The Homeodomain Protein CDP Regulates Mammary-Specific Gene Transcription and Tumorigenesis

REFERENCES

• Ai, W., Toussaint E., and Roman A.. 1999. CCAAT displacement protein binds to and negatively regulates human papillomavirus type 6 E6, E7, and E1 promoters. J. Virol. 73:4220–4229.
   PubMedGoogle Scholar
• Aufiero, B., Neufeld E. J., and Orkin S. H.. 1994. Sequence-specific DNA binding of individual cut repeats of the human CCAAT displacement/cut homeodomain protein. Proc. Natl. Acad. Sci. USA 91:7757–7761.
   PubMedGoogle Scholar
• Banan, M., Rojas I. C., Lee W. H., King H. L., Harriss J. V., Kobayashi R., Webb C. F., and Gottlieb P. D.. 1997. Interaction of the nuclear matrix-associated region (MAR)-binding proteins, SATB1 and CDP/Cux, with a MAR element (L2a) in an upstream regulatory region of the mouse CD8α gene. J. Biol. Chem. 272:18440–18452.
   PubMedGoogle Scholar
• Barberis, A., Superti-Furga G., and Busslinger M.. 1987. Mutually exclusive interaction of the CCAAT-binding factor and of a displacement protein with overlapping sequences of a histone gene promoter. Cell 50:347–359.
   PubMed Web of Science ®Google Scholar
• Bodmer, R., Barbel S., Sheperd S., Jack J. W., Jan L. Y., and Jan Y. N.. 1987. Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell 51:293–307.
   PubMedGoogle Scholar
• Campbell, S. M., Rosen J. M., Hennighausen L. G., Strech-Jurk U., and Sippel A. E.. 1984. Comparison of the whey acidic protein genes of the rat and mouse. Nucleic Acids Res. 12:8685–8697.
   PubMedGoogle Scholar
• Chattopadhyay, S., Whitehurst C. E., and Chen J.. 1998. A nuclear matrix attachment region upstream of the T cell receptor β gene enhancer binds Cux/CDP and SATB1 and modulates enhancer-dependent reporter gene expression but not endogenous gene expression. J. Biol. Chem. 273:29838–29846.
   PubMedGoogle Scholar
• Cho, K., Ferrick D. A., and Morris D. W.. 1995. Structure and biological activity of the subgenomic Mtv-6 endogenous provirus. Virology 206:395–402.
   PubMedGoogle Scholar
• Choi, Y., Kappler J. W., and Marrack P.. 1991. A superantigen encoded in the open reading frame of the 3′ long terminal repeat of mouse mammary tumour virus. Nature 350:203–207.
   PubMed Web of Science ®Google Scholar
• Doppler, W., Welte T., and Philipp S.. 1995. CCAAT/enhancer-binding protein isoforms beta and delta are expressed in mammary epithelial cells and bind to multiple sites in the β-casein gene promoter. J. Biol. Chem. 270:17962–17969.
   PubMed Web of Science ®Google Scholar
• Dudley, J. P. 1999. Mouse mammary tumor virus, p. 965–972. In Webster R. G. and Granoff A. (ed.), Encyclopedia of virology. Academic Press Ltd., London, United Kingdom.
   Google Scholar
• Dufort, D., and Nepveu A.. 1994. The human cut homeodomain protein represses transcription from the c-myc promoter. Mol. Cell. Biol. 14:4251–4257.
   PubMedGoogle Scholar
• Durban, E. M., Knepper J. E., Medina D., and Butel J. S.. 1990. Influence of mammary cell differentiation on the expression of proteins encoded by endogenous BALB/c mouse mammary tumor virus genes. Virus Res. 16:307–323.
   PubMedGoogle Scholar
• Ellis, T., Gambardella L., Horcher M., Tschanz S., Capol J., Bertram P., Jochum W., Barrandon Y., and Busslinger M.. 2001. The transcriptional repressor CDP (Cutl1) is essential for epithelial cell differentiation of the lung and the hair follicle. Genes Dev. 15:2307–2319.
