Evidence of a novel role for Pygopus in rRNA transcription

Biochemical Journal

Volumn 453, Issue 1, 2013, Pages 61-70

  Andrews, Phillip G P ^a   He, Zhijian ^a   Tzenov, Youlian R ^a   Popadiuk, Catherine ^a   Kao, Kenneth R ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Cancer cell growth mechanisms; Chromatin remodelling; Histone acetylation; Nucleolar stress; Pygopus; Ribosome biogenesis.

Indexed keywords

PYGOPUS; RIBOSOME DNA; RIBOSOME RNA; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; BIOGENESIS; CANCER CELL; CANCER GROWTH; CELL CYCLE G1 PHASE; GROWTH DISORDER; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; RNA TRANSCRIPTION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEOLUS; HELA CELLS; HISTONE ACETYLTRANSFERASES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; RNA, RIBOSOMAL; TRANSCRIPTION, GENETIC;

PYGOPUS;

EID: 84879023191     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121667     Document Type: Article

References (45)

1. Moss, T. (2004) At the crossroads of growth control; making ribosomal RNA. Curr. Opin. Genet. Dev. 14, 210-217
2. Moss, T., Langlois, F., Gagnon-Kugler, T. and Stefanovsky, V. (2007) A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci. 64, 29-49 (Pubitemid 46159444)
3. Russell, J. and Zomerdijk, J. C. (2005) RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem. Sci. 30, 87-96 (Pubitemid 40187301)
4. Prieto, J. L. and McStay, B. (2007) Recruitment of factors linking transcription and processing of pre-rRNA to NOR chromatin is UBF-dependent and occurs independent of transcription in human cells. Genes Dev. 21, 2041-2054
5. Grummt, I. and Pikaard, C. S. (2003) Epigenetic silencing of RNA polymerase I transcription. Nat. Rev. Mol. Cell Biol. 4, 641-649 (Pubitemid 36934966)
6. McStay, B. and Grummt, I. (2008) The epigenetics of rRNA genes: from molecular to chromosome biology. Annu. Rev. Cell Dev. Biol. 24, 131-157
7. Kramps, T., Peter, O., Brunner, E., Nellen, D., Froesch, B., Chatterjee, S., Murone, M., Zullig, S. and Basler, K. (2002) Wnt/wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear β-catenin-TCF complex. Cell 109, 47-60 (Pubitemid 34327516)
8. Thompson, B., Townsley, F., Rosin-Arbesfeld, R., Musisi, H. and Bienz, M. (2002) A new nuclear component of the Wnt signalling pathway. Nat. Cell Biol. 4, 367-373 (Pubitemid 34521032)
9. Fiedler, M., Sanchez-Barrena, M. J., Nekrasov, M., Mieszczanek, J., Rybin, V., Muller, J., Evans, P. and Bienz, M. (2008) Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex. Mol. Cell 30, 507-518 (Pubitemid 351672372)
10. Gu, B., Sun, P., Yuan, Y., Moraes, R. C., Li, A., Teng, A., Agrawal, A., Rheaume, C., Bilanchone, V., Veltmaat, J. M. et al. (2009) Pygo2 expands mammary progenitor cells by facilitating histone H3 K4 methylation. J. Cell Biol. 185, 811-826
11. Andrews, P. G., He, Z., Popadiuk, C. and Kao, K. R. (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
12. Chen, J., Luo, Q., Yuan, Y., Huang, X., Cai, W., Li, C., Wei, T., Zhang, L., Yang, M., Liu, Q. et al. (2010) Pygo2 associates with MLL2 histone methyltransferase and GCN5 histone acetyltransferase complexes to augment Wnt target gene expression and breast cancer stem-like cell expansion. Mol. Cell. Biol. 30, 5621-5635
13. Song, N., Schwab, K. R., Patterson, L. T., Yamaguchi, T., Lin, X., Potter, S. S. and Lang, R. A. (2007) Pygopus 2 has a crucial, Wnt pathway-independent function in lens induction. Development 134, 1873-1885 (Pubitemid 46939233)
