Oct-1 Counteracts Autoinhibition of Runx2 DNA Binding To Form a Novel Runx2/Oct-1 Complex on the Promoter of the Mammary Gland-Specific Gene β-casein

REFERENCES

• Alliston, T., L. Choy, P. Ducy, G. Karsenty, and R. Derynck. 2001. TGF-beta-induced repression of CBFA1 by Smad3 decreases cbfa1 and osteocalcin expression and inhibits osteoblast differentiation. EMBO J. 20:2254–2272.
   PubMed Web of Science ®Google Scholar
• Ball, R. K., R. R. Friis, C. A. Schoenenberger, W. Doppler, and B. Groner. 1988. Prolactin regulation of beta-casein gene expression and of a cytosolic 120-kd protein in a cloned mouse mammary epithelial cell line. EMBO J. 7:2089–2095.
   PubMed Web of Science ®Google Scholar
• Barnes, G. L., K. E. Hebert, M. Kamal, A. Javed, T. A. Einhorn, J. B. Lian, G. S. Stein, and L. C. Gerstenfeld. 2004. Fidelity of Runx2 activity in breast cancer cells is required for the generation of metastases-associated osteolytic disease. Cancer Res. 64:4506–4513.
   PubMedGoogle Scholar
• Barnes, G. L., A. Javed, S. M. Waller, M. H. Kamal, K. E. Hebert, M. Q. Hassan, A. Bellahcene, A. J. Van Wijnen, M. F. Young, J. B. Lian, G. S. Stein, and L. C. Gerstenfeld. 2003. Osteoblast-related transcription factors Runx2 (Cbfa1/AML3) and MSX2 mediate the expression of bone sialoprotein in human metastatic breast cancer cells. Cancer Res. 63:2631–2637.
   PubMed Web of Science ®Google Scholar
• Berardi, M. J., C. Sun, M. Zehr, F. Abildgaard, J. Peng, N. A. Speck, and J. H. Bushweller. 1999. The Ig fold of the core binding factor alpha Runt domain is a member of a family of structurally and functionally related Ig-fold DNA-binding domains. Struct. Fold Des. 7:1247–1256.
   Google Scholar
• Bravo, J., Z. Li, N. A. Speck, and A. J. Warren. 2001. The leukemia-associated AML1 (Runx1)-CBF beta complex functions as a DNA-induced molecular clamp. Nat. Struct. Biol. 8:371–378.
   PubMedGoogle Scholar
• Bristow, C. A., and P. Shore. 2003. Transcriptional regulation of the human MIP-1alpha promoter by RUNX1 and MOZ. Nucleic Acids Res. 31:2735–2744.
   PubMedGoogle Scholar
• Brummelkamp, T. R., R. Bernards, and R. Agami. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550–553.
   PubMed Web of Science ®Google Scholar
• Cella, N., B. Groner, and N. E. Hynes. 1998. Characterization of Stat5a and Stat5b homodimers and heterodimers and their association with the glucocortiocoid receptor in mammary cells. Mol. Cell. Biol. 18:1783–1792.
   PubMedGoogle Scholar
• Chandran, U. R., B. S. Warren, C. T. Baumann, G. L. Hager, and D. B. DeFranco. 1999. The glucocorticoid receptor is tethered to DNA-bound Oct-1 at the mouse gonadotropin-releasing hormone distal negative glucocorticoid response element. J. Biol. Chem. 274:2372–2378.
   PubMedGoogle Scholar
• Chasman, D., K. Cepek, P. A. Sharp, and C. O. Pabo. 1999. Crystal structure of an OCA-B peptide bound to an Oct-1 POU domain/octamer DNA complex: specific recognition of a protein-DNA interface. Genes Dev. 13:2650–2657.
   PubMedGoogle Scholar
• D'Alonzo, R. C., N. Selvamurugan, G. Karsenty, and N. C. Partridge. 2002. Physical interaction of the activator protein-1 factors c-Fos and c-Jun with Cbfa1 for collagenase-3 promoter activation. J. Biol. Chem. 277:816–822.
