Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specifi c function

Journal of Cell Biology

Volumn 184, Issue 1, 2009, Pages 57-66

  Xu, Ren ^a   Nelson, Celeste M ^a,b   Muschler, John L ^c   Veiseh, Mandana ^a   Vonderhaar, Barbara K ^d   Bissell, Mina J ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b Princeton University   (United States)

^c California Pacifi c Medical Center Research Institute   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CASEIN; LAMININ; LAMININ 111; MILK PROTEIN; PROLACTIN; PROLACTIN RECEPTOR; STAT5 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CASEIN; DYSTROGLYCAN; HISTONE; JAK2 PROTEIN, MOUSE; JANUS KINASE 2; MESSENGER RNA;

ANIMAL CELL; ARTICLE; BREAST EPITHELIUM; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPITHELIUM CELL; GENE EXPRESSION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; ACETYLATION; ANIMAL; CULTURE TECHNIQUE; CYTOLOGY; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROMOTER REGION; UDDER;

ACETYLATION; ANIMALS; CASEINS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DYSTROGLYCANS; HISTONES; JANUS KINASE 2; LAMININ; MAMMARY GLANDS, ANIMAL; MICE; MILK PROTEINS; PHOSPHORYLATION; PROLACTIN; PROMOTER REGIONS, GENETIC; RECEPTORS, PROLACTIN; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR;

EID: 59849098041     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200807021     Document Type: Article

References (54)

