SnoN regulates mammary gland alveologenesis and onset of lactation by promoting prolactin/stat5 signaling

Development (Cambridge)

Volumn 139, Issue 17, 2012, Pages 3147-3156

  Jahchan, Nadine S ^a,c   Wang, Douglas ^a   Bissell, Mina J ^b   Luo, Kunxin ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Lactation; LrECM; Mammary gland; Mouse; SnoN; Stat5; TGF

Indexed keywords

PROLACTIN; PROTEIN; SNON PROTEIN; STAT5 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BREAST EPITHELIUM; CONTROLLED STUDY; LACTATION; MAMMARY GLAND ALVEOLOGENESIS; MAMMARY GLAND FUNCTION; MILK PRODUCTION; MORPHOGENESIS; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; DNA PRIMERS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; MICE, KNOCKOUT; PREGNANCY; PROLACTIN; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

MUS;

EID: 84864812813     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.079616     Document Type: Article

References (68)

1. Alcaraz, J., Xu, R., Mori, H., Nelson, C. M., Mroue, R., Spencer, V. A., Brownfield, D., Radisky, D. C., Bustamante, C. and Bissell, M. J. (2008). Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO J. 27, 2829-2838.
2. Anderson, S. M., Rudolph, M. C., McManaman, J. L. and Neville, M. C. (2007). Key stages in mammary gland development. Secretory activation in the mammary gland: it's not just about milk protein synthesis! Breast Cancer Res. 9, 204.
3. Bailey, J. P., Nieport, K. M., Herbst, M. P., Srivastava, S., Serra, R. A. and Horseman, N. D. (2004). Prolactin and transforming growth factor-beta signaling exert opposing effects on mammary gland morphogenesis, involution, and the Akt-forkhead pathway. Mol. Endocrinol. 18, 1171-1184.
4. Bierie, B. and Moses, H. L. (2006). Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat. Rev. Cancer 6, 506-520.
5. Brisken, C., Kaur, S., Chavarria, T. E., Binart, N., Sutherland, R. L., Weinberg, R. A., Kelly, P. A. and Ormandy, C. J. (1999). Prolactin controls mammary gland development via direct and indirect mechanisms. Dev. Biol. 210, 96-106.
6. Bruno, R. D. and Smith, G. H. (2011). Functional characterization of stem cell activity in the mouse mammary gland. Stem Cell Rev. 7, 238-247.
7. Chen, Y. G. and Wang, X. F. (2009). A special issue on TGF-beta signaling. Cell Res. 19, 1-2.
8. 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.
9. Debnath, J., Muthuswamy, S. K. and Brugge, J. S. (2003). Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256-268.
10. Deheuninck, J. and Luo, K. (2009). Ski and SnoN, potent negative regulators of TGF-beta signaling. Cell Res. 19, 47-57.
11. Fata, J. E., Mori, H., Ewald, A. J., Zhang, H., Yao, E., Werb, Z. and Bissell, M. J. (2007). The MAPK(ERK-1,2) pathway integrates distinct and antagonistic signals from TGFalpha and FGF7 in morphogenesis of mouse mammary epithelium. Dev. Biol. 306, 193-207.
12. Feigin, M. E. and Muthuswamy, S. K. (2009). Polarity proteins regulate mammalian cell-cell junctions and cancer pathogenesis. Curr. Opin. Cell Biol. 21, 694-700.
13. Freeman, M. E., Kanyicska, B., Lerant, A. and Nagy, G. (2000). Prolactin: structure, function, and regulation of secretion. Physiol. Rev. 80, 1523-1631.
14. Gallego, M. I., Binart, N., Robinson, G. W., Okagaki, R., Coschigano, K. T., Perry, J., Kopchick, J. J., Oka, T., Kelly, P. A. and Hennighausen, L. (2001). Prolactin, growth hormone, and epidermal growth factor activate Stat5 in different compartments of mammary tissue and exert different and overlapping developmental effects. Dev. Biol. 229, 163-175.