   PubMed Web of Science ®Google Scholar
• Gilead, Z., Jeng Y. H., Wold W. S., Sugawara K., Rho H. M., Harter, L. M., and Green M.. 1976. Immunological identification of two adenovirus 2-induced early proteins possibly involved in cell transformation. Nature 264:263–266.
   PubMedGoogle Scholar
• Golovkina, T. V., Chervonsky A., Dudley J. P., and Ross S. R.. 1992. Transgenic mouse mammary tumor virus superantigen expression prevents viral infection. Cell 69:637–645.
   PubMed Web of Science ®Google Scholar
• Hennighausen, L. G., Steudle A., and Sippel A. E.. 1982. Nucleotide sequence of cloned cDNA coding for mouse epsilon casein. Eur. J. Biochem. 126:569–572.
   PubMedGoogle Scholar
• Hsu, C. L., Fabritius C., and Dudley J.. 1988. Mouse mammary tumor virus proviruses in T-cell lymphomas lack a negative regulatory element in the long terminal repeat. J. Virol. 62:4644–4652.
   PubMedGoogle Scholar
• Jackson, R. J., Antonia S. J., Wright K. L., Moon N. S., Nepveu A., and Munoz-Antonia T.. 1999. Human cut-like repressor protein binds TGFβ type II receptor gene promoter. Arch. Biochem. Biophys. 371:290–300.
   PubMedGoogle Scholar
• Khanna-Gupta, A., Zibello T., Sun H., Gaines P., and Berliner N.. 2003. Chromatin immunoprecipitation (ChIP) studies indicate a role for CCAAT enhancer binding proteins alpha and epsilon (C/EBPα and C/EBPε) and CDP/cut in myeloid maturation-induced lactoferrin gene expression. Blood 101:3460–3468.
   PubMedGoogle Scholar
• Khanna-Gupta, A., Zibello T., Sun H., Lekstrom-Himes J., and Berliner N.. 2001. C/EBP ε mediates myeloid differentiation and is regulated by the CCAAT displacement protein (CDP/cut). Proc. Natl. Acad. Sci. USA 98:8000–8005.
   PubMedGoogle Scholar
• Lievens, P. M., Donady J. J., Tufarelli C., and Neufeld E. J.. 1995. Repressor activity of CCAAT displacement protein in HL-60 myeloid leukemia cells. J. Biol. Chem. 270:12745–12750.
   PubMedGoogle Scholar
• Liu, J., Barnett A., Neufeld E. J., and Dudley J. P.. 1999. Homeoproteins CDP and SATB1 interact: potential for tissue-specific regulation. Mol. Cell. Biol. 19:4918–4926.
   PubMedGoogle Scholar
• Liu, J., Bramblett D., Zhu Q., Lozano M., Kobayashi R., Ross S. R., and Dudley J. P.. 1997. The matrix attachment region-binding protein SATB1 participates in negative regulation of tissue-specific gene expression. Mol. Cell. Biol. 17:5275–5287.
   PubMed Web of Science ®Google Scholar
• Liu, S., McLeod E., and Jack J.. 1991. Four distinct regulatory regions of the cut locus and their effect on cell type specification in Drosophila. Genetics 127:151–159.
   PubMedGoogle Scholar
• Luong, M. X., van der Meijden C. M., Xing D., Hesselton R., Monuki E. S., Jones S. N., Lian J. B., Stein J. L., Stein G. S., Neufeld E. J., and van Wijnen A. J.. 2002. Genetic ablation of the CDP/Cux protein C terminus results in hair cycle defects and reduced male fertility. Mol. Cell. Biol. 22:1424–1437.
   PubMedGoogle Scholar
• Moon, N. S., Berube G., and Nepveu A.. 2000. CCAAT displacement activity involves CUT repeats 1 and 2, not the CUT homeodomain. J. Biol. Chem. 275:31325–31334.