   PubMed Web of Science ®Google Scholar
• Doppler, W., B. Groner, and R. K. Ball. 1989. Prolactin and glucocorticoid hormones synergistically induce expression of transfected rat beta-casein gene promoter constructs in a mammary epithelial cell line. Proc. Natl. Acad. Sci. USA 86:104–108.
   PubMed Web of Science ®Google Scholar
• Doppler, W., T. Welte, and S. Philipp. 1995. CCAAT/enhancer-binding protein isoforms beta and delta are expressed in mammary epithelial cells and bind to multiple sites in the beta-casein gene promoter. J. Biol. Chem. 270:17962–17969.
   PubMed Web of Science ®Google Scholar
• Ducy, P., M. Starbuck, M. Priemel, J. Shen, G. Pinero, V. Geoffroy, M. Amling, and G. Karsenty. 1999. A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev. 13:1025–1036.
   PubMed Web of Science ®Google Scholar
• Ducy, P., R. Zhang, V. Geoffroy, A. L. Ridall, and G. Karsenty. 1997. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89:747–754.
   PubMed Web of Science ®Google Scholar
• Franceschi, R. T., and G. Xiao. 2003. Regulation of the osteoblast-specific transcription factor, Runx2: responsiveness to multiple signal transduction pathways. J. Cell. Biochem. 88:446–454.
   PubMed Web of Science ®Google Scholar
• Goetz, T. L., T.-L. Gu, N. A. Speck, and B. J. Graves. 2000. Autoinhibition of Ets-1 is counteracted by DNA binding cooperativity with core-binding factor α2. Mol. Cell. Biol. 20:81–90.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Grenfell, S. J., D. S. Latchman, and N. S. Thomas. 1996. Oct-1 and Oct-2 DNA-binding site specificity is regulated in vitro by different kinases. Biochem. J. 315:889–893.
   PubMedGoogle Scholar
• Groenen, M. A., R. J. Dijkhof, J. J. van der Poel, R. van Diggelen, and E. Verstege. 1992. Multiple octamer binding sites in the promoter region of the bovine alpha s2-casein gene. Nucleic Acids Res. 20:4311–4318.
   PubMedGoogle Scholar
• Gu, T. L., T. L. Goetz, B. J. Graves, and N. A. Speck. 2000. Autoinhibition and partner proteins, core-binding factor beta (CBFβ) and Ets-1, modulate DNA binding by CBFα2 (AML1). Mol. Cell. Biol. 2:91–103.
   Google Scholar
• Hauschka, P. V. 1986. Osteocalcin: the vitamin K-dependent Ca2+-binding protein of bone matrix. Haemostasis 16:258–272.
   PubMedGoogle Scholar
• Herr, W., and M. A. Cleary. 1995. The POU domain: versatility in transcriptional regulation by a flexible two-in-one DNA-binding domain. Genes Dev. 9:1679–1693.
   PubMed Web of Science ®Google Scholar
• Hess, J., D. Porte, C. Munz, and P. Angel. 2001. AP-1 and Cbfa/runt physically interact and regulate parathyroid hormone-dependent MMP13 expression in osteoblasts through a new osteoblast-specific element 2/AP-1 composite element. J. Biol. Chem. 276:20029–20038.
   PubMed Web of Science ®Google Scholar
• Inman, C. K., and P. Shore. 2003. The osteoblast transcription factor Runx2 is expressed in mammary epithelial cells and mediates osteopontin expression. J. Biol. Chem. 278:48684–48689.
   PubMedGoogle Scholar
• Ito, Y. 1999. Molecular basis of tissue-specific gene expression mediated by the runt domain transcription factor PEBP2/CBF. Genes Cells 4:685–696.
   PubMed Web of Science ®Google Scholar
• Ito, Y. 2004. Oncogenic potential of the RUNX gene family: ‘overview.’. Oncogene 23:4198–4208.
   PubMed Web of Science ®Google Scholar
• Karsenty, G. 2000. Role of Cbfa1 in osteoblast differentiation and function. Semin. Cell Dev. Biol. 11:343–346.