15. Goffin, V., Binart, N., Clément-Lacroix, P., Bouchard, B., Bole-Feysot, C., Edery, M., Lucas, B. K., Touraine, P., Pezet, A., Maaskant, R. et al. (1999). From the molecular biology of prolactin and its receptor to the lessons learned from knockout mice models. Genet. Anal. 15, 189-201.
16. González-Mariscal, L., Tapia, R. and Chamorro, D. (2008). Crosstalk of tight junction components with signaling pathways. Biochim. Biophys. Acta 1778, 729-756.
17. Heldin, C. H., Landström, M. and Moustakas, A. (2009). Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr. Opin. Cell Biol. 21, 166-176.
18. Hennighausen, L. and Robinson, G. W. (2008). Interpretation of cytokine signaling through the transcription factors STAT5A and STAT5B. Genes Dev. 22, 711-721.
19. Inman, J. L. and Bissell, M. J. (2010). Apical polarity in three-dimensional culture systems: where to now? J. Biol. 9, 2.
20. Itoh, M. and Bissell, M. J. (2003). The organization of tight junctions in epithelia: implications for mammary gland biology and breast tumorigenesis. J. Mammary Gland Biol. Neoplasia 8, 449-462.
21. Jahchan, N. S. and Luo, K. (2010). SnoN in mammalian development, function and diseases. Curr. Opin. Pharmacol. 10, 670-675.
22. Jahchan, N. S., You, Y. H., Muller, W. J. and Luo, K. (2010). Transforming growth factor-beta regulator SnoN modulates mammary gland branching morphogenesis, postlactational involution, and mammary tumorigenesis. Cancer Res. 70, 4204-4213.
23. Jhappan, C., Geiser, A. G., Kordon, E. C., Bagheri, D., Hennighausen, L., Roberts, A. B., Smith, G. H. and Merlino, G. (1993). Targeting expression of a transforming growth factor beta 1 transgene to the pregnant mammary gland inhibits alveolar development and lactation. EMBO J. 12, 1835-1845.
24. Katz, E. and Streuli, C. H. (2007). The extracellular matrix as an adhesion checkpoint for mammary epithelial function. Int. J. Biochem. Cell Biol. 39, 715-726.
25. Kelly, P. A., Bachelot, A., Kedzia, C., Hennighausen, L., Ormandy, C. J., Kopchick, J. J. and Binart, N. (2002). The role of prolactin and growth hormone in mammary gland development. Mol. Cell. Endocrinol. 197, 127-131.
26. Kirch, H. C., Putzer, B., Brockmann, D., Esche, H. and Kloke, O. (1997). Formation of the early-region-2 transcription-factor-1-retinoblastoma-protein (E2F- 1-RB) transrepressor and release of the retinoblastoma protein from nuclear complexes containing cyclin A is induced by interferon alpha in U937V cells but not in interferon-alpha-resistant U937VR cells. Eur. J. Biochem. 246, 736-744.
27. Knust, E. (2000). Control of epithelial cell shape and polarity. Curr. Opin. Genet. Dev. 10, 471-475.
28. Krakowski, A. R., Laboureau, J., Mauviel, A., Bissell, M. J. and Luo, K. (2005). Cytoplasmic SnoN in normal tissues and nonmalignant cells antagonizes TGF-beta signaling by sequestration of the Smad proteins. Proc. Natl. Acad. Sci. USA 102, 12437-12442.
29. 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.
30. Luo, K. (2004). Ski and SnoN: negative regulators of TGF-beta signaling. Curr. Opin. Genet. Dev. 14, 65-70.
31. Miyoshi, K., Shillingford, J. M., Smith, G. H., Grimm, S. L., Wagner, K. U., Oka, T., Rosen, J. M., Robinson, G. W. and Hennighausen, L. (2001). Signal transducer and activator of transcription (Stat) 5 controls the proliferation and differentiation of mammary alveolar epithelium. J. Cell Biol. 155, 531-542.
