Loading of PAX3 to mitotic chromosomes is mediated by arginine methylation and associated with Waardenburg syndrome

Journal of Biological Chemistry

Volumn 290, Issue 33, 2015, Pages 20556-20564

  Wu, Tsu Fang ^a,c   Yao, Ya Li ^a,b   Lai, I Lu ^a   Lai, Chien Chen ^a   Lin, Pei Lun ^a   Yang, Wen Ming ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b ASIA UNIVERSITY   (Taiwan)

^c HUNGKUANG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; AMINO ACIDS; ARGININE; CELL PROLIFERATION; CHROMOSOMES; MAMMALS; METHYLATION; PROTEINS; TRANSCRIPTION;

DEMETHYLASE; DOMINANT NEGATIVE; HOMEODOMAIN; LOCALIZATION PATTERNS; METHYLTRANSFERASES; MITOTIC CHROMOSOMES; MOLECULAR MECHANISM; NORMAL FUNCTION;

LOADING;

ARGININE; JUMONJI DOMAIN CONTAINING 6 DEMETHYLASE; METHYLTRANSFERASE; MUTANT PROTEIN; OXYGENASE; PROTEIN ARGININE METHYLTRANSFERASE 5; TRANSCRIPTION FACTOR PAX3; UNCLASSIFIED DRUG; PAIRED BOX TRANSCRIPTION FACTOR; PAX3 PROTEIN, HUMAN; PRMT5 PROTEIN, HUMAN; PROTEIN ARGININE METHYLTRANSFERASE;

ANIMAL EXPERIMENT; ARTICLE; CELL DIVISION; CELL PROLIFERATION; CHROMOSOME; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE MUTATION; HUMAN; HUMAN CELL; METHYLATION; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; WAARDENBURG SYNDROME; ZEBRA FISH; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEK293 CELL LINE; HUMAN CHROMOSOME; LARVA; METABOLISM;

DANIO RERIO; MAMMALIA;

ANIMALS; ARGININE; CHROMOSOMES, HUMAN; HEK293 CELLS; HUMANS; LARVA; METHYLATION; MITOSIS; PAIRED BOX TRANSCRIPTION FACTORS; PROTEIN-ARGININE N-METHYLTRANSFERASES; WAARDENBURG SYNDROME; ZEBRAFISH;

EID: 84939617609     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.607713     Document Type: Article

References (29)

