The Kruppel-like Factor 15 as a Molecular Link between Myogenic Factors and a Chromosome 4q Transcriptional Enhancer Implicated in Facioscapulohumeral Dystrophy
Dmitriev, P; Petrov, A; Ansseau, Eugénieet al.
2011 • In Journal of Biological Chemistry, 286, p. 44620-44631
[en] Facioscapulohumeral muscular dystrophy (FSHD), a dominant hereditary disease with a prevalence of 7 per 100,000 individuals, is associated with a partial deletion in the subtelomeric D4Z4 repeat array on chromosome 4q. The D4Z4 repeat contains a strong transcriptional enhancer that activates promoters of several FSHD-related genes. We report here that the enhancer within the D4Z4 repeat binds the Krüppel-like factor KLF15. KLF15 was found to be up-regulated during myogenic differentiation induced by serum starvation or by overexpression of the myogenic differentiation factor MYOD. When overexpressed, KLF15 activated the D4Z4 enhancer and led to overexpression of DUX4c (Double homeobox 4, centromeric) and FRG2 (FSHD region gene 2) genes, whereas its silencing caused inactivation of the D4Z4 enhancer. In immortalized human myoblasts, the D4Z4 enhancer was activated by the myogenic factor MYOD, an effect that was abolished upon KLF15 silencing or when the KLF15-binding sites within the D4Z4 enhancer were mutated, indicating that the myogenesis-related activation of the D4Z4 enhancer was mediated by KLF15. KLF15 and several myogenesis-related factors were found to be expressed at higher levels in myoblasts, myotubes, and muscle biopsies from FSHD patients than in healthy controls. We propose that KLF15 serves as a molecular link between myogenic factors and the activity of the D4Z4 enhancer, and it thus contributes to the overexpression of the DUX4c and FRG2 genes during normal myogenic differentiation and in FSHD.
The Kruppel-like Factor 15 as a Molecular Link between Myogenic Factors and a Chromosome 4q Transcriptional Enhancer Implicated in Facioscapulohumeral Dystrophy
Publication date :
21 September 2011
Journal title :
Journal of Biological Chemistry
ISSN :
0021-9258
Publisher :
American Society for Biochemistry and Molecular Biology, Moldova
Lunt, P. W., and Harper, P. S. (1991) J. Med. Genet. 28, 655-664
van Deutekom, J. C., Wijmenga, C., van Tienhoven, E. A., Gruter, A. M., Hewitt, J. E., Padberg, G. W., van Ommen, G. J., Hofker, M. H., and Frants, R. R. (1993) Hum. Mol. Genet. 2, 2037-2042
Lemmers, R. J., Wohlgemuth, M., van der Gaag, K. J., van der Vliet, P. J., van Teijlingen, C. M., de Knijff, P., Padberg, G. W., Frants, R. R., and van der Maarel, S. M. (2007) Am. J. Hum. Genet. 81, 884-894
Laoudj-Chenivesse, D., Carnac, G., Bisbal, C., Hugon, G., Bouillot, S., Desnuelle, C., Vassetzky, Y., and Fernandez, A. (2005) J. Mol. Med. 83, 216-224
Osborne, R. J., Welle, S., Venance, S. L., Thornton, C. A., and Tawil, R. (2007) Neurology 68, 569-577