   PubMedGoogle Scholar
• Moon, N. S., Rong Z. W., Premdas P., Santaguida M., Berube G., and Nepveu A.. 2002. Expression of N-terminally truncated isoforms of CDP/CUX is increased in human uterine leiomyomas. Int. J. Cancer 100:429–432.
   PubMed Web of Science ®Google Scholar
• Morrison, B. W., and Leder P.. 1994. neu and ras initiate murine mammary tumors that share genetic markers generally absent in c-myc and int-2-initiated tumors. Oncogene 9:3417–3426.
   PubMed Web of Science ®Google Scholar
• Mustafa, F., Bhadra S., Johnston D., Lozano M., and Dudley J. P.. 2003. The type B leukemogenic virus truncated superantigen is dispensable for T-cell lymphomagenesis. J. Virol. 77:3866–3870.
   PubMedGoogle Scholar
• Mustafa, F., Lozano M., and Dudley J. P.. 2000. C3H mouse mammary tumor virus superantigen function requires a splice donor site in the envelope gene. J. Virol. 74:9431–9440.
   PubMedGoogle Scholar
• Nepveu, A. 2001. Role of the multifunctional CDP/Cut/Cux homeodomain transcription factor in regulating differentiation, cell growth and development. Gene 270:1–15.
   PubMedGoogle Scholar
• O'Connor, M. J., Stunkel W., Koh C. H., Zimmermann H., and Bernard H. U.. 2000. The differentiation-specific factor CDP/Cut represses transcription and replication of human papillomaviruses through a conserved silencing element. J. Virol. 74:401–410.
   PubMedGoogle Scholar
• Pattison, S., Skalnik D. G., and Roman A.. 1997. CCAAT displacement protein, a regulator of differentiation-specific gene expression, binds a negative regulatory element within the 5′ end of the human papillomavirus type 6 long control region. J. Virol. 71:2013–2022.
   PubMedGoogle Scholar
• Rabson, A. B., and Graves B. J.. 1997. Synthesis and processing of viral RNA, p. 205–261. In Coffin J. M., Hughes S. H., and Varmus H. E. (ed.), Retroviruses. Cold Spring Harbor Laboratory Press, New York, N.Y.
   Google Scholar
• Robinson, G. W., Johnson P. F., Hennighausen L., and Sterneck E.. 1998. The C/EBPβ transcription factor regulates epithelial cell proliferation and differentiation in the mammary gland. Genes Dev. 12:1907–1916.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Rosen, J. M., Wyszomierski S. L., and Hadsell D.. 1999. Regulation of milk protein gene expression. Annu. Rev. Nutr. 19:407–436.
   PubMedGoogle Scholar
• Seagroves, T. N., Krnacik S., Raught B., Gay J., Burgess B., Darlington G. J., and Rosen J. M.. 1998. C/EBPβ, but not C/EBPα, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev. 12:1917–1928.
   PubMedGoogle Scholar
• Shackleford, G. M., MacArthur C. A., Kwan H. C., and Varmus H. E.. 1993. Mouse mammary tumor virus infection accelerates mammary carcinogenesis in Wnt-1 transgenic mice by insertional activation of int-2/Fgf-3 and hst/Fgf-4. Proc. Natl. Acad. Sci. USA 90:740–744.
   PubMed Web of Science ®Google Scholar
• Shackleford, G. M., and Varmus H. E.. 1988. Construction of a clonable, infectious, and tumorigenic mouse mammary tumor virus provirus and a derivative genetic vector. Proc. Natl. Acad. Sci. USA 85:9655–9659.
   PubMed Web of Science ®Google Scholar
• Sinclair, A. M., Lee J. A., Goldstein A., Xing D., Liu S., Ju R., Tucker P. W., Neufeld E. J., and Scheuermann R. H.. 2001. Lymphoid apoptosis and myeloid hyperplasia in CCAAT displacement protein mutant mice. Blood 98:3658–3667.
