C/EBPβ, but not C/EBPα, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland

Genes and Development

Volumn 12, Issue 12, 1998, Pages 1917-1928

  Seagroves, Tiffany N ^a   Krnacik, Susanne ^a   Raught, Brian ^a,b   Gay, Jason ^a   Burgess Beusse, Bonnie ^a   Darlington, Gretchen J ^a   Rosen, Jeffrey M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

C EBP; Ductal growth; Lactogenesis; Mammary development; Whey acidic protein; casein

Indexed keywords

BETA CASEIN; CASEIN; CCAAT ENHANCER BINDING PROTEIN; DNA BINDING PROTEIN; ESTROGEN; MESSENGER RNA; MILK PROTEIN; NUCLEAR PROTEIN; PROGESTERONE; TRANSCRIPTION FACTOR; WHEY ACIDIC PROTEINS;

ANIMAL CELL; ARTICLE; BREAST CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE ACTIVATION; GENE DELETION; HORMONAL REGULATION; MAMMARY GLAND; MILK PRODUCTION; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL DIVISION; DRUG ANTAGONISM; DRUG EFFECT; EPITHELIUM; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MOUSE MUTANT; MOUSE STRAIN; MUTATION; NORTHERN BLOTTING; PHYSIOLOGY; PREGNANCY; TISSUE TRANSPLANTATION; TRANSPLANTATION; UDDER;

ANIMALIA; MUS MUSCULUS; RODENTIA; VERTEBRATA;

ANIMALS; APOPTOSIS; BLOTTING, NORTHERN; CASEINS; CCAAT-ENHANCER-BINDING PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; DNA-BINDING PROTEINS; EPITHELIAL CELLS; EPITHELIUM; ESTROGENS; FEMALE; GENE DELETION; GENE EXPRESSION; MALE; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, MUTANT STRAINS; MILK PROTEINS; MORPHOGENESIS; MUTATION; NUCLEAR PROTEINS; PREGNANCY; PROGESTERONE; RNA, MESSENGER; TISSUE TRANSPLANTATION; TRANSCRIPTION FACTORS;

EID: 0032525340     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.12.1917     Document Type: Article

References (58)