Arashiro, P., Eisenberg, I., Kho, A. T., Cerqueira, A. M., Canovas, M., Silva, H. C., Pavanello, R. C., Verjovski-Almeida, S., Kunkel, L. M., and Zatz, M. (2009) Proc. Natl. Acad. Sci. U.S.A. 106, 6220-6225
Bakay, M., Wang, Z., Melcon, G., Schiltz, L., Xuan, J., Zhao, P., Sartorelli, V., Seo, J., Pegoraro, E., Angelini, C., Shneiderman, B., Escolar, D., Chen, Y. W., Winokur, S. T., Pachman, L. M., Fan, C., Mandler, R., Nevo, Y., Gordon, E., Zhu, Y., Dong, Y., Wang, Y., and Hoffman, E. P. (2006) Brain 129, 996-1013
Celegato, B., Capitanio, D., Pescatori, M., Romualdi, C., Pacchioni, B., Cagnin, S., Viganò, A., Colantoni, L., Begum, S., Ricci, E., Wait, R., Lanfranchi, G., and Gelfi, C. (2006) Proteomics 6, 5303-5321
Winokur, S. T., Chen, Y. W., Masny, P. S., Martin, J. H., Ehmsen, J. T., Tapscott, S. J., van der Maarel, S. M., Hayashi, Y., and Flanigan, K. M. (2003) Hum. Mol. Genet. 12, 2895-2907
Gabellini, D., Green, M. R., and Tupler, R. (2002) Cell 110, 339-348
Rijkers, T., Deidda, G., van Koningsbruggen, S., van Geel, M., Lemmers, R. J., van Deutekom, J. C., Figlewicz, D., Hewitt, J. E., Padberg, G. W., Frants, R. R., and van der Maarel, S. M. (2004) J. Med. Genet. 41, 826-836
Ansseau, E., Laoudj-Chenivesse, D., Marcowycz, A., Tassin, A., Vanderplanck, C., Sauvage, S., Barro, M., Mahieu, I., Leroy, A., Leclercq, I., Mainfroid, V., Figlewicz, D., Mouly, V., Butler-Browne, G., Belayew, A., and Coppée, F. (2009) PLoS ONE 4, e7482
Dixit, M., Ansseau, E., Tassin, A., Winokur, S., Shi, R., Qian, H., Sauvage, S., Mattéotti, C., van Acker, A. M., Leo, O., Figlewicz, D., Barro, M., Laoudj-Chenivesse, D., Belayew, A., Coppée, F., and Chen, Y. W. (2007) Proc. Natl. Acad. Sci. U.S.A. 104, 18157-18162
Dmitriev, P., Lipinski, M., and Vassetzky, Y. S. (2009) Neuromuscul. Disord. 19, 17-20
Cabianca, D. S., and Gabellini, D. (2010) J. Cell Biol. 191, 1049-1060
Bosnakovski, D., Xu, Z., Gang, E. J., Galindo, C. L., Liu, M., Simsek, T., Garner, H. R., Agha-Mohammadi, S., Tassin, A., Coppée, F., Belayew, A., Perlingeiro, R. R., and Kyba, M. (2008) EMBO J. 27, 2766-2779
Bosnakovski, D., Lamb, S., Simsek, T., Xu, Z., Belayew, A., Perlingeiro, R., and Kyba, M. (2008) Exp. Neurol. 214, 87-96
Gabellini, D., D'Antona, G., Moggio, M., Prelle, A., Zecca, C., Adami, R., Angeletti, B., Ciscato, P., Pellegrino, M. A., Bottinelli, R., Green, M. R., and Tupler, R. (2006) Nature 439, 973-977
Lemmers, R. J., van der Vliet, P. J., Klooster, R., Sacconi, S., Camaño, P., Dauwerse, J. G., Snider, L., Straasheijm, K. R., van Ommen, G. J., Padberg, G. W., Miller, D. G., Tapscott, S. J., Tawil, R., Frants, R. R., and van der Maarel, S. M. (2010) Science 329, 1650-1653
Petrov, A. P., Laoudj, D., and Vassetzky, Y. S. (2003) Genetics 39, 147-151