   PubMedGoogle Scholar
• Tufarelli, C., Fujiwara Y., Zappulla D. C., and Neufeld E. J.. 1998. Hair defects and pup loss in mice with targeted deletion of the first cut repeat domain of the Cux/CDP homeoprotein gene. Dev. Biol. 200:69–81.
   PubMedGoogle Scholar
• Vanden Heuvel, G. B., Bodmer R., McConnell K. R., Nagami G. T., and Igarashi P.. 1996. Expression of a cut-related homeobox gene in developing and polycystic mouse kidney. Kidney Int. 50:453–461.
   PubMedGoogle Scholar
• Vilotte, J. L., and Soulier S.. 1992. Isolation and characterization of the mouse α-lactalbumin-encoding gene: interspecies comparison, tissue- and stage-specific expression. Gene 119:287–292.
   PubMedGoogle Scholar
• Wang, Z., Goldstein A., Zong R. T., Lin D., Neufeld E. J., Scheuermann R. H., and Tucker P. W.. 1999. Cux/CDP homeoprotein is a component of NF-μNR and represses the immunoglobulin heavy chain intronic enhancer by antagonizing the bright transcription activator. Mol. Cell. Biol. 19:284–295.
   PubMedGoogle Scholar
• Webster, M. A., Martin-Soudant N., Nepveu A., Cardiff R. D., and Muller W. J.. 1998. The induction of uterine leiomyomas and mammary tumors in transgenic mice expressing polyomavirus (PyV) large T (LT) antigen is associated with the ability of PyV LT antigen to form specific complexes with retinoblastoma and CUTL1 family members. Oncogene 16:1963–1972.
   PubMedGoogle Scholar
• Wrona, T. J., Lozano M., Binhazim A. A., and Dudley J. P.. 1998. Mutational and functional analysis of the C-terminal region of the C3H mouse mammary tumor virus superantigen. J. Virol. 72:4746–4755.
   PubMedGoogle Scholar
• Xu, L., Wrona T. J., and Dudley J. P.. 1996. Exogenous mouse mammary tumor virus (MMTV) infection induces endogenous MMTV sag expression. Virology 215:113–123.
   PubMedGoogle Scholar
• Xu, L., Wrona T. J., and Dudley J. P.. 1997. Strain-specific expression of spliced MMTV RNAs containing the superantigen gene. Virology 236:54–65.
   PubMedGoogle Scholar
• Yoshimura, M., and Oka T.. 1989. Isolation and structural analysis of the mouse beta-casein gene. Gene 78:267–275.
   PubMed Web of Science ®Google Scholar
• Zeng, W. R., Scherer S. W., Koutsilieris M., Huizenga J. J., Filteau F., Tsui L. C., and Nepveu A.. 1997. Loss of heterozygosity and reduced expression of the CUTL1 gene in uterine leiomyomas. Oncogene 14:2355–2365.
   PubMedGoogle Scholar
• Zeng, W. R., Watson P., Lin J., Jothy S., Lidereau R., Park M., and Nepveu A.. 1999. Refined mapping of the region of loss of heterozygosity on the long arm of chromosome 7 in human breast cancer defines the location of a second tumor suppressor gene at 7q22 in the region of the CUTL1 gene. Oncogene 18:2015–2021.
   PubMedGoogle Scholar
• Zhu, Q., and Dudley J. P.. 2002. CDP binding to multiple sites in the mouse mammary tumor virus long terminal repeat suppresses basal and glucocorticoid-induced transcription. J. Virol. 76:2168–2179.
   PubMedGoogle Scholar
• Zhu, Q., Gregg K., Lozano M., Liu J., and Dudley J. P.. 2000. CDP is a repressor of mouse mammary tumor virus expression in the mammary gland. J. Virol. 74:6348–6357.
   PubMedGoogle Scholar