1. Akhtar, N., and C.H. Streuli. 2006. Rac1 links integrin-mediated adhesion to the control of lactational differentiation in mammary epithelia. J. Cell Biol. 173:781-793.
2. Alcaraz, J., R. Xu, H. Mori, C.M. Nelson, R. Mroue, V.A. Spencer, D. Brownf eld , D.C. Radisky, C. Bustamante, and M.J. Bissell. 2008. Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO J. 27:2829-2838.
3. Barcellos-Hoff, M.H., J. Aggeler, T.G. Ram, and M.J. Bissell. 1989. Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development. 105:223-235.
4. Ben-Jonathan, N., J.L. Mershon, D.L. Allen, and R.W. Steinmetz. 1996. Extrapituitary prolactin: distribution, regulation, functions, and clinical aspects. Endocr. Rev. 17:639-669.
5. Boulanger, C.A., D.L. Mack, B.W. Booth, and G.H. Smith. 2007. Interaction with the mammary microenvironment redirects spermatogenic cell fate in vivo. Proc. Natl. Acad. Sci. USA. 104:3871-3876.
6. Chen, L.H., and M.J. Bissell. 1989. A novel regulatory mechanism for whey acidic protein gene expression. Cell Regul. 1:45-54.
7. Das, R.B., R. Biswas, and B.K. Vonderhaar. 1993. Characteristics of a membrane-associated antilactogen binding site for tamoxifen. Mol. Cell. Endocrinol. 98:1-8.
8. Emerman, J.T., J. Enami, D.R. Pitelka, and S. Nandi. 1977. Hormonal effects on intracellular and secreted casein in cultures of mouse mammary epithelial cells on f oating collagen membranes. Proc. Natl. Acad. Sci. USA. 74:4466-4470.
9. Faraldo, M.M., M.A. Deugnier, S. Tlouzeau, J.P. Thiery , and M.A. Glukhova. 2002 . Perturbation of beta1-integrin function in involuting mammary gland results in premature dedifferentiation of secretory epithelial cells. Mol. Biol. Cell. 13:3521-3531.
10. Freeman, M.E., M.S. Smith, S.J. Nazian, and J.D. Neill. 1974. Ovarian and hypothalamic control of the daily surges of prolactin secretion during pseudo pregnancy in the rat. Endocrinology. 94:875-882.
11. Goffn, V., N. Binart, P. Touraine, and P.A. Kelly. 2002 . Prolactin: the new biology of an old hormone. Annu. Rev. Physiol. 64:47-67.
12. Gouilleux, F., H. Wakao, M. Mundt, and B. Groner. 1994. Prolactin induces phosphorylation of Tyr694 of Stat5 (MGF), a prerequisite for DNA binding and induction of transcription. EMBO J. 13:4361-4369.
13. Henry , M.D., and K.P. Campbell. 1998. A role for dystroglycan in basement membrane assembly. Cell. 95:859-870.
14. Kabotyanski, E.B., M. Huetter, W. Xian, M. Rijnkels, and J.M. Rosen. 2006 . Integration of prolactin and glucocorticoid signaling at the beta-casein promoter and enhancer by ordered recruitment of specif c transcription factors and chromatin modifers. Mol. Endocrinol. 20:2355-2368.
15. Lee, E.Y., W.H. Lee, C.S. Kaetzel, G. Parry , and MJ. Bissell. 1985. Interaction of mouse mammary epithelial cells with collagen substrata: regulation of casein gene expression and secretion. Proc. Natl. Acad. Sci. USA. 82: 1419-1423.
16. Li, M.L., J. Aggeler, D.A. Farson, C. Hatier , J. Hassell, and M.J. Bissell. 1987. Inf uence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells. Proc. Natl. Acad. Sci. USA. 84:136-140.
17. Lin, C.Q., P.J. Dempsey, R.J. Coffey, and M.J. Bissell. 1995. Extracellular matrix regulates whey acidic protein gene expression by suppression of TGF-a in mouse mammary epithelial cells: studies in culture and in transgenic mice. J. Cell Biol. 129:1115-1126.
18. Liu, H., D.C. Radisky, F. Wang, and M.J. Bissell. 2004. Polarity and proliferation are controlled by distinct signaling pathways downstream of PI3-kinase in breast epithelial tumor cells. J. Cell Biol. 164:603-612.
19. Liu, X., G.W. Robinson, and L. Hennighausen. 1996. Activation of Stat5a and Stat5b by tyrosine phosphorylation is tightly linked to mammary gland differentiation. Mol. Endocrinol. 10:1496-1506.
20. McNally, J.G., W.G. Muller, D. Walker , R. Wolford, and G.L. Hager . 2000. The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science. 287:1262-1265.
21. Metivier, R., G. Penot, M.R. Hubner, G. Reid, H. Brand, M. Kos, and F. Gannon . 2003 . Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell. 115:751-763.
22. Murphy, S.J., J.J. Dore, M. Edens, R.J. Coffey, J.A. Barnard, H. Mitchell, M. Wilkes, and E.B. Leof. 2004. Differential traff cking of transforming growth factor-beta receptors and ligand in polarized epithelial cells. Mol. Biol. Cell. 15:2853-2862.
23. Muschler , J., A. Lochter , CD. Roskelley , P. Yurchenco, and M.J. Bissell. 1999. Division of labor among the alpha6beta4 integrin, beta1 integrins, and an E3 laminin receptor to signal morphogenesis and beta-casein expression in mammary epithelial cells. Mol. Biol. Cell. 10:2817-2828.
24. Muthuswamy, S.K., D. Li, S. Lelievre, M.J. Bissell, and J.S. Brugge. 2001. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat. Cell Biol. 3:785-792.
25. Naylor, M.J., N. Li, J. Cheung, E.T. Lowe, E. Lambert, R. Marlow, P. Wang, F Schatzmann, T. Wintermantel, G. Schuetz, et al. 2005. Ablation of β1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. J. Cell Biol. 171:717-728.
26. Nelson, E.A., S.R. Walker, J.V. Alvarez, and D.A. Frank. 2004. Isolation of unique STAT5 targets by chromatin immunoprecipitation-based gene identifcation. J. Biol. Chem. 279:54724-54730.
27. Nelson, W.J. 2003. Adaptation of core mechanisms to generate cell polarity. Nature. 422:766-774.