Petrov, A., Allinne, J., Pirozhkova, I., Laoudj, D., Lipinski, M., and Vassetzky, Y. S. (2008) Genome Res. 18, 39-45
Coppée, F., Mattéotti, C., Anseau, E., Sauvage, S., Leclercq, I., Leroy, A., Marcowycz, A., Gerbaux, C., Figlewicz, D., Ding, H., and Belayew, A. (2004) in Facioscapulohumeral Muscular Dystrophy: Clinical Medicine and Molecular Biology (Upadhyaya, M., and Cooper, D., eds) pp. 1-250, Garland:BIOS Scientific Publishers, Abingdon, UK
Pirozhkova, I., Petrov, A., Dmitriev, P., Laoudj, D., Lipinski M, and Vassetzky, Y. S. (2008) PLoS ONE 3, e3389
Bodega, B., Ramirez, G. D., Grasser, F., Cheli, S., Brunelli, S., Mora, M., Meneveri, R., Marozzi, A., Mueller, S., Battaglioli, E., and Ginelli, E. (2009) BMC Biol. 7, 41
Ansseau, E., Marcowycz, A., Laoudj-Chenivesse, D., Tassin, A., Sauvage, S., Vanderplanck, C., Barro, M., Leroy, A., Leclercq, I., Mainfroid, V., Figlewicz, D., Belayew, A., and Coppée, F. (2009) PLoS ONE, e7482
Hsu, D. K., Guo, Y., Alberts, G. F., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Peifley, K. A., and Winkles, J. A. (1996) J. Biol. Chem. 271, 13786-13795
Zhu, C. H., Mouly, V., Cooper, R. N., Mamchaoui, K., Bigot, A., Shay, J. W., Di Santo, J. P., Butler-Browne, G. S., and Wright, W. E. (2007) Aging Cell 6, 515-523
Barro, M., Carnac, G., Flavier, S., Mercier, J., Vassetzky, Y., and Laoudj- Chenivesse, D. (2010) J. Cell. Mol. Med. 14, 275-289
Yu, J., de Belle, I., Liang, H., and Adamson, E. D. (2004) Mol. Cell 15, 83-94
Otteson, D. C., Liu, Y., Lai, H., Wang, C., Gray, S., Jain, M. K., and Zack, D. J. (2004) Invest. Ophthalmol. Vis. Sci. 45, 2522-2530
Meijer, A. H., Ouwerkerk, P. B., and Hoge, J. H. (1998) Yeast 14, 1407-1415
Ausubel, F. M. (2003) Current Protocols in Molecular Biology, Section 12.1 (Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K., eds) John Wiley & Sons, Hoboken, NJ
Otteson, D. C., Lai, H., Liu, Y., and Zack, D. J. (2005) BMC Mol. Biol. 6, 15
Uchida, S., Sasaki, S., and Marumo, F. (2001) Kidney Int. 60, 416-421
Lemaire, P., Vesque, C., Schmitt, J., Stunnenberg, H., Frank, R., and Charnay, P. (1990) Mol. Cell. Biol. 10, 3456-3467
Adachi, H., and Tsujimoto, M. (2002) J. Biol. Chem. 277, 24014-24021
Chen, Q. K., Hertz, G. Z., and Stormo, G. D. (1995) Comput. Appl. Biosci. 11, 563-566
Workman, C. T., Yin, Y., Corcoran, D. L., Ideker, T., Stormo, G. D., and Benos, P. V. (2005) Nucleic Acids Res. 33, W389-W392
McDonald, J. H. (2009) Handbook of Biological Statistics, pp. 1-313, Sparky House Publishing, Baltimore, MD
Livak, K. J., and Schmittgen, T. D. (2001) Methods 25, 402-408
Viñals, F., Fandos, C., Santalucia, T., Ferré, J., Testar, X., Palacín, M., and Zorzano, A. (1997) J. Biol. Chem. 272, 12913-12921
Gray, S., Feinberg, M. W., Hull, S., Kuo, C. T., Watanabe, M., Sen-Banerjee, S., DePina, A., Haspel, R., and Jain, M. K. (2002) J. Biol. Chem. 277, 34322-34328
