., Hilton,H.N., Kazlauskas,M., Pritchard,M.A., Chodosh,L.A., Pfeffer,P.L. et al. (2008) The Ets transcription factor Elf5 specifies mammary alveolar cell fate. Genes Dev., 22, 581-586.
31. Dong,J., Tong,T., Reynado,A.M., Rosen,J.M., Huang,S. and Li,Y. (2010) Genetic manipulation of individual somatic mammary cells in vivo reveals a master role of STAT5a in inducing alveolar fate commitment and lactogenesis even in the absence of ovarian hormones. Dev. Biol., 346, 196-203.
32. Iavnilovitch,E., Cardiff,R.D., Groner,B. and Barash,I. (2004) Deregulation of Stat5 expression and activation causes mammary tumors in transgenic mice. Int. J. Cancer, 112, 607-619.
33. Iavnilovitch,E., Groner,B. and Barash,I. (2002) Overexpression and forced activation of stat5 in mammary gland of transgenic mice promotes cellular proliferation, enhances differentiation, and delays postlactational apoptosis. Mol. Cancer Res., 1, 32-47.
34. Schepers,H., van Gosliga,D., Wierenga,A.T., Eggen,B.J., Schuringa,J.J. and Vellenga,E. (2007) STAT5 is required for long-term maintenance of normal and leukemic human stem/progenitor cells. Blood, 110, 2880-2888.
35. Vafaizadeh,V., Klemmt,P., Brendel,C., Weber,K., Doebele,C., Britt,K., Grez,M., Fehse,B., Desrivieres,S. and Groner,B. (2010) Mammary epithelial reconstitution with gene-modified stem cells assigns roles to Stat5 in luminal alveolar cell fate decisions, differentiation, involution, and mammary tumor formation. Stem Cells, 28, 928-938.
36. Wierenga,A.T., Vellenga,E. and Schuringa,J.J. (2008) Maximal STAT5-induced proliferation and self-renewal at intermediate STAT5 activity levels. Mol. Cell. Biol., 28, 6668-6680.
37. Guyette,W.A., Matusik,R.J. and Rosen,J.M. (1979) Prolactin-mediated transcriptional and post-transcriptional control of casein gene expression. Cell, 17, 1013-1023.
38. Devinoy,E., Thepot,D., Stinnakre,M.G., Fontaine,M.L., Grabowski,H., Puissant,C., Pavirani,A. and Houdebine,L.M. (1994) High level production of human growth hormone in the milk of transgenic mice: the upstream region of the rabbit whey acidic protein (WAP) gene targets transgene expression to the mammary gland. Transgenic Res., 3, 79-89.
39. Miyoshi,K., Meyer,B., Gruss,P., Cui,Y., Renou,J.P., Morgan,F.V., Smith,G.H., Reichenstein,M., Shani,M., Hennighausen,L. et al. (2002) Mammary epithelial cells are not able to undergo pregnancy-dependent differentiation in the absence of the helix-loop-helix inhibitor Id2. Mol. Endocrinol., 16, 2892-2901.
40. Kouros-Mehr,H., Slorach,E.M., Sternlicht,M.D. and Werb,Z. (2006) GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell, 127, 1041-1055.
41. Vorbach,C., Scriven,A. and Capecchi,M.R. (2002) The housekeeping gene xanthine oxidoreductase is necessary for milk fat droplet enveloping and secretion: gene sharing in the lactating mammary gland. Genes Dev., 16, 3223-3235.
42. Wang,W., Lv,N., Zhang,S., Shui,G., Qian,H., Zhang,J., Chen,Y., Ye,J., Xie,Y., Shen,Y. et al. (2012) Cidea is an essential transcriptional coactivator regulating mammary gland secretion of milk lipids. Nat. Med., 18, 235-243.
43. MacIsaac,K.D., Lo,K.A., Gordon,W., Motola,S., Mazor,T. and Fraenkel,E. (2010) A quantitative model of transcriptional regulation reveals the influence of binding location on expression. PLoS Comput. Biol., 6, e1000773.
44. Zhu,B.M., Kang,K., Yu,J.H., Chen,W., Smith,H.E., Lee,D., Sun,H.W., Wei,L. and Hennighausen,L. (2012) Genome-wide analyses reveal the extent of opportunistic STAT5 binding that does not yield transcriptional activation of neighboring genes. Nucleic Acids Res., 40, 4461-4472.
45. Rijnkels,M., Kabotyanski,E., Montazer-Torbati,M.B., Hue Beauvais,C., Vassetzky,Y., Rosen,J.M. and Devinoy,E. (2010) The epigenetic landscape of mammary gland development and functional differentiation. J. Mammary Gland Biol. Neoplasia, 15, 85-100.
46. Chia,D.J., Young,J.J., Mertens,A.R. and Rotwein,P. (2010) Distinct alterations in chromatin organization of the two IGF-I promoters precede growth hormone-induced activation of IGF-I gene transcription. Mol. Endocrinol., 24, 779-789.
47. Cooper,G.M., Stone,E.A., Asimenos,G., Green,E.D., Batzoglou,S. and Sidow,A. (2005) Distribution and intensity of constraint in mammalian genomic sequence. Genome Res., 15, 901-913.