Mammary-specific gene activation is defined by progressive recruitment of STAT5 during pregnancy and the establishment of H3K4me3 marks

Molecular and Cellular Biology

Volumn 34, Issue 3, 2014, Pages 464-473

  Kang, Keunsoo ^a   Yamaji, Daisuke ^a   Yoo, Kyung Hyun ^a   Robinson, Gertraud W ^a   Hennighausen, Lothar ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; STAT5 PROTEIN; TRANSCRIPTOME; TRIMETHYLATED HISTONE H3 AT K4; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ARTICLE; BREAST EPITHELIUM; CELL DIFFERENTIATION; CONTROLLED STUDY; ENHANCER REGION; GENE ACTIVATION; NUCLEOTIDE SEQUENCE; PREGNANCY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; RNA SEQUENCE; TRANSCRIPTION INITIATION;

ANIMALS; ANIMALS, NEWBORN; CHROMATIN; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE ONTOLOGY; HISTONES; LYSINE; MAMMARY GLANDS, ANIMAL; METHYLATION; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PREGNANCY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; STAT5 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION; TRANSCRIPTOME;

EID: 84892448429     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00988-13     Document Type: Article

References (41)

1. Seagroves TN, Krnacik S, Raught B, Gay J, Burgess-Beusse B, Darlington GJ, Rosen JM. 1998. C/EBPbeta, but not C/EBPalpha, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev. 12:1917-1928. http: //dx.doi.org/10.1101/gad.12.12.1917.
2. Lee HJ, Ormandy CJ. 2012. Elf5, hormones and cell fate. Trends Endocrinol. Metab. 23:292-298. http://dx.doi.org/10.1016/j.tem.2012.02.006.
3. Oakes SR, Naylor MJ, Asselin-Labat ML, Blazek KD, Gardiner-Garden M, Hilton HN, Kazlauskas M, Pritchard MA, Chodosh LA, Pfeffer PL, Lindeman GJ, Visvader JE, Ormandy CJ. 2008. The Ets transcription factor Elf5 specifies mammary alveolar cell fate. Genes Dev. 22:581-586. http://dx.doi.org/10.1101/gad.1614608.
4. Zhou J, Chehab R, Tkalcevic J, Naylor MJ, Harris J, Wilson TJ, Tsao S, Tellis I, Zavarsek S, Xu D, Lapinskas EJ, Visvader J, Lindeman GJ, Thomas R, Ormandy CJ, Hertzog PJ, Kola I, Pritchard MA. 2005. Elf5 is essential for early embryogenesis and mammary gland development during pregnancy and lactation. EMBO J. 24:635-644. http://dx.doi.org/10.1038/sj.emboj.7600538.
5. LaMarca HL, Visbal AP, Creighton CJ, Liu H, Zhang Y, Behbod F, Rosen JM. 2010. CCAAT/enhancer binding protein beta regulates stemcell activity and specifies luminal cell fate in the mammary gland. Stem Cells 28:535-544. http://dx.doi.org/10.1002/stem.297.
6. Hennighausen L, Robinson GW. 2005. Information networks in the mammary gland. Nat. Rev. Mol. Cell Biol. 6:715-725. http://dx.doi.org/10.1038/nrm1714.
7. Hughes K, Watson CJ. 2012. The spectrum of STAT functions in mammary gland development. JAK-STAT 1:151-158. http://dx.doi.org/10.4161/jkst.19691.
8. Brisken C, O'Malley B. 2010. Hormone action in the mammary gland. Cold Spring Harb. Perspect. Biol. 2:a003178. http://dx.doi.org/10.1101/cshperspect.a003178.
9. Robinson GW, Johnson PF, Hennighausen L, Sterneck E. 1998. The C/EBPbeta transcription factor regulates epithelial cell proliferation and differentiation in the mammary gland. Genes Dev. 12:1907-1916. http: //dx.doi.org/10.1101/gad.12.12.1907.
10. Yamaji D, Kang K, Robinson GW, Hennighausen L. 2013. Sequential activation of genetic programs in mouse mammary epithelium during pregnancy depends on STAT5A/B concentration. Nucleic Acids Res. 41: 2-1636. http://dx.doi.org/10.1093/nar/gks1310.
11. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. 2007. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77-88. http://dx.doi.org/10.1016/j.cell.2007.05.042.
12. Abraham BJ, Cui K, Tang Q, Zhao K. 2013. Dynamic regulation of epigenomic landscapes during hematopoiesis. BMC Genomics 14:193. http://dx.doi.org/10.1186/1471-2164-14-193.
13. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14:R36. http://dx.doi.org /10.1186/gb-2013-14-4-r36.
14. Roberts A, Pimentel H, Trapnell C, Pachter L. 2011. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics. 7:2325-2329. http://dx.doi.org/10.1093/bioinformatics/btr355.
15. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, Wagner U, Dixon J, Lee L, Lobanenkov VV, Ren B. 2012. A map of the cis-regulatory sequences in the mouse genome. Nature 488:116-120. http://dx.doi.org /10.1038/nature11243.
16. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106. http://dx.doi.org/10.1186/gb-2010-11 -10-r106.
17. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. http://dx.doi.org/10.1186/gb-2009-10-3-r25.
18. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38:576-589. http://dx.doi.org/10.1016/j.molcel.2010.05.004.
19. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nat. Biotechnol. 9:24-26. http://dx.doi.org/10.1038/nbt.1754.
20. Machanick P, Bailey TL. 2011. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27:1696-1697. http://dx.doi.org/10.1093/bioinformatics /btr189.
21. Warde-Farley D, Donaldson SL, Comes O, Zuberi K, Badrawi R, Chao P, Franz M, Grouios C, Kazi F, Lopes CT, Maitland A, Mostafavi S, Montojo J, Shao Q, Wright G, Bader GD, Morris Q. 2010. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res. 38:W214- W220. http://dx.doi.org/10.1093/nar/gkq537.
22. Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, Pico AR, Bader GD, Ideker T. 2012. A travel guide to Cytoscape plugins. Nat. Methods 9:1069-1076. http://dx.doi.org/10.1038/nmeth.2212.
23. Mandal M, Powers SE, Maienschein-Cline M, Bartom ET, Hamel KM, Kee BL, Dinner AR, Clark MR. 2011. Epigenetic repression of the Igk locus by STAT5-mediated recruitment of the histone methyltransferase Ezh2. Nat. Immunol. 12:1212-1220. http://dx.doi.org/10.1038/ni.2136.
24. Kang K, Robinson GW, Hennighausen L. 2013. Comprehensive metaanalysis of signal transducers and activators of transcription (STAT) genomic binding patterns discerns cell-specific cis-regulatory modules. BMC Genomics 14:4. http://dx.doi.org/10.1186/1471-2164-14-4.
25. Shore AN, Kabotyanski EB, Roarty K, Smith MA, Zhang Y, Creighton CJ, Dinger ME, Rosen JM. 2012. Pregnancy-induced noncoding RNA (PINC) associates with polycomb repressive complex 2 and regulates mammary epithelial differentiation. PLoS Genet. 8:e1002840. http://dx.doi.org/10.1371/journal.pgen.1002840.
26. Zhang Y, Laz EV, Waxman DJ. 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. http://dx.doi.org/10.1128 /MCB.06312-11.
27. Burdon TG, Maitland KA, Clark AJ, Wallace R, Watson CJ. 1994. Regulation of the sheep beta-lactoglobulin gene by lactogenic hormones is mediated by a transcription factor that binds an interferon-gamma activation site-related element. Mol. Endocrinol. 8:1528-1536. http://dx.doi.org/10.1210/me.8.11.1528.
28. Vahedi G, Takahashi H, Nakayamada S, Sun HW, Sartorelli V, Kanno Y, O'Shea JJ. 2012. STATs shape the active enhancer landscape of T cell populations. Cell 151:981-993. http://dx.doi.org/10.1016/j.cell.2012.09.044.