32. Moses, H. and Barcellos-Hoff, M. H. (2011). TGF-beta biology in mammary development and breast cancer. Cold Spring Harb. Perspect. Biol. 3, a003277.
33. Muschler, J. and Streuli, C. H. (2010). Cell-matrix interactions in mammary gland development and breast cancer. Cold Spring Harb. Perspect. Biol. 2, a003202.
34. Muschler, J., Lochter, A., Roskelley, C. D., Yurchenco, P. and Bissell, M. J. (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.
35. Neville, M. C., McFadden, T. B. and Forsyth, I. (2002). Hormonal regulation of mammary differentiation and milk secretion. J. Mammary Gland Biol. Neoplasia 7, 49-66.
36. Nguyen, D. A. and Neville, M. C. (1998). Tight junction regulation in the mammary gland. J. Mammary Gland Biol. Neoplasia 3, 233-246.
37. Nguyen, D. A., Parlow, A. F. and Neville, M. C. (2001). Hormonal regulation of tight junction closure in the mouse mammary epithelium during the transition from pregnancy to lactation. J. Endocrinol. 170, 347-356.
38. Nomura, T., Khan, M. M., Kaul, S. C., Dong, H. D., Wadhwa, R., Colmenares, C., Kohno, I. and Ishii, S. (1999). Ski is a component of the histone deacetylase complex required for transcriptional repression by Mad and thyroid hormone receptor. Genes Dev. 13, 412-423.
39. Novaro, V., Roskelley, C. D. and Bissell, M. J. (2003). Collagen-IV and laminin-1 regulate estrogen receptor alpha expression and function in mouse mammary epithelial cells. J. Cell Sci. 116, 2975-2986.
40. Oakes, S. R., Hilton, H. N. and Ormandy, C. J. (2006). The alveolar switch: coordinating the proliferative cues and cell fate decisions that drive the formation of lobuloalveoli from ductal epithelium. Breast Cancer Res. 8, 207.
41. Oakes, S. R., Rogers, R. L., Naylor, M. J. and Ormandy, C. J. (2008). Prolactin regulation of mammary gland development. J. Mammary Gland Biol. Neoplasia 13, 13-28.
42. Onishi, M., Nosaka, T., Misawa, K., Mui, A. L., Gorman, D., McMahon, M., Miyajima, A. and Kitamura, T. (1998). Identification and characterization of a constitutively active STAT5 mutant that promotes cell proliferation. Mol. Cell. Biol. 18, 3871-3879.
43. 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.
44. Palmer, C. A., Lubon, H. and McManaman, J. L. (2003). Transgenic mice expressing recombinant human protein C exhibit defects in lactation and impaired mammary gland development. Transgenic Res. 12, 283-292.
45. Palmer, C. A., Neville, M. C., Anderson, S. M. and McManaman, J. L. (2006). Analysis of lactation defects in transgenic mice. J. Mammary Gland Biol. Neoplasia 11, 269-282.
46. Pan, D., Zhu, Q. and Luo, K. (2009). SnoN functions as a tumour suppressor by inducing premature senescence. EMBO J. 28, 3500-3513.
47. Pearson-White, S. and Crittenden, R. (1997). Proto-oncogene Sno expression, alternative isoforms and immediate early serum response. Nucleic Acids Res. 25, 2930-2937.
48. Pearson-White, S. and McDuffie, M. (2003). Defective T-cell activation is associated with augmented transforming growth factor Beta sensitivity in mice with mutations in the Sno gene. Mol. Cell. Biol. 23, 5446-5459.
49. Pierce, D. F., Jr, Johnson, M. D., Matsui, Y., Robinson, S. D., Gold, L. I., Purchio, A. F., Daniel, C. W., Hogan, B. L. and Moses, H. L. (1993). Inhibition of mammary duct development but not alveolar outgrowth during pregnancy in transgenic mice expressing active TGF-beta 1. Genes Dev. 7, 2308-2317.