14. Popadiuk, C. M., Xiong, J., Wells, M. G., Andrews, P. G., Dankwa, K., Hirasawa, K., Lake, B. B. and Kao, K. R. (2006) Antisense suppression of pygopus2 results in growth arrest of epithelial ovarian cancer. Clin. Cancer Res. 12, 2216-2223
15. Sakai, D. and Trainor, P. A. (2009) Treacher Collins syndrome: unmasking the role of Tcof1/treacle. Int. J. Biochem. Cell Biol. 41, 1229-1232
16. Sanij, E. and Hannan, R. D. (2009) The role of UBF in regulating the structure and dynamics of transcriptionally active rDNA chromatin. Epigenetics 4, 374-382
17. Andrews, P. G., Kennedy, M. W., Popadiuk, C. M. and Kao, K. R. (2008) Oncogenic activation of the human Pygopus2 promoter by E74-like factor-1. Mol. Cancer Res. 6, 259-266 (Pubitemid 351342414)
18. Andrews, P. G., Lake, B. B., Popadiuk, C. and Kao, K. R. (2007) Requirement of Pygopus 2 in breast cancer. Int. J. Oncol. 30, 357-363
19. Valdez, B. C., Henning, D., So, R. B., Dixon, J. and Dixon, M. J. (2004) The Treacher Collins syndrome (TCOF1) gene product is involved in ribosomal DNA gene transcription by interacting with upstream binding factor. Proc. Natl. Acad. Sci. U.S.A. 101, 10709-10714 (Pubitemid 38955807)
20. Andersen, J. S., Lyon, C. E., Fox, A. H., Leung, A. K., Lam, Y. W., Steen, H., Mann, M. and Lamond, A. I. (2002) Directed proteomic analysis of the human nucleolus. Curr. Biol. 12, 1-11
21. Gorski, J. J., Pathak, S., Panov, K., Kasciukovic, T., Panova, T., Russell, J. and Zomerdijk, J. C. (2007) A novel TBP-associated factor of SL1 functions in RNA polymerase I transcription. EMBO J. 26, 1560-1568 (Pubitemid 46480930)
22. Sweet, T., Yen, W., Khalili, K. and Amini, S. (2008) Evidence for involvement of NFBP in processing of ribosomal RNA. J. Cell. Physiol. 214, 381-388 (Pubitemid 350308994)
23. Pestov, D. G., Lapik, Y. R. and Lau, L. F. (2008) Assays for ribosomal RNA processing and ribosome assembly. Curr. Protoc. Cell Biol. 39, 22.11.1-22.11.16
24. Carrera, I., Janody, F., Leeds, N., Duveau, F. and Treisman, J. E. (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 (Pubitemid 351754560)
25. Stadeli, R. and Basler, K. (2005) Dissecting nuclear Wingless signalling: recruitment of the transcriptional co-activator Pygopus by a chain of adaptor proteins. Mech. Dev. 122, 1171-1182 (Pubitemid 41476322)
26. Dixon, J., Hovanes, K., Shiang, R. and Dixon, M. J. (1997) Sequence analysis, identification of evolutionary conserved motifs and expression analysis of murine tcof1 provide further evidence for a potential function for the gene and its human homologue, TCOF1. Hum. Mol. Genet. 6, 727-737 (Pubitemid 27199066)
27. Dixon, J., Edwards, S. J., Anderson, I., Brass, A., Scambler, P. J. and Dixon, M. J. (1997) Identification of the complete coding sequence and genomic organization of the Treacher Collins syndrome gene. Genome Res. 7, 223-234 (Pubitemid 27165689)
28. Heix, J., Vente, A., Voit, R., Budde, A., Michaelidis, T. M. and Grummt, I. (1998) Mitotic silencing of human rRNA synthesis: inactivation of the promoter selectivity factor SL1 by cdc2/cyclin B-mediated phosphorylation. EMBO J. 17, 7373-7381 (Pubitemid 29002705)
29. Roussel, P., Andre, C., Comai, L. and Hernandez-Verdun, D. (1996) The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs. J. Cell Biol. 133, 235-246 (Pubitemid 26131612)