1. Alam, T., M.R. An, and J. Papaconstantinou. 1992. Differential expression of three C/EBP isoforms in multiple tissues during the acute phase response. J. Biol. Chem. 267: 5021-5024.
2. Bissell, M.J. and J. Aggeler. 1987. Dynamic reciprocity: How do extracellular matrix and hormones direct gene expression? Prog. Clin. Biol. Res. 249: 251-262.
3. Biais, S., F. Boudreau, J.F. Beaulieu, and C. Asselin. 1995. CCAAT/enhancer binding protein isoforms expression in the colon of neonatal mice. Dev. Dyn. 204: 66-76.
4. Buck, M., H. Turler, and M. Chojkier. 1994. LAP (NF-IL-6), a tissue-specific transcriptional activator, is an inhibitor of hepatoma cell proliferation. EMBO J. 13: 851-860.
5. Cao, Z., R.M. Umek, and S.L. McKnight. 1991. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes & Dev. 5: 1538-1552.
6. Chen, P.L., D.J. Riley, Y. Chen, and W.H. Lee. 1996a. Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs. Genes & Dev. 10: 2794-2804.
7. Chen, P.L., D.J. Riley, S. Chen-Kiang, and W.H. Lee. 1996b. Retinoblastoma protein directly interacts with and activates the transcription factor NF-IL6. Proc. Natl. Acad. Sci. 93: 465-469.
8. Church, G.M. and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. 81: 1991-1995.
9. DeOme, K.B., L.J. Fauklin, H.A. Bern, and P.B. Blair. 1959. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res. 78: 515-520.
10. Descombes, P. and U. Schibler. 1991. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67: 569-579.
11. Diehl, A.M., P. Michaelson, and S.Q. Yang. 1994. Selective induction of CCAAT/enhancer binding protein isoforms occurs during rat liver development. Gastroenterology 106: 1625-1637.
12. Fantl, V., G. Stamp, A. Andrews, I. Rosewell, and C. Dickson. 1995. Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes &. Dev. 9: 2364-2372.
13. Gigliotti, A.P. and J.W. DeWille. 1998. Lactation status influences expression of CCAAT/enhancer binding protein isoform mRNA in the mouse mammary gland. J. Cell Physiol. 174: 232-239.
14. Hendricks-Taylor, L.R. and G.J. Darlington. 1995. Inhibition of cell proliferation by C/EBPa occurs in many cell types, does not require the presence of p53 or Rb, and is not affected by large T-antigen. Nucleic Acids Res. 23: 4726-4733.
15. Hennighausen, L. and G.W. Robinson. 1998. Think globally, act locally: The making of a mouse mammary gland. Genes &. Dev. 12: 449-455.
16. Hu, Z., L. Zhuang, X. Guan, J. Yneng, and M.L. Dufau. 1997. Steroidogenic factor-1 is an essential transcriptional activator for gonad-specific expression of promoter I of the rat prolactin receptor gene. J. Biol. Chem. 272: 14263-14271.
17. Humphreys, R.C., M. Krajewska, S. Krnacik, R. Jaeger, H. Weiher, S. Krajewski, J.C. Reed, and J.M. Rosen. 1996. Apoptosis in the terminal endbud of the murine mammary gland: A mechanism of ductal morphogenesis. Development 122: 4013-4022.
18. Jackson, D., J. Bresnick, I. Rosewell, T. Crafton, R. Poulsom, G. Stamp, and C. Dickson. 1997. Fibroblast growth factor receptor signalling has a role in lobuloalveolar development of the mammary gland. J. Cell. Sci. 110: 1261-1268.
19. Kaetzel, C.S. and D.B. Ray. 1984. Immunochemical characterization with monoclonal antibodies of three major caseins and alpha-lactalbumin from rat milk. J. Dairy Sci. 67: 64-75.
20. Kel, O.V., A.G. Romaschenko, A.E. Kel, E. Wingender, and N.A. Kolchanov. 1995. A compilation of composite response regulatory elements affecting gene transcription in vertebrates. Nucleic Acids Res. 23: 4097-4103.
21. Landschulz, W.H., P.F. Johnson, E.Y. Adashi, B.J. Graves, and S.L. McKnight. 1988. Isolation of a recombinant copy of the gene encoding C/EBP. Genes &. Dev. 2: 786-800.
22. Lee, Y.H., S.C. Williams, M. Baer, E. Sterneck, F.J. Gonzalez, and P.F. Johnson. 1997. The ability of C/EBP beta but not C/EBP alpha to synergize with an Sp1 protein is specified by the leucine zipper and activation domain. Mol. Cell. Biol. 17: 2038-2047.