29. Li S, Rosen JM. 1995. Nuclear factor I and mammary gland factor (STAT5) play a critical role in regulating rat whey acidic protein gene expression in transgenic mice. Mol. Cell. Biol. 15:2063-2070.
30. Kabotyanski EB, Rijnkels M, Freeman-Zadrowski C, Buser AC, Edwards DP, Rosen JM. 2009. Lactogenic hormonal induction of long distance interactions between beta-casein gene regulatory elements. J. Biol. Chem. 284:22815-22824. http://dx.doi.org/10.1074/jbc.M109.032490.
31. Kabotyanski EB, Huetter M, Xian W, Rijnkels M, Rosen JM. 2006. Integration of prolactin and glucocorticoid signaling at the beta-casein promoter and enhancer by ordered recruitment of specific transcription factors and chromatin modifiers. Mol. Endocrinol. 20:2355-2368. http: //dx.doi.org/10.1210/me.2006-0160.
32. De Gobbi M, Garrick D, Lynch M, Vernimmen D, Hughes JR, Goardon N, Luc S, Lower KM, Sloane-Stanley JA, Pina C, Soneji S, Renella R, Enver T, Taylor S, Jacobsen SE, Vyas P, Gibbons RJ, Higgs DR. 2011. Generation of bivalent chromatin domains during cell fate decisions. Epigenetics Chromatin 4:9. http://dx.doi.org/10.1186/1756-8935-4-9.
33. Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W, Zhao K. 2009. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 4:80-93. http://dx.doi.org/10.1016/j.stem.2008.11.011.
34. Rijnkels M, Freeman-Zadrowski C, Hernandez J, Potluri V, Wang L, Li W, Lemay DG. 2013. Epigenetic modifications unlock the milk protein gene loci during mouse mammary gland development and differentiation. PLoS One 8:e53270. http://dx.doi.org/10.1371/journal.pone.0053270.
35. Deng C, Li Y, Liang S, Cui K, Salz T, Yang H, Tang Z, Gallagher PG, Qiu Y, Roeder R, Zhao K, Bungert J, Huang S. 2013. USF1 and hSET1A mediated epigenetic modifications regulate lineage differentiation and HoxB4 transcription. PLoS Genet. 9:e1003524. http://dx.doi.org/10.1371 /journal.pgen.1003524.
36. Tarulli GA, De Silva D, Ho V, Kunasegaran K, Ghosh K, Tan BC, Bulavin DV, Pietersen AM. 2013. Hormone-sensing cells require Wip1 for paracrine stimulation in normal and premalignant mammary epithelium. Breast Cancer Res. 15:R10. http://dx.doi.org/10.1186/bcr3381.
37. Sugathan A, Waxman DJ. 2013. Genome-wide analysis of chromatin states reveals distinct mechanisms of sex-dependent gene regulation in male and female mouse liver. Mol. Cell. Biol. 33:3594-3610. http://dx.doi.org/10.1128/MCB.00280-13.
38. Pittius CW, Hennighausen L, Lee E, Westphal H, Nicols E, Vitale J, Gordon K. 1988. A milk protein gene promoter directs the expression of human tissue plasminogen activator cDNA to the mammary gland in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 85:5874-5878. http://dx.doi.org/10.1073/pnas.85.16.5874.
39. Gordon K, Lee E, Vitale JA, Smith AE, Westphal H, Hennighausen L. 1992. Production of human tissue plasminogen activator in transgenic mouse milk. 1987. Biotechnology 24:425-428.
40. McKnight RA, Spencer M, Wall RJ, Hennighausen L. 1996. Severe position effects imposed on a 1 kb mouse whey acidic protein gene promoter are overcome by heterologous matrix attachment regions. Mol. Reprod. Dev. 44:179 -184. http://dx.doi.org/10.1002/(SICI)1098 -2795(199606)44:2179::AID-MRD63.0.CO;2-K.
41. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57. http://dx.doi.org/10.1038/nprot.2008.211.