Pygo2 Associates with MLL2 Histone Methyltransferase and GCN5 Histone Acetyltransferase Complexes To Augment Wnt Target Gene Expression and Breast Cancer Stem-Like Cell Expansion

REFERENCES

• Al-Hajj, M., M. S. Wicha, A. Benito-Hernandez, S. J. Morrison, and M. F. Clarke. 2003. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. U. S. A. 100:3983–3988.
   PubMed Web of Science ®Google Scholar
• Allis, C. D., S. L. Berger, J. Cote, S. Dent, T. Jenuwien, T. Kouzarides, L. Pillus, D. Reinberg, Y. Shi, R. Shiekhattar, A. Shilatifard, J. Workman, and Y. Zhang. 2007. New nomenclature for chromatin-modifying enzymes. Cell 131:633–636.
   PubMed Web of Science ®Google Scholar
• Amit, S., A. Hatzubai, Y. Birman, J. S. Andersen, E. Ben-Shushan, M. Mann, Y. Ben-Neriah, and I. Alkalay. 2002. Axin-mediated CKI phosphorylation of beta-catenin at Ser 45: a molecular switch for the Wnt pathway. Genes Dev. 16:1066–1076.
   PubMed Web of Science ®Google Scholar
• Andrews, P. G., Z. He, C. Popadiuk, and K. R. Kao. 2009. The transcriptional activity of Pygopus is enhanced by its interaction with cAMP-response-element-binding protein (CREB)-binding protein. Biochem. J. 422:493–501.
   PubMedGoogle Scholar
• Balendra, S., C. Lesieur, T. J. Smith, and H. Dalton. 2002. Positively charged amino acids are essential for electron transfer and protein-protein interactions in the soluble methane monooxygenase complex from Methylococcus capsulatus (Bath). Biochemistry 41:2571–2579.
   PubMedGoogle Scholar
• Belenkaya, T. Y., C. Han, H. J. Standley, X. Lin, D. W. Houston, J. Heasman, and X. Lin. 2002. pygopus encodes a nuclear protein essential for wingless/Wnt signaling. Development 129:4089–4101.
   PubMed Web of Science ®Google Scholar
• Briggs, S. D., M. Bryk, B. D. Strahl, W. L. Cheung, J. K. Davie, S. Y. Dent, F. Winston, and C. D. Allis. 2001. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15:3286–3295.
   PubMed Web of Science ®Google Scholar
• Brown, A. M. 2001. Wnt signaling in breast cancer: have we come full circle? Breast Cancer Res. 3:351–355.
   PubMedGoogle Scholar
• Brownell, J. E., J. Zhou, T. Ranalli, R. Kobayashi, D. G. Edmondson, S. Y. Roth, and C. D. Allis. 1996. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84:843–851.
   PubMed Web of Science ®Google Scholar
• Carrera, I., F. Janody, N. Leeds, F. Duveau, and J. E. Treisman. 2008. Pygopus activates Wingless target gene transcription through the mediator complex subunits Med12 and Med13. Proc. Natl. Acad. Sci. U. S. A. 105:6644–6649.
   PubMed Web of Science ®Google Scholar
• Cheung, W. L., S. D. Briggs, and C. D. Allis. 2000. Acetylation and chromosomal functions. Curr. Opin. Cell Biol. 12:326–333.
   PubMed Web of Science ®Google Scholar
• Crawford, B. D., and J. L. Hess. 2006. MLL core components give the green light to histone methylation. ACS Chem. Biol. 1:495–498.
   PubMedGoogle Scholar
• de la Roche, M., and M. Bienz. 2007. Wingless-independent association of Pygopus with dTCF target genes. Curr. Biol. 17:556–561.
   PubMedGoogle Scholar
• Dontu, G., W. M. Abdallah, J. M. Foley, K. W. Jackson, M. F. Clarke, M. J. Kawamura, and M. S. Wicha. 2003. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17:1253–1270.
   PubMed Web of Science ®Google Scholar
• Fiedler, M., M. J. Sanchez-Barrena, M. Nekrasov, J. Mieszczanek, V. Rybin, J. Muller, P. Evans, and M. Bienz. 2008. Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex. Mol. Cell 30:507–518.