23. Lin, F.T. and M.D. Lane. 1994. CCAAT/enhancer binding protein alpha is sufficient to initiate the 3T3-L1 adipocyte differentiation program. Proc. Natl. Acad. Sci. 91: 8757-8761.
24. Lin, F.T., O.A. MacDougald, A.M. Diehl, and M.D. Lane. 1993. A 30-kDa alternative translation product of the CCAAT/ enhancer binding protein alpha message: Transcriptional activator lacking antimitotic activity. Proc. Natl. Acad. Sci. 90: 9606-9610.
25. Lin, X., G.W. Robinson, K.U. Wagner, L. Garrett, A. Wynshaw-Boris, and L. Hennighausen. 1997. Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes & Dev. 11: 179-186.
26. Lydon, J.P., F.J. DeMayo, C.R. Funk, S.K. Mani, A.R. Hughes, C.A. Montgomery, Jr., G. Shyamala, O.M. Conneely, and B.W. O'Malley. 1995. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes & Dev. 9: 2266-2278.
27. Murphy, A.M., T. Lee, C.M. Andrews, B.Z. Shilo, and D.J. Montell. 1995. The breathless FGF receptor homolog, a downstream target of Drosophila C/EBP in the developmental control of cell migration. Development 121: 2255-2263.
28. Ormandy, C.J., A. Camus, J. Barra, D. Damotte, B. Lucas, H. Buteau, M. Edery, N. Brousse, C. Babinet, N. Binart, and P.A. Kelly. 1997. Null mutation of the prolactin receptor gene produces multiple reproductive detects in the mouse. Genes & Dev. 11: 167-178.
29. Ossipow, V., P. Descombes, and U. Schibler. 1993. CCAAT/ enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials. Proc. Natl. Acad. Sci. 90: 8219-8223.
30. Piontkewitz, Y., S. Enerback, and L. Hedin. 1993. Expression and hormonal regulation of the CCAAT enhancer binding protein-alpha during differentiation of rat ovarian follicles. Endocrinology 133: 2327-2333.
31. Pullan, S.E. and C.H. Streuli. 1996. The mammary gland epithelial cell. In Epithelial cell culture (ed. A. Harris), pp. 97-121. Cambridge University Press, Cambridge, UK.
32. Rana, B., D. Mischoulon, Y. Xie, N.L. Bucher, and S.R. Farmer. 1994. Cell-extracellular matrix interactions can regulate the switch between growth and differentiation in rat hepatocytes: Reciprocal expression of C/EBPα and immediate-early growth response transcription factors. Mol. Cell. Biol. 14: 5858-5869.
33. Raught, B., W.S. Liao, and J.M. Rosen. 1995. Developmentally and hormonally regulated CCAAT/enhancer-binding protein isoforms influence beta-casein gene expression. Mol. Endocrinol. 9: 1223-1232.
34. Raught, B., A.C. Gingras, A. James, D. Medina, N. Sonenberg, and J.M. Rosen. 1996. Expression of a translationally regulated, dominant-negative CCAAT/enhancer-bindmg protein β isoform and up-regulation of the eukaryotic translation initiation factor 2α are correlated with neoplastic transformation of mammary epithelial cells. Cancer Res. 56: 4382-4386.
35. Reichman-Fried, M. and B.Z. Shilo. 1995. Breathless, a Drosophila FGF receptor homolog, is required for the onset of tracheal cell migration and tracheole formation. Mech. Dev. 52: 265-273.
36. Reichman-Fried, M., B. Dickson, E. Hafen, and B.Z. Shilo. 1994. Elucidation of the role of breathless, a Drosophila FGF receptor homolog, in tracheal cell migration. Genes & Dev. 8: 428-439.
37. Robinson, G.W., P.F. Johnson, L. Hennighausen, and E. Sterneck. 1998. The C/EBPβ transcription factor regulates epithelial cell proliferation and differentiation in the mammary gland. Genes & Dev. (this issue).
38. Roop, D.R., C.K. Cheng, L. Titterington, C.A. Meyers, J.R. Stanley, P.M. Steinert, and S.H. Yuspa. 1984. Synthetic peptides corresponding to keratin subunits elicit highly specific antibodies. J. Biol. Chem. 259: 8037-8040.
39. Rosen, J.M., C. Zahnow, A. Kazansky, and B. Raught. 1997. Composite response elements mediate hormonal and developmental regulation of milk protein gene expression. Biochem. Soc. Symp. 63: 101-113.