30. Sirri, V., Roussel, P. and Hernandez-Verdun, D. (1999) The mitotically phosphorylated form of the transcription termination factor TTF-1 is associated with the repressed rDNA transcription machinery. J. Cell Sci. 112, 3259-3268 (Pubitemid 29507206)
31. Shav-Tal, Y., Blechman, J., Darzacq, X., Montagna, C., Dye, B. T., Patton, J. G., Singer, R. H. and Zipori, D. (2005) Dynamic sorting of nuclear components into distinct nucleolar caps during transcriptional inhibition. Mol. Biol. Cell 16, 2395-2413 (Pubitemid 40632221)
32. Reichow, S. L., Hamma, T., Ferre-D'Amare, A. R. and Varani, G. (2007) The structure and function of small nucleolar ribonucleoproteins. Nucleic Acids Res. 35, 1452-1464 (Pubitemid 46592868)
33. Yao, Z., Duan, S., Hou, D., Wang, W., Wang, G., Liu, Y., Wen, L. and Wu, M. (2010) B23 acts as a nucleolar stress sensor and promotes cell survival through its dynamic interaction with hnRNPU and hnRNPA1. Oncogene 29, 1821-1834
34. Gu, B., Watanabe, K. and Dai, X. (2012) Pygo2 regulates histone gene expression and H3 K56 acetylation in human mammary epithelial cells. Cell Cycle 11, 79-87
35. Ghoshal, K., Majumder, S., Datta, J., Motiwala, T., Bai, S., Sharma, S. M., Frankel, W. and Jacob, S. T. (2004) Role of human ribosomal RNA (rRNA) promoter methylation and of methyl-CpG-binding protein MBD2 in the suppression of rRNA gene expression. J. Biol. Chem. 279, 6783-6793 (Pubitemid 38248820)
36. Lohrum, M. A., Ludwig, R. L., Kubbutat, M. H., Hanlon, M. and Vousden, K. H. (2003) Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 3, 577-587 (Pubitemid 36808652)
37. Zhang, Y. and Lu, H. (2009) Signaling to p53: ribosomal proteins find their way. Cancer Cell, 16, 369-377
38. Barak, Y., Juven, T., Haffner, R. and Oren, M. (1993) Mdm2 expression is induced by wild type p53 activity. EMBO J. 12, 461-468 (Pubitemid 23073692)
39. Denissov, S., Lessard, F., Mayer, C., Stefanovsky, V., van Driel, M., Grummt, I., Moss, T. and Stunnenberg, H. G. (2011) A model for the topology of active ribosomal RNA genes. EMBO Rep. 12, 231-237
40. Li, B., Mackay, D. R., Ma, J. and Dai, X. (2004) Cloning and developmental expression of mouse pygopus 2, a putative Wnt signaling component. Genomics 84, 398-405 (Pubitemid 38834176)
41. Li, B., Rheaume, C., Teng, A., Bilanchone, V., Munguia, J. E., Hu, M., Jessen, S., Piccolo, S., Waterman, M. L. and Dai, X. (2007) Developmental phenotypes and reduced Wnt signaling in mice deficient for pygopus 2. Genesis 45, 318-325 (Pubitemid 46842897)
42. Schwab, K. R., Patterson, L. T., Hartman, H. A., Song, N., Lang, R. A., Lin, X. and Potter, S. S. (2007) Pygo1 and Pygo2 roles in Wnt signaling in mammalian kidney development. BMC Biol. 5, 15
43. Jones, N. C., Lynn, M. L., Gaudenz, K., Sakai, D., Aoto, K., Rey, J. P., Glynn, E. F., Ellington, L., Du, C., Dixon, J. et al. (2008) Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat. Med. 14, 125-133 (Pubitemid 351214559)
44. Tzenov, Y. R., Andrews, P. G., Voisey, K., Popadiuk, P., Xiong, J., Popadiuk, C. and Kao, K. R. (2013) Human papilloma virus (HPV) E7-mediated attenuation of retinoblastoma (Rb) induces hPygopus2 expression via Elf-1 in cervical cancer. Mol. Cancer Res. 11, 19-30
45. Wang, Z. X., Chen, Y. Y., Li, B. A., Tan, G. W., Liu, X. Y., Shen, S. H., Zhu, H. W. and Wang, H. D. (2010) Decreased pygopus 2 expression suppresses glioblastoma U251 cell growth. J. Neuro-Oncol. 100, 31-41