50. Richert, M. M., Schwertfeger, K. L., Ryder, J. W. and Anderson, S. M. (2000). An atlas of mouse mammary gland development. J. Mammary Gland Biol. Neoplasia 5, 227-241.
51. Robinson, S. D., Silberstein, G. B., Roberts, A. B., Flanders, K. C. and Daniel, C. W. (1991). Regulated expression and growth inhibitory effects of transforming growth factor-beta isoforms in mouse mammary gland development. Development 113, 867-878.
52. Rosen, J. M., Wyszomierski, S. L. and Hadsell, D. (1999). Regulation of milk protein gene expression. Annu. Rev. Nutr. 19, 407-436.
53. Schwertfeger, K. L., McManaman, J. L., Palmer, C. A., Neville, M. C. and Anderson, S. M. (2003). Expression of constitutively activated Akt in the mammary gland leads to excess lipid synthesis during pregnancy and lactation. J. Lipid Res. 44, 1100-1112.
54. Siegel, P. M., Shu, W., Cardiff, R. D., Muller, W. J. and Massagué, J. (2003). Transforming growth factor beta signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis. Proc. Natl. Acad. Sci. USA 100, 8430-8435.
55. Stelwagen, K., McFadden, H. A. and Demmer, J. (1999). Prolactin, alone or in combination with glucocorticoids, enhances tight junction formation and expression of the tight junction protein occludin in mammary cells. Mol. Cell. Endocrinol. 156, 55-61.
56. Streuli, C. H. and Bissell, M. J. (1990). Expression of extracellular matrix components is regulated by substratum. J. Cell Biol. 110, 1405-1415.
57. Streuli, C. H. and Akhtar, N. (2009). Signal co-operation between integrins and other receptor systems. Biochem. J. 418, 491-506.
58. Streuli, C. H., Bailey, N. and Bissell, M. J. (1991). Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. J. Cell Biol. 115, 1383-1395.
59. Teglund, S., McKay, C., Schuetz, E., van Deursen, J. M., Stravopodis, D., Wang, D., Brown, M., Bodner, S., Grosveld, G. and Ihle, J. N. (1998). Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 93, 841-850.
60. Tian, M. and Schiemann, W. P. (2009). The TGF-beta paradox in human cancer: an update. Future Oncol. 5, 259-271.
61. 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.
62. Vasioukhin, V. and Fuchs, E. (2001). Actin dynamics and cell-cell adhesion in epithelia. Curr. Opin. Cell Biol. 13, 76-84.
63. Wagner, K. U., Young, W. S., 3rd, Liu, X., Ginns, E. I., Li, M., Furth, P. A. and Hennighausen, L. (1997). Oxytocin and milk removal are required for postpartum mammary-gland development. Genes Funct. 1, 233-244.
64. Watkin, H., Richert, M. M., Lewis, A., Terrell, K., McManaman, J. P. and Anderson, S. M. (2008). Lactation failure in Src knockout mice is due to impaired secretory activation. BMC Dev. Biol. 8, 6.
65. Xu, R., Boudreau, A. and Bissell, M. J. (2009a). Tissue architecture and function: dynamic reciprocity via extra- and intra-cellular matrices. Cancer Metastasis Rev. 28, 167-176.
66. Xu, R., Nelson, C. M., Muschler, J. L., Veiseh, M., Vonderhaar, B. K. and Bissell, M. J. (2009b). Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function. J. Cell Biol. 184, 57-66.
67. Zhu, Q., Pearson-White, S. and Luo, K. (2005). Requirement for the SnoN oncoprotein in transforming growth factor beta-induced oncogenic transformation of fibroblast cells. Mol. Cell. Biol. 25, 10731-10744.
68. Zhu, Q., Krakowski, A. R., Dunham, E. E., Wang, L., Bandyopadhyay, A., Berdeaux, R., Martin, G. S., Sun, L. and Luo, K. (2007). Dual role of SnoN in mammalian tumorigenesis. Mol. Cell. Biol. 27, 324-339.