Emerin inhibits Lmo7 binding to the Pax3 and MyoD promoters and expression of myoblast proliferation genes

Journal of Cell Science

Volumn 124, Issue 10, 2011, Pages 1691-1702

  Dedeic, Zinaida ^a   Cetera, Maureen ^a   Cohen, Tatiana V ^b   Holaska, James M ^a,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Emerin; Emerin Dreifuss muscular dystrophy; Lmo7; Myogenic differentiation; Nuclear envelope

Indexed keywords

BETA TUBULIN; EMERIN; GAMMA TUBULIN; GREEN FLUORESCENT PROTEIN; MYOD PROTEIN; MYOGENIC FACTOR 5; MYOGENIN; PROTEIN LMO7; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX7; UNCLASSIFIED DRUG; TRANSCRIPTION FACTOR LMO7;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; IN VITRO STUDY; MYF5 GENE; MYOBLAST; MYOD GENE; MYOTUBE; NONHUMAN; PAX3 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CELL LINE; CELL NUCLEUS; CYTOPLASM; DOWN-REGULATION; FLUORESCENT ANTIBODY TECHNIQUE; HOMEODOMAIN PROTEINS; MEMBRANE PROTEINS; MICE; MYOBLASTS; MYOD PROTEIN; NUCLEAR PROTEINS; PAIRED BOX TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 79956083487     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.080259     Document Type: Article

References (62)