   PubMedGoogle Scholar
• Glaser, S., J. Schaft, S. Lubitz, K. Vintersten, F. van der Hoeven, K. R. Tufteland, R. Aasland, K. Anastassiadis, S. L. Ang, and A. F. Stewart. 2006. Multiple epigenetic maintenance factors implicated by the loss of Mll2 in mouse development. Development 133:1423–1432.
   PubMed Web of Science ®Google Scholar
• Grant, P. A., A. Eberharter, S. John, R. G. Cook, B. M. Turner, and J. L. Workman. 1999. Expanded lysine acetylation specificity of Gcn5 in native complexes. J. Biol. Chem. 274:5895–5900.
   PubMed Web of Science ®Google Scholar
• Gu, B., P. Sun, Y. Yuan, R. C. Moraes, A. Li, A. Teng, A. Agrawal, C. Rheaume, V. Bilanchone, J. M. Veltmaat, K. Takemaru, S. Millar, E. Y. Lee, M. T. Lewis, B. Li, and X. Dai. 2009. Pygo2 expands mammary progenitor cells by facilitating histone H3 K4 methylation. J. Cell Biol. 185:811–826.
   PubMed Web of Science ®Google Scholar
• He, T. C., A. B. Sparks, C. Rago, H. Hermeking, L. Zawel, L. T. da Costa, P. J. Morin, B. Vogelstein, and K. W. Kinzler. 1998. Identification of c-MYC as a target of the APC pathway. Science 281:1509–1512.
   PubMed Web of Science ®Google Scholar
• Hoffmans, R., and K. Basler. 2004. Identification and in vivo role of the Armadillo-Legless interaction. Development 131:4393–4400.
   PubMed Web of Science ®Google Scholar
• Hoffmans, R., R. Stadeli, and K. Basler. 2005. Pygopus and legless provide essential transcriptional coactivator functions to armadillo/beta-catenin. Curr. Biol. 15:1207–1211.
   PubMed Web of Science ®Google Scholar
• Hughes, C. M., O. Rozenblatt-Rosen, T. A. Milne, T. D. Copeland, S. S. Levine, J. C. Lee, D. N. Hayes, K. S. Shanmugam, A. Bhattacharjee, C. A. Biondi, G. F. Kay, N. K. Hayward, J. L. Hess, and M. Meyerson. 2004. Menin associates with a trithorax family histone methyltransferase complex and with the Hoxc8 locus. Mol. Cell 13:587–597.
   PubMed Web of Science ®Google Scholar
• Jessen, S., B. Gu, and X. Dai. 2008. Pygopus and the Wnt signaling pathway: a diverse set of connections. Bioessays 30:448–456.
   PubMed Web of Science ®Google Scholar
• Kay, B. K., M. P. Williamson, and M. Sudol. 2000. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14:231–241.
   PubMed Web of Science ®Google Scholar
• Kessler, R., G. Hausmann, and K. Basler. 2009. The PHD domain is required to link Drosophila Pygopus to Legless/beta-catenin and not to histone H3. Mech. Dev. 126:752–759.
   PubMedGoogle Scholar
• Kramps, T., O. Peter, E. Brunner, D. Nellen, B. Froesch, S. Chatterjee, M. Murone, S. Zullig, and K. Basler. 2002. Wnt/wingless signaling requires BCL9/legless-mediated recruitment of Pygopus to the nuclear beta-catenin-TCF complex. Cell 109:47–60.
   PubMed Web of Science ®Google Scholar
• Krieghoff, E., J. Behrens, and B. Mayr. 2006. Nucleo-cytoplasmic distribution of beta-catenin is regulated by retention. J. Cell Sci. 119:1453–1463.
   PubMedGoogle Scholar
• Kuo, M. H., J. E. Brownell, R. E. Sobel, T. A. Ranalli, R. G. Cook, D. G. Edmondson, S. Y. Roth, and C. D. Allis. 1996. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature 383:269–272.
   PubMed Web of Science ®Google Scholar
• Lane, T. F., and P. Leder. 1997. Wnt-10b directs hypermorphic development and transformation in mammary glands of male and female mice. Oncogene 15:2133–2144.