40. Roskelley, C.D., A. Srebrow, and M.J. Bissell. 1995. A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression. Curr. Opin. Cell Biol. 7: 736-747.
41. Samakovlis, C., N. Hacohen, G. Manning, D.C. Sutherland, K. Guillemin, and M.A. Krasnow. 1996. Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122: 1395-1407.
42. Screpanti, I., L. Romani, P. Musiani, A. Modesti, E. Fattori, D. Lazzaro, C. Sellitto, S. Scarpa, D. Bellavia, G. Lattanzio, et al. 1995. Lymphoproliferative disorder and imbalanced T-helper response in C/EBPβ-deficient mice. EMBO J. 14: 1932-1941.
43. Shamay, A., V.G. Pursel, E. Wilkinson, R.J. Wall, and L. Hennighausen. 1992. Expression of the whey acidic protein in transgenic pigs impairs mammary development. Transgenic Res. 1: 124-132.
44. Sicinski, P., J.L. Donaher, S.B. Parker, T. Li, A. Fazelli, H. Gardner, S.Z. Haslam, R.T. Bronson, S.J. Elledge, and R.A. Weinberg. 1995. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82: 621-630.
45. Sterneck, E., L. Tessarollo, and P.F. Johnson. 1997. An essential role for C/EBPβ in female reproduction. Genes & Dev. 11: 2153-2162.
46. Tanaka, T., S. Akira, K. Yoshida, M. Umemoto, Y. Yoneda, N. Shirafuji, H. Fujiwara, S. Suematsu, N. Yoshida, and T. Kishimoto. 1995. Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages. Cell 80: 353-361.
47. Tanaka, T., N. Yoshida, T. Kishimoto, and S. Akira. 1997. Defective adipocyte differentiation in mice lacking the C/EBPβ and/or C/EBPδ gene. EMBO J. 16: 7432-7443.
48. Timchenko, N.A., T.E. Harris, M. Wilde, T.A. Bilyeu, B.L. Burgess-Beusse, M.J. Finegold, and G.J. Darlington. 1997. CCAAT/enhancer binding protein alpha regulates p21 protein and hepatocyte proliferation in newborn mice. Mol. Cell Biol. 17: 7353-7361.
49. Toscani, A., R.V. Mettus, R. Coupland, H. Simpkins, J. Litvin, J. Orth, K.S. Hatton, and E.P. Reddy. 1997. Arrest of spermatogenesis and defective breast development in mice lacking A-myb. Nature 386: 713-717.
50. Udy, G.A., R.P. Towers, R.G. Snell, R.J. Wilkins, S.-H. Park, P. Ram, D.J. Waxman, and H.W. Davey. 1997. Requirement for STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc. Natl. Acad. Sci. 94: 7239-7244.
51. Umek, R.M., A.D. Friedman, and S.L. McKnight. 1991. CCAAT-enhancer binding protein: A component of a differentiation switch. Science 251: 288-292.
52. Wang, N.D., M.J. Finegold, A. Bradley, C.N. Ou, S.V. Abdelsayed, M.D. Wilde, L.R. Taylor, D.R. Wilson, and G.J. Darlington. 1995. Impaired energy homeostasis in C/EBP alpha knockout mice. Science 269: 1108-1112.
53. Williams, S.C., C.A. Cantwell, and P.F. Johnson. 1991. A family of C/EBP-related proteins capable of forming covalently linked leucine zipper dimers in vitro. Genes & Dev. 5: 1553-1567.
54. Williams, S.C., M. Baer, A.J. Dillner, and P.F. Johnson. 1995. CRP2 (C/EBP beta) contains a bipartite regulatory domain that controls transcriptional activation, DNA binding and cell specificity. EMBO J. 14: 3170-3183.
55. Yeh, W.C., Z. Cao, M. Classon, and S.L. McKnight. 1995. Cascade regulation of terminal adipocyte differentiation by three members of the C/EBP family of leucine zipper proteins. Genes & Dev. 9: 168-181.
56. Yi, E.S., A.A. Bedoya, H. Lee, S. Kim, R.M. Housley, S.L. Aukerman, J.E. Tarpley, C. Starnes, S. Yin, G.F. Pierce, et al. 1994. Keratinocyte growth factor causes cystic dilation of the mammary glands of mice. Interactions of keratinocyte growth factor, estrogen, and progesterone in vivo. Am. J. Pathol. 145: 1015-1022.
57. Zahnow, C.A., P. Younes, R. Laucirica, and J.M. Rosen. 1997. Overexpression of C/EBPβ-LIP, a naturally occurring, dominant-negative transcription factor, in human breast cancer. J. Natl. Cancer Inst. 89: 1887-1891.
58. Zhang, D.E., P. Zhang, N.D. Wang, C.J. Hetherington, G.J. Darlington, and D.G. Tenen. 1997. Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Proc. Natl. Acad. Sci. 94: 569-574.