Yamamoto, J., Ikeda, Y., Iguchi, H., Fujino, T., Tanaka, T., Asaba, H., Iwasaki, S., Ioka, R. X., Kaneko, I. W., Magoori, K., Takahashi, S., Mori, T., Sakaue, H., Kodama, T., Yanagisawa, M., Yamamoto, T. T., Ito, S., and Sakai, J. (2004) J. Biol. Chem. 279, 16954-16962
Fisch, S., Gray, S., Heymans, S., Haldar, S. M., Wang, B., Pfister, O., Cui, L., Kumar, A., Lin, Z., Sen-Banerjee, S., Das, H., Petersen, C. A., Mende, U., Burleigh, B. A., Zhu, Y., Pinto, Y. M., Pinto, Y., Liao, R., and Jain, M. K. (2007) Proc. Natl. Acad. Sci. U.S.A. 104, 7074-7079
Wang, B., Haldar, S. M., Lu, Y., Ibrahim, O. A., Fisch, S., Gray, S., Leask, A., and Jain, M. K. (2008) J. Mol. Cell. Cardiol. 45, 193-197
Ottaviani, A., Rival-Gervier, S., Boussouar, A., Foerster, A. M., Rondier, D., Sacconi, S., Desnuelle, C., Gilson, E., and Magdinier, F. (2009) PLoS Genet. 5, e1000394
Mori, T., Sakaue, H., Iguchi, H., Gomi, H., Okada, Y., Takashima, Y., Nakamura, K., Nakamura, T., Yamauchi, T., Kubota, N., Kadowaki, T., Matsuki, Y., Ogawa, W., Hiramatsu, R., and Kasuga, M. (2005) J. Biol. Chem. 280, 12867-12875
Klooster, R., Straasheijm, K., Shah, B., Sowden, J., Frants, R., Thornton, C., Tawil, R., and van der Maarel, S. (2009) Eur. J. Hum. Genet. 17, 1615-1624
Wijmenga, C., Hewitt, J. E., Sandkuijl, L. A., Clark, L. N., Wright, T. J., Dauwerse, H. G., Gruter, A. M., Hofker, M. H., Moerer, P., Williamson, R., Van Ommen, G. B., Padberg, G., and Frants, R. (1992) Nat. Genet. 2, 26-30
Uchida, S., Tanaka, Y., Ito, H., Saitoh-Ohara, F., Inazawa, J., Yokoyama, K. K., Sasaki, S., and Marumo, F. (2000) Mol. Cell. Biol. 20, 7319-7331
Leenders, J. J., Wijnen, W. J., Hiller, M., van der Made, I., Lentink, V., van Leeuwen, R. E., Herias, V., Pokharel, S., Heymans, S., de Windt, L. J., Høydal, M. A., Pinto, Y. M., and Creemers, E. E. (2010) J. Biol. Chem. 285, 27449-27456
Gray, S., Wang, B., Orihuela, Y., Hong, E. G., Fisch, S., Haldar, S., Cline, G. W., Kim, J. K., Peroni, O. D., Kahn, B. B., and Jain, M. K. (2007) Cell Metab. 5, 305-312
Winokur, S. T., Barrett, K., Martin, J. H., Forrester, J. R., Simon, M., Tawil, R., Chung, S. A., Masny, P. S., and Figlewicz, D. A. (2003) Neuromuscul. Disord. 13, 322-333
Luo, S. W., Zhang, C., Zhang, B., Kim, C. H., Qiu, Y. Z., Du, Q. S., Mei, L., and Xiong, W. C. (2009) EMBO J. 28, 2568-2582
Huang, C., Han, Y., Wang, Y., Sun, X., Yan, S., Yeh, E. T., Chen, Y., Cang, H., Li, H., Shi, G., Cheng, J., Tang, X., and Yi, J. (2009) EMBO J. 28, 2748-2762
Petrov, A., Pirozhkova, I., Carnac, G., Laoudj, D., Lipinski, M., and Vassetzky, Y. S. (2006) Proc. Natl. Acad. Sci. U.S.A. 103, 6982-6987
Gabriëls, J., Beckers, M. C., Ding, H., De Vriese, A., Plaisance, S., van der Maarel, S. M., Padberg, G. W., Frants, R. R., Hewitt, J. E., Collen, D., and Belayew, A. (1999) Gene 236, 25-32