   PubMed Web of Science ®Google Scholar
• Lee, S., D. K. Lee, Y. Dou, J. Lee, B. Lee, E. Kwak, Y. Y. Kong, S. K. Lee, R. G. Roeder, and J. W. Lee. 2006. Coactivator as a target gene specificity determinant for histone H3 lysine 4 methyltransferases. Proc. Natl. Acad. Sci. U. S. A. 103:15392–15397.
   PubMed Web of Science ®Google Scholar
• Li, Y., B. Welm, K. Podsypanina, S. Huang, M. Chamorro, X. Zhang, T. Rowlands, M. Egeblad, P. Cowin, Z. Werb, L. K. Tan, J. M. Rosen, and H. E. Varmus. 2003. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 100:15853–15858.
   PubMed Web of Science ®Google Scholar
• Lindvall, C., W. Bu, B. O. Williams, and Y. Li. 2007. Wnt signaling, stem cells, and the cellular origin of breast cancer. Stem Cell Rev. 3:157–168.
   PubMedGoogle Scholar
• Liu, C., Y. Li, M. Semenov, C. Han, G. H. Baeg, Y. Tan, Z. Zhang, X. Lin, and X. He. 2002. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108:837–847.
   PubMed Web of Science ®Google Scholar
• Logan, C. Y., and R. Nusse. 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20:781–810.
   PubMed Web of Science ®Google Scholar
• Lustig, B., and J. Behrens. 2003. The Wnt signaling pathway and its role in tumor development. J. Cancer Res. Clin. Oncol. 129:199–221.
   PubMed Web of Science ®Google Scholar
• Martinez, E., V. B. Palhan, A. Tjernberg, E. S. Lymar, A. M. Gamper, T. K. Kundu, B. T. Chait, and R. G. Roeder. 2001. Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol. Cell. Biol. 21:6782–6795.
   PubMed Web of Science ®Google Scholar
• Milne, T. A., S. D. Briggs, H. W. Brock, M. E. Martin, D. Gibbs, C. D. Allis, and J. L. Hess. 2002. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10:1107–1117.
   PubMed Web of Science ®Google Scholar
• Moon, R. T., and J. R. Miller. 1997. The APC tumor suppressor protein in development and cancer. Trends Genet. 13:256–258.
   PubMedGoogle Scholar
• Mosimann, C., G. Hausmann, and K. Basler. 2009. Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat. Rev. Mol. Cell Biol. 10:276–286.
   PubMed Web of Science ®Google Scholar
• Nagy, Z., and L. Tora. 2007. Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 26:5341–5357.
   PubMed Web of Science ®Google Scholar
• Nair, M., I. Nagamori, P. Sun, D. P. Mishra, C. Rheaume, B. Li, P. Sassone-Corsi, and X. Dai. 2008. Nuclear regulator Pygo2 controls spermiogenesis and histone H3 acetylation. Dev. Biol. 320:446–455.
   PubMedGoogle Scholar
• Narlikar, G. J., H. Y. Fan, and R. E. Kingston. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108:475–487.
   PubMed Web of Science ®Google Scholar
• Parker, D. S., J. Jemison, and K. M. Cadigan. 2002. Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development 129:2565–2576.
   PubMed Web of Science ®Google Scholar
• Polakis, P. 2000. Wnt signaling and cancer. Genes Dev. 14:1837–1851.
   PubMed Web of Science ®Google Scholar
• Ponti, D., A. Costa, N. Zaffaroni, G. Pratesi, G. Petrangolini, D. Coradini, S. Pilotti, M. A. Pierotti, and M. G. Daidone. 2005. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 65:5506–5511.
   PubMed Web of Science ®Google Scholar
• Prasad, R., A. B. Zhadanov, Y. Sedkov, F. Bullrich, T. Druck, R. Rallapalli, T. Yano, H. Alder, C. M. Croce, K. Huebner, A. Mazo, and E. Canaani. 1997. Structure and expression pattern of human ALR, a novel gene with strong homology to ALL-1 involved in acute leukemia and to Drosophila trithorax. Oncogene 15:549–560.