28. Onishi, M., T. Nosaka, K. Misawa, A.L. Mui, D. Gorman, M. McMahon, A. Miyajima, andT. Kitamura. 1998. Identif cation and characterization of a constitutively active STAT5 mutant that promotes cell proliferation. Mol. Cell. Biol. 18:3871-3879.
29. Porter, J.C., M. Falzon, and A. Hall. 2008. Polarized localization of epithelial CXCL11 in chronic obstructive pulmonary disease and mechanisms of T cell egression. J. Immunol. 180:1866-1877.
30. Reichmann, E., R. Ball, B. Groner, and R.R. Friis. 1989. New mammary epithelial and f broblastic cell clones in coculture form structures competent to differentiate functionally. J. Cell Biol. 108:1127-1138.
31. Rijnkels , M. , D.A. Wheeler , H.A. de Boer, and F.R. Pieper. 1997. Structure and expression of the mouse casein gene locus. Mamm. Genome. 8:9-15.
32. Rosen, J.M., S.L. Wyszomierski, and D. Hadsell. 1999. Regulation of milk protein gene expression. Annu. Rev. Nutr. 19:407-436.
33. Roskelley , C.D. , P.Y. Desprez, and M.J. Bissell. 1994. Extracellular matrixdependent tissue-specif c gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc. Natl. Acad. Sci. USA. 91:12378-12382.
34. Schwartz, G.J., J. Barasch, and Q. Al-Awqati. 1985. Plasticity of functional epithelial polarity. Nature. 318:368-371.
35. Schwartz, M.A. , and V. Baron . 1999 . Interactions between mitogenic stimuli, or, a thousand and one connections. Curr Opin. Cell Biol. 11:197-202.
36. Selvaraj, N.G., E. Omi, G. Gibori, and M.C. Rao . 2000 . Janus kinase 2 (JAK2) regulates prolactin-mediated chloride transport in mouse mammary epithelial cells through tyrosine phosphorylation of Na+-K+-2Cl- cotransporter. Mol. Endocrinol. 14:2054-2065.
37. Streuli, C.H., and M.J. Bissell. 1990. Expression of extracellular matrix components is regulated by substratum. J. Cell Biol. 110:1405-1415.
38. Streuli, C.H., N. Bailey, and M.J. Bissell. 1991. Control of mammary epithelial differentiation: basement membrane induces tissue-specif c gene expression in the absence of cell - cell interaction and morphological polarity J. Cell Biol. 115:1383-1395.
39. Streuli, C.H., G.M. Edwards, M. Delcommenne, C.B. Whitelaw, T.G. Burdon, C. Schindler , and C.J. Watson . 1995a . Stat5 as a target for regulation by extracellular matrix. J. Biol. Chem. 270:21639-21644.
40. Streuli, C.H., C. Schmidhauser, N. Bailey, P. Yurchenco, A.P. Skubitz, C. Roskelley, and M.J. Bissell. 1995b. Laminin mediates tissue-specif c gene expression in mammary epithelia. J. Cell Biol. 129:591-603.
41. Sympson , C.J. , R.S. Talhouk , C.M. Alexander , J.R. Chin, S.M. Clift, M.J. Bissell, and Z. Werb. 1994 . Targeted expression of stromelysin-1 in mammary gland provides evidence for a role of proteinases in branching morphogenesis and the requirement for an intact basement membrane for tissuespecif c gene expression. J. Cell Biol. 125:681-693.
42. Takahashi , K. , and S. Yamanaka . 2006 . Induction of pluripotent stem cells from mouse embryonic and adult f broblast cultures by def ned factors. Cell. 126:663-676.
43. Talhouk, R.S., J.R. Chin, E.N. Unemori, Z. Werb, and M.J. Bissell. 1991. Proteinases of the mammary gland: developmental regulation in vivo and vectorial secretion in culture. Development. 112:439-449.
44. Talhouk, R.S., M.J. Bissell, and Z. Werb. 1992 . Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. J. Cell Biol. 118:1271-1282.
45. Tourkine , N., C. Schindler , M. Larose, and L.M. Houdebine . 1995 . Activation of STAT factors by prolactin, interferon-gamma, growth hormones, and a tyrosine phosphatase inhibitor in rabbit primary mammary epithelial cells. J. Biol. Chem. 270:20952-20961.
46. Vermeer , P.D. , L.A. Einwalter , TO. Moninger , T. Rokhlina, J.A. Kern, J. Zabner, and M.J. Welsh . 2003 . Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature. 422:322-326.
47. Wagner , K.U. , A. Krempler , A.A. Triplett , Y. Qi , N.M. George , J. Zhu , and H. Rui . 2004 . Impaired alveologenesis and maintenance of secretory mammary epithelial cells in Jak2 conditional knockout mice. Mol. Cell. Biol. 24:5510-5520.
48. Wang, F., V.M. Weaver, O.W Petersen , C.A. Larabell , S. Dedhar , P. Briand, R. Lupu, and M.J. Bissell. 1998. Reciprocal interactions between beta1- integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology Proc. Natl. Acad. Sci. USA. 95:14821-14826.
49. Watson, C.J., and T.G. Burdon . 1996 . Prolactin signal transduction mechanisms in the mammary gland: the role of the Jak/Stat pathway. Rev. Reprod. 1:1-5.
50. Weaver , V.M. , O.W. Petersen , F. Wang , C.A. Larabell , P. Briand , C. Damsky , and M.J. Bissell . 1997 . Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell Biol. 137 : 231-245 .
51. Weir , M.L. , M.L. Oppizzi , M.D. Henry , A. Onishi , K.P Campbell, M.J. Bissell, and J.L. Muschler . 2006 . Dystroglycan loss disrupts polarity and betacasein induction in mammary epithelial cells by perturbing laminin anchoring. J. Cell Sci. 119:4047-4058.
52. Wipff, P.J., D.B. Rifkin, J.J. Meister, and B. Hinz. 2007. Myof broblast contraction activates latent TGF-β1 from the extracellular matrix. J. Cell Biol. 179:1311-1323.
53. Xu, R., V.A. Spencer, and M.J. Bissell. 2007. Extracellular matrix-regulated gene expression requires cooperation of SWI/SNF and transcription factors. J. Biol. Chem. 282:14992-14999.
54. Yamada, K.M., and S. Even-Ram. 2002. Integrin regulation of growth factor receptors. Nat. Cell Biol. 4:E75-E76.