   PubMedGoogle Scholar
• Kemler, I., and W. Schaffner. 1990. Octamer transcription factors and the cell type-specificity of immunoglobulin gene expression. FASEB J. 4:1444–1449.
   PubMedGoogle Scholar
• Kim, S., T. Koga, M. Isobe, B. E. Kern, T. Yokochi, Y. E. Chin, G. Karsenty, T. Taniguchi, and H. Takayanagi. 2003. Stat1 functions as a cytoplasmic attenuator of Runx2 in the transcriptional program of osteoblast differentiation. Genes Dev. 17:1979–1991.
   PubMed Web of Science ®Google Scholar
• Kim, W. Y., M. Sieweke, E. Ogawa, H. J. Wee, U. Englmeier, T. Graf, and Y. Ito. 1999. Mutual activation of Ets-1 and AML1 DNA binding by direct interaction of their autoinhibitory domains. EMBO J. 18:1609–1620.
   PubMed Web of Science ®Google Scholar
• Komori, T., H. Yagi, S. Nomura, A. Yamaguchi, K. Sasaki, K. Deguchi, Y. Shimizu, R. T. Bronson, Y. H. Gao, M. Inada, M. Sato, R. Okamoto, Y. Kitamura, S. Yoshiki, and T. Kishimoto. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755–764.
   PubMed Web of Science ®Google Scholar
• Komori, T. 2002. Runx2, a multifunctional transcription factor in skeletal development. J. Cell. Biochem. 87:1–8.
   PubMed Web of Science ®Google Scholar
• Lechner, J., T. Welte, and W. Doppler. 1997. Mechanism of interaction between the glucocorticoid receptor and Stat5: role of DNA-binding. Immunobiology 198:112–123.
   PubMedGoogle Scholar
• Magne, S., S. Caron, M. Charon, M. C. Rouyez, and I. Dusanter-Fourt. 2003. STAT5 and Oct-1 form a stable complex that modulates cyclin D1 expression. Mol. Cell. Biol. 23:8934–8945.
   PubMedGoogle Scholar
• Martin, T. J., and M. T. Gillespie. 2001. Receptor activator of nuclear factor kappa B ligand (RANKL): another link between breast and bone. Trends Endocrinol. Metab. 12:2–4.
   PubMedGoogle Scholar
• McCarthy, T. L., W. Z. Chang, Y. Liu, and M. Centrella. 2003. Runx2 integrates estrogen activity in osteoblasts. J. Biol. Chem. 278:43121–43129.
   PubMedGoogle Scholar
• Meyers, S., N. Lenny, and S. W. Hiebert. 1995. The t(8;21) fusion protein interferes with AML-1B-dependent transcriptional activation. Mol. Cell. Biol. 15:1974–1982.
   PubMed Web of Science ®Google Scholar
• Miyazono, K., S. Maeda, and T. Imamura. 2004. Coordinate regulation of cell growth and differentiation by TGF-beta superfamily and Runx proteins. Oncogene 23:4232–4237.
   PubMedGoogle Scholar
• Mundlos, S., F. Otto, C. Mundlos, J. B. Mulliken, A. S. Aylsworth, S. Albright, D. Lindhout, W. G. Cole, W. Henn, J. H. Knoll, M. J. Owen, R. Mertelsmann, B. U. Zabel, and B. R. Olsen. 1997. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89:773–779.
   PubMed Web of Science ®Google Scholar
• Nagata, T., V. Gupta, D. Sorce, W. Y. Kim, A. Sali, B. T. Chait, K. Shigesada, Y. Ito, and M. H. Werner. 1999. Immunoglobulin motif DNA recognition and heterodimerization of the PEBP2/CBF Runt domain. Nat. Struct. Biol. 6:615–619.
   PubMedGoogle Scholar
• Ning, Y. M., and D. M. Robins. 1999. AML3/CBFalpha1 is required for androgen-specific activation of the enhancer of the mouse sex-limited protein (Slp) gene. J. Biol. Chem. 274:30624–30630.
   PubMedGoogle Scholar
• Otto, F., H. Kanegane, and S. Mundlos. 2002. Mutations in the RUNX2 gene in patients with cleidocranial dysplasia. Hum. Mutat. 19:209–216.