   PubMed Web of Science ®Google Scholar
• Shackleton, M., F. Vaillant, K. J. Simpson, J. Stingl, G. K. Smyth, M. L. Asselin-Labat, L. Wu, G. J. Lindeman, and J. E. Visvader. 2006. Generation of a functional mammary gland from a single stem cell. Nature 439:84–88.
   PubMed Web of Science ®Google Scholar
• Sierra, J., T. Yoshida, C. A. Joazeiro, and K. A. Jones. 2006. The APC tumor suppressor counteracts beta-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev. 20:586–600.
   PubMed Web of Science ®Google Scholar
• Sims, R. J., III, K. Nishioka, and D. Reinberg. 2003. Histone lysine methylation: a signature for chromatin function. Trends Genet. 19:629–639.
   PubMed Web of Science ®Google Scholar
• Stadeli, R., and K. Basler. 2005. Dissecting nuclear Wingless signalling: recruitment of the transcriptional co-activator Pygopus by a chain of adaptor proteins. Mech. Dev. 122:1171–1182.
   PubMed Web of Science ®Google Scholar
• Stingl, J., P. Eirew, I. Ricketson, M. Shackleton, F. Vaillant, D. Choi, H. I. Li, and C. J. Eaves. 2006. Purification and unique properties of mammary epithelial stem cells. Nature 439:993–997.
   PubMed Web of Science ®Google Scholar
• Sustmann, C., H. Flach, H. Ebert, Q. Eastman, and R. Grosschedl. 2008. Cell-type-specific function of BCL9 involves a transcriptional activation domain that synergizes with beta-catenin. Mol. Cell. Biol. 28:3526–3537.
   PubMedGoogle Scholar
• Taipale, J., and P. A. Beachy. 2001. The Hedgehog and Wnt signalling pathways in cancer. Nature 411:349–354.
   PubMed Web of Science ®Google Scholar
• Thompson, B., F. Townsley, R. Rosin-Arbesfeld, H. Musisi, and M. Bienz. 2002. A new nuclear component of the Wnt signalling pathway. Nat. Cell Biol. 4:367–373.
   PubMed Web of Science ®Google Scholar
• Townsley, F. M., B. Thompson, and M. Bienz. 2004. Pygopus residues required for its binding to Legless are critical for transcription and development. J. Biol. Chem. 279:5177–5183.
   PubMed Web of Science ®Google Scholar
• Van Dusen, C. M., L. Yee, L. M. McNally, and M. T. McNally. 2010. A glycine-rich domain of hnRNP H/F promotes nucleocytoplasmic shuttling and nuclear import through an interaction with transportin 1. Mol. Cell. Biol. 30:2552–2562.
   PubMedGoogle Scholar
• Wieczorek, E., M. Brand, X. Jacq, and L. Tora. 1998. Function of TAF (II)-containing complex without TBP in transcription by RNA polymerase II. Nature 393:187–191.
   PubMedGoogle Scholar
• Wodarz, A., and R. Nusse. 1998. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14:59–88.
   PubMed Web of Science ®Google Scholar
• Wright, K. J., and R. Tjian. 2009. Wnt signaling targets ETO coactivation domain of TAF4/TFIID in vivo. Proc. Natl. Acad. Sci. U. S. A. 106:55–60.
   PubMedGoogle Scholar
• Wysocka, J., M. P. Myers, C. D. Laherty, R. N. Eisenman, and W. Herr. 2003. Human Sin3 deacetylase and trithorax-related Set1/Ash2 histone H3-K4 methyltransferase are tethered together selectively by the cell-proliferation factor HCF-1. Genes Dev. 17:896–911.
   PubMed Web of Science ®Google Scholar
• Wysocka, J., T. Swigut, T. A. Milne, Y. Dou, X. Zhang, A. L. Burlingame, R. G. Roeder, A. H. Brivanlou, and C. D. Allis. 2005. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121:859–872.
   PubMed Web of Science ®Google Scholar
• Yokoyama, A., Z. Wang, J. Wysocka, M. Sanyal, D. J. Aufiero, I. Kitabayashi, W. Herr, and M. L. Cleary. 2004. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol. Cell. Biol. 24:5639–5649.
   PubMed Web of Science ®Google Scholar