1. Blake, J. A., and Ziman, M. R. (2014) Pax genes: regulators of lineage specification and progenitor cell maintenance. Development 141, 737-751
2. Vogan, K. J., and Gros, P. (1997) The C-terminal subdomain makes an important contribution to the DNA binding activity of the Pax-3 paired domain. J. Biol. Chem. 272, 28289-28295
3. Lang, D., Powell, S. K., Plummer, R. S., Young, K. P., and Ruggeri, B. A. (2007) PAX genes: roles in development, pathophysiology, and cancer. Biochem. Pharmacol. 73, 1-14
4. Maroto, M., Reshef, R., Münsterberg, A. E., Koester, S., Goulding, M., and Lassar, A. B. (1997) Ectopic Pax-3 activatesMyoDand Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89, 139-148
5. Ridgeway, A. G., and Skerjanc, I. S. (2001) Pax3 is essential for skeletal myogenesis and the expression of Six1 and Eya2. J. Biol. Chem. 276, 19033-19039
6. Lang, D., Lu, M. M., Huang, L., Engleka, K. A., Zhang, M., Chu, E. Y., Lipner, S., Skoultchi, A., Millar, S. E., and Epstein, J. A. (2005) Pax3 functions at a nodal point in melanocyte stem cell differentiation. Nature 433, 884-887
7. Kubic, J. D., Young, K. P., Plummer, R. S., Ludvik, A. E., and Lang, D. (2008) Pigmentation PAX-ways: the role of Pax3 in melanogenesis, melanocyte stem cell maintenance, and disease. Pigment Cell Melanoma Res. 21, 627-645
8. Bulut-Karslioglu, A., Perrera, V., Scaranaro, M., de la Rosa-Velazquez, I. A., van de Nobelen, S., Shukeir, N., Popow, J., Gerle, B., Opravil, S., Pagani, M., Meidhof, S., Brabletz, T., Manke, T., Lachner, M., and Jenuwein, T. (2012) A transcription factor-based mechanism for mouse heterochromatin formation. Nat. Struct. Mol. Biol. 19, 1023-1030
9. Neumann, B., Walter, T., Hériché, J. K., Bulkescher, J., Erfle, H., Conrad, C., Rogers, P., Poser, I., Held, M., Liebel, U., Cetin, C., Sieckmann, F., Pau, G., Kabbe, R., Wünsche, A., Satagopam, V., Schmitz, M. H., Chapuis, C., Gerlich, D. W., Schneider, R., Eils, R., Huber, W., Peters, J. M., Hyman, A. A., Durbin, R., Pepperkok, R., and Ellenberg, J. (2010) Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464, 721-727
10. Tassabehji, M., Newton, V. E., Liu, X. Z., Brady, A., Donnai, D., Krajewska-Walasek, M., Murday, V., Norman, A., Obersztyn, E., and Reardon, W. (1995) The mutational spectrum in Waardenburg syndrome. Hum. Mol. Genet. 4, 2131-2137
11. Pingault, V., Ente, D., Dastot-Le Moal, F., Goossens, M., Marlin, S., and Bondurand, N. (2010) Review and update of mutations causing Waardenburg syndrome. Hum. Mutat. 31, 391-406
12. Epstein, D. J., Vekemans, M., and Gros, P. (1991) splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3. Cell 67, 767-774
13. Birrane, G., Soni, A., and Ladias, J. A. (2009) Structural basis for DNA recognition by the human PAX3 homeodomain. Biochemistry 48, 1148-1155
14. Corry, G. N., Hendzel, M. J., and Underhill, D. A. (2008) Subnuclear localization and mobility are key indicators of PAX3 dysfunction in Waardenburg syndrome. Hum. Mol. Genet. 17, 1825-1837
15. Branscombe, T. L., Frankel, A., Lee, J. H., Cook, J. R., Yang, Z., Pestka, S., and Clarke, S. (2001) PRMT5 (Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J. Biol. Chem. 276, 32971-32976
16. Chang, B., Chen, Y., Zhao, Y., and Bruick, R. K. (2007) JMJD6 is a histone arginine demethylase. Science 318, 444-447
17. Hsieh, M. J., Yao, Y. L., Lai, I. L., and Yang, W. M. (2006) Transcriptional repression activity of PAX3 is modulated by competition between corepressor KAP1 and heterochromatin protein 1. Biochem. Biophys. Res. Commun. 349, 573-581
18. Lai, I. L., Lin, T. P., Yao, Y. L., Lin, C. Y., Hsieh, M. J., and Yang, W. M. (2010) Histone deacetylase 10 relieves repression on the melanogenic program by maintaining the deacetylation status of repressors. J. Biol. Chem. 285, 7187-7196
19. Richard, S., Morel, M., and Cléroux, P. (2005) Arginine methylation regulates IL-2 gene expression: a role for protein arginine methyltransferase 5 (PRMT5). Biochem. J. 388, 379-386
20. Yao, Y. L., and Yang, W. M. (2003) The metastasis-associated proteins 1 and 2 form distinct protein complexes with histone deacetylase activity. J. Biol. Chem. 278, 42560-42568
21. Hsieh, F. S., Chen, N. T., Yao, Y. L., Wang, S. Y., Chen, J. J., Lai, C. C., and Yang, W. M. (2014) The transcriptional repression activity of STAF65γ is facilitated by promoter tethering and nuclear import of class IIa histone deacetylases. Biochim. Biophys. Acta 1839, 579-591
22. Burke, L. J., Zhang, R., Bartkuhn, M., Tiwari, V. K., Tavoosidana, G., Kurukuti, S., Weth, C., Leers, J., Galjart, N., Ohlsson, R., and Renkawitz, R. (2005) CTCF binding and higher order chromatin structure of the H19 locus are maintained in mitotic chromatin. EMBO J. 24, 3291-3300
23. Westerfield, M. (2000) The Zebrafish Book.AGuide for the Laboratory Use of Zebrafish (Danio rerio), 4th Ed., University of Oregon Press, Eugene,OR
24. Jeon, H. Y., and Lee, H. (2013) Depletion of Aurora-A in zebrafish causes growth retardation due to mitotic delay and p53-dependent cell death. FEBS J. 280, 1518-1530
25. Wu, T. F., Yao, Y. L., Lai, I. L., Lee, T. H., Underhill, D. A., and Yang, W. M. (2014) PAX3 Loads onto pericentromeric heterochromatin during S phase through PARP1. Anticancer Res. 34, 4717-4722
26. Kadauke, S., Udugama, M. I., Pawlicki, J. M., Achtman, J. C., Jain, D. P., Cheng, Y., Hardison, R. C., and Blobel, G. A. (2012) Tissue-specific mitotic bookmarking by hematopoietic transcription factor GATA1. Cell 150, 725-737
27. Zaidi, S. K., Young, D. W., Montecino, M. A., Lian, J. B., van Wijnen, A. J., Stein, J. L., and Stein, G. S. (2010) Mitotic bookmarking of genes: a novel dimension to epigenetic control. Nat. Rev. Genet. 11, 583-589
28. Di Lorenzo, A., and Bedford, M. T. (2011) Histone arginine methylation. FEBS Lett. 585, 2024-2031
29. Caravaca, J. M., Donahue, G., Becker, J. S., He, X., Vinson, C., and Zaret, K. S. (2013) Bookmarking by specific and nonspecific binding of FoxA1 pioneer factor to mitotic chromosomes. Genes Dev. 27, 251-260