   PubMed Web of Science ®Google Scholar
• Otto, F., M. Lubbert, and M. Stock. 2003. Upstream and downstream targets of RUNX proteins. J. Cell. Biochem. 89:9–18.
   PubMedGoogle Scholar
• Otto, F., A. P. Thornell, T. Crompton, et al. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89:765–771.
   PubMed Web of Science ®Google Scholar
• Paredes, R., G. Arriagada, F. Cruzat, A. Villagra, J. Olate, K. Zaidi, A. Van Wijnen, J. B. Lian, G. S. Stein, J. L. Stein, and M. Montecino. 2004. Bone-specific transcription factor Runx2 interacts with the 1α,25-dihydroxyvitamin D3 receptor to up-regulate rat osteocalcin gene expression in osteoblastic cells. Mol. Cell. Biol. 24:8847–8861.
   PubMedGoogle Scholar
• Phillips, K., and B. Luisi. 2000. The virtuoso of versatility: POU proteins that flex to fit. J. Mol. Biol. 302:1023–1039.
   PubMed Web of Science ®Google Scholar
• Prefontaine, G. G., R. Walther, W. Giffin, M. E. Lemieux, L. Pope, and R. J. Hache. 1999. Selective binding of steroid hormone receptors to octamer transcription factors determines transcriptional synergism at the mouse mammary tumor virus promoter. J. Biol. Chem. 274:26713–26719.
   PubMedGoogle Scholar
• Saito, H., and T. Oka. 1996. Hormonally regulated double- and single-stranded DNA-binding complexes involved in mouse beta-casein gene transcription. J. Biol. Chem. 271:8911–8918.
   PubMed Web of Science ®Google Scholar
• Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Sato, M., E. Morii, T. Komori, H. Kawahata, M. Sugimoto, K. Terai, H. Shimizu, T. Yasui, H. Ogihara, T. N. Yasui, Ochi, Y. Kitamura, Y. Ito, and S. Nomura. 1998. Transcriptional regulation of osteopontin gene in vivo by PEBP2alphaA/CBFA1 and ETS1 in the skeletal tissues. Oncogene 17:1517–1525.
   PubMed Web of Science ®Google Scholar
• Schmitt-Ney, M., W. Doppler, R. K. Ball, and B. Groner. 1991. Beta-casein gene promoter activity is regulated by the hormone-mediated relief of transcriptional repression and a mammary-gland-specific nuclear factor. Mol. Cell. Biol. 11:3745–3755.
   PubMed Web of Science ®Google Scholar
• Selvamurugan, N., S. Kwok, and N. C. Partridge. 2004. Smad3 interacts with JunB and Cbfa1/Runx2 for transforming growth factor-beta1-stimulated collagenase-3 expression in human breast cancer cells. J. Biol. Chem. 279:27764–27773.
   PubMedGoogle Scholar
• Selvamurugan, N., and N. C. Partridge. 2000. Constitutive expression and regulation of collagenase-3 in human breast cancer cells. Mol. Cell. Biol. Res. Commun. 3:218–223.
   PubMedGoogle Scholar
• Shah, P. C., E. Bertolino, and H. Singh. 1997. Using altered specificity Oct-1 and Oct-2 mutants to analyze the regulation of immunoglobulin gene transcription. EMBO J. 16:7105–7117.
   PubMedGoogle Scholar
• Shore, P., and A. D. Sharrocks. 1994. The transcription factors Elk-1 and serum response factor interact by direct protein-protein contacts mediated by a short region of Elk-1. Mol. Cell. Biol. 14:3283–3291.
   PubMedGoogle Scholar
• Staudt, L. M., and M. J. Lenardo. 1991. Immunoglobulin gene transcription. Annu. Rev. Immunol. 9:373–398.
   PubMed Web of Science ®Google Scholar
• Stein, G. S., J. B. Lian, A. J. van Wijnen, J. L. Stein, M. Montecino, A. Javed, S. K. Zaidi, D. W. Young, J. Y. Choi, and S. M. Pockwinse. 2004. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene 23:4315–4329.
   PubMed Web of Science ®Google Scholar
• Stoecklin, E., M. Wissler, R. Moriggl, and B. Groner. 1997. Specific DNA binding of Stat5, but not of glucocorticoid receptor, is required for their functional cooperation in the regulation of gene transcription. Mol. Cell. Biol. 17:6708–6716.
   PubMedGoogle Scholar
• Tahirov, T. H., T. Inoue-Bungo, H. Morii, A. Fujikawa, M. Sasaki, K. Kimura, K. M. Shiina, Sato, T. Kumasaka, M. Yamamoto, S. Ishii, and K. Ogata. 2001. Structural analyses of DNA recognition by the AML1/Runx-1 Runt domain and its allosteric control by CBFbeta. Cell 104:755–767.
   PubMed Web of Science ®Google Scholar
• Vegarud, G. E., T. Langsrud, and C. Svenning. 2000. Mineral-binding milk proteins and peptides; occurrence, biochemical and technological characteristics. Br. J. Nutr. 84(Suppl. 1):S91–S98.
   PubMedGoogle Scholar
• Verrijzer, C. P., and P. C. Van der Vliet. 1993. POU domain transcription factors. Biochim. Biophys. Acta 1173:1–21.
   PubMedGoogle Scholar
• Wakao, H., F. Gouilleux, and B. Groner. 1994. Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J. 13:2182–2191.
   PubMed Web of Science ®Google Scholar
• Westendorf, J. J., and S. W. Hiebert. 1999. Mammalian runt-domain proteins and their roles in hematopoiesis, osteogenesis, and leukemia. J. Cell. Biochem. Suppl. 32-33:51–58.
   Google Scholar
• Wheeler, J. C., K. Shigesada, J. P. Gergen, and Y. Ito. 2000. Mechanisms of transcriptional regulation by Runt domain proteins. Semin. Cell Dev. Biol. 11:369–375.
   PubMedGoogle Scholar
• Yoshimura, M., and T. Oka. 1989. Isolation and structural analysis of the mouse beta-casein gene. Gene 78:267–275.
   PubMed Web of Science ®Google Scholar
• Zaidi, S. K., A. Javed, J. Y. Choi, A. J. van Wijnen, J. L. Stein, J. B. Lian, and G. S. Stein. 2001. A specific targeting signal directs Runx2/Cbfa1 to subnuclear domains and contributes to transactivation of the osteocalcin gene. J. Cell Sci. 114:3093–3102.
   PubMedGoogle Scholar
• Zhang, D. E., C. J. Hetherington, S. Meyers, K. L. Rhoades, C. J. Larson, H. M. Chen, S. W. Hiebert, and D. G. Tenen. 1996. CCAAT enhancer-binding protein (C/EBP) and AML1 (CBFα2) synergistically activate the macrophage colony-stimulating factor receptor promoter. Mol. Cell. Biol. 16:1231–1240.
   PubMed Web of Science ®Google Scholar
• Zhang, L., S. M. Lukasik, N. A. Speck, and J. H. Bushweller. 2003. Structural and functional characterization of Runx1, CBF beta, and CBF beta-SMMHC. Blood Cells Mol. Dis. 30:147–156.
   PubMedGoogle Scholar
• Zhao, F. Q., K. Adachi, and T. Oka. 2002. Involvement of Oct-1 in transcriptional regulation of beta-casein gene expression in mouse mammary gland. Biochim. Biophys. Acta 1577:27–37.
   PubMed Web of Science ®Google Scholar
• Zhao, F. Q., Y. Zheng, B. Dong, and T. Oka. 2004. Cloning, genomic organization, expression, and effect on beta-casein promoter activity of a novel isoform of the mouse Oct-1 transcription factor. Gene 326:175–187.
   PubMed Web of Science ®Google Scholar
• Ziros, P. G., T. Georgakopoulos, I. Habeos, E. K. Basdra, and A. G. Papavassiliou. 2004. Growth hormone attenuates the transcriptional activity of runx2 by facilitating its physical association with stat3beta. J. Bone Miner. Res. 19:1892–1904.
   PubMed Web of Science ®Google Scholar