1. Amanchy, R., Kalume, D. E., Iwahori, A., Zhong, J. and Pandey, A. (2005). Phosphoproteome analysis of HeLa cells using stable isotope labeling with amino acids in cell culture (SILAC). J. Proteome Res. 4, 1661-1671.
2. Bajard, L., Relaix, F., Lagha, M., Rocancourt, D., Daubas, P. and Buckingham, M. E. (2006). A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 20, 2450-2464.
3. Bakay, M., Wang, Z., Melcon, G., Schiltz, L., Xuan, J., Zhao, P., Sartorelli, V., Seo, J., Pegoraro, E., Angelini, C. et al. (2006). Nuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration. Brain 129, 996-1013.
4. Beausoleil, S. A., Villen, J., Gerber, S. A., Rush, J. and Gygi, S. P. (2006). A probabilitybased approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24, 1285-1292.
5. Boutet, S. C., Disatnik, M. H., Chan, L. S., Iori, K. and Rando, T. A. (2007). Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors. Cell 130, 349-362.
6. Boyle, S., Gilchrist, S., Bridger, J. M., Mahy, N. L., Ellis, J. A. and Bickmore, W. A. (2001). The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum. Mol. Genet. 10, 211-219.
7. Brill, L. M., Salomon, A. R., Ficarro, S. B., Mukherji, M., Stettler-Gill, M. and Peters, E. C. (2004). Robust phosphoproteomic profiling of tyrosine phosphorylation sites from human T cells using immobilized metal affinity chromatography and tandem mass spectrometry. Anal. Chem. 76, 2763-2772.
8. Brunelli, S., Relaix, F., Baesso, S., Buckingham, M. and Cossu, G. (2007). Beta cateninindependent activation of MyoD in presomitic mesoderm requires PKC and depends on Pax3 transcriptional activity. Dev. Biol. 304, 604-614.
9. Chen, I. H., Huber, M., Guan, T., Bubeck, A. and Gerace, L. (2006). Nuclear envelope transmembrane proteins (NETs) that are up-regulated during myogenesis. BMC Cell Biol. 7, 38.
10. Dephoure, N., Zhou, C., Villen, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J. and Gygi, S. P. (2008). A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105, 10762-10767.
11. Fidzianska, A. and Hausmanowa-Petrusewicz, I. (2003). Architectural abnormalities in muscle nuclei. Ultrastructural differences between X-linked and autosomal dominant forms of EDMD. J. Neurol. Sci. 210, 47-51.
12. Frock, R. L., Kudlow, B. A., Evans, A. M., Jameson, S. A., Hauschka, S. D. and Kennedy, B. K. (2006). Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev. 20, 486-500.
13. Goldhamer, D. J., Faerman, A., Shani, M. and Emerson, C. P., Jr (1992). Regulatory elements that control the lineage-specific expression of myoD. Science 256, 538-542.
14. Goulding, M., Lumsden, A. and Paquette, A. J. (1994). Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120, 957-971.
15. Hetzer, M. W., Walther, T. C. and Mattaj, I. W. (2005). Pushing the envelope: structure, function, and dynamics of the nuclear periphery. Annu. Rev. Cell Dev. Biol. 21, 347-380.
16. Hirano, Y., Segawa, M., Ouchi, F. S., Yamakawa, Y., Furukawa, K., Takeyasu, K. and Horigome, T. (2005). Dissociation of emerin from barrier-to-autointegration factor is regulated through mitotic phosphorylation of emerin in a xenopus egg cell-free system. J. Biol. Chem. 280, 39925-39933.
17. Holaska, J. M. and Wilson, K. L. (2006). Multiple roles for emerin: implications for Emery-Dreifuss muscular dystrophy. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 288, 676-680.
18. Holaska, J. M. and Wilson, K. L. (2007). An emerin "proteome" : purification of distinct emerin-containing complexes from HeLa cells suggests molecular basis for diverse roles including gene regulation, mRNA splicing, signaling, mechanosensing, and nuclear architecture. Biochemistry 46, 8897-8908.
19. Holaska, J., Lee, K., Kowalski, A. and Wilson, K. (2003). Transcriptional repressor germ cell-less (GCL) and barrier-to-autointegration factor (BAF) compete for binding to emerin in vitro. J. Biol. Chem. 278, 6969-6975.
20. Holaska, J. M., Rais-Bahrami, S. and Wilson, K. L. (2006). Lmo7 is an emerin-binding protein that regulates the transcription of emerin and many other muscle-relevant genes. Hum. Mol. Genet. 15, 3459-3472.
21. Hutcheson, D. A., Zhao, J., Merrell, A., Haldar, M. and Kardon, G. (2009). Embryonic and fetal limb myogenic cells are derived from developmentally distinct progenitors and have different requirements for beta-catenin. Genes Dev. 23, 997-1013.
22. Kuang, S. and Rudnicki, M. A. (2008). The emerging biology of satellite cells and their therapeutic potential. Trends Mol. Med. 14, 82-91.
23. Kuang, S., Charge, S. B., Seale, P., Huh, M. and Rudnicki, M. A. (2006). Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol. 172, 103-113.
24. Kuang, S., Kuroda, K., Le Grand, F. and Rudnicki, M. A. (2007). Asymmetric selfrenewal and commitment of satellite stem cells in muscle. Cell 129, 999-1010.
25. Kucharczuk, K. L., Love, C. M., Dougherty, N. M. and Goldhamer, D. J. (1999). Finescale transgenic mapping of the MyoD core enhancer: MyoD is regulated by distinct but overlapping mechanisms in myotomal and non-myotomal muscle lineages. Development 126, 1957-1965.
26. Kurihara, L. J., Semenova, E., Miller, W., Ingram, R. S., Guan, X. J. and Tilghman, S. M. (2002). Candidate genes required for embryonic development: a comparative analysis of distal mouse chromosome 14 and human chromosome 13q22. Genomics 79, 154-161.
27. L'Honore, A., Rana, V., Arsic, N., Franckhauser, C., Lamb, N. J. and Fernandez, A. (2007). Identification of a new hybrid serum response factor and myocyte enhancer factor 2-binding element in MyoD enhancer required for MyoD expression during myogenesis. Mol. Biol. Cell 18, 1992-2001.
28. Lee, H., Quinn, J. C., Prasanth, K. V., Swiss, V. A., Economides, K. D., Camacho, M. M., Spector, D. L. and Abate-Shen, C. (2006). PIAS1 confers DNA-binding specificity on the Msx1 homeoprotein. Genes Dev. 20, 784-794.
29. Lee, K. K., Haraguchi, T., Lee, R. S., Koujin, T., Hiraoka, Y. and Wilson, K. L. (2001). Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J. Cell Sci. 114, 4567-4573.
30. Leibham, D., Wong, M. W., Cheng, T. C., Schroeder, S., Weil, P. A., Olson, E. N. and Perry, M. (1994). Binding of TFIID and MEF2 to the TATA element activates transcription of the Xenopus MyoDa promoter. Mol. Cell. Biol. 14, 686-699.
31. Lin, F., Morrison, J. M., Wu, W. and Worman, H. J. (2005). MAN1, an integral protein of the inner nuclear membrane, binds Smad2 and Smad3 and antagonizes transforming growth factor-beta signaling. Hum. Mol. Genet. 14, 437-445.
32. Lindvall, J. M., Blomberg, K. E., Wennborg, A. and Smith, C. I. (2005). Differential expression and molecular characterisation of Lmo7, Myo1e, Sash1, and Mcoln2 genes in Btk-defective B-cells. Cell. Immunol. 235, 46-55.
33. Margalit, A., Brachner, A., Gotzmann, J., Foisner, R. and Gruenbaum, Y. (2007). Barrier-to-autointegration factor-a BAFfling little protein. Trends Cell Biol. 17, 202-208.
34. Markiewicz, E., Tilgner, K., Barker, N., van de Wetering, M., Clevers, H., Dorobek, M., Hausmanowa-Petrusewicz, I., Ramaekers, F. C., Broers, J. L., Blankesteijn, W. M. et al. (2006). The inner nuclear membrane protein emerin regulates beta-catenin activity by restricting its accumulation in the nucleus. EMBO J. 25, 3275-3285.
35. Maroto, M., Reshef, R., Munsterberg, A. E., Koester, S., Goulding, M. and Lassar, A. B. (1997). Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89, 139-148.
36. Melcon, G., Kozlov, S., Cutler, D. A., Sullivan, T., Hernandez, L., Zhao, P., Mitchell, S., Nader, G., Bakay, M., Rottman, J. N. et al. (2006). Loss of emerin at the nuclear envelope disrupts the Rb1/E2F and MyoD pathways during muscle regeneration. Hum. Mol. Genet. 15, 637-651.
37. Montarras, D., Morgan, J., Collins, C., Relaix, F., Zaffran, S., Cumano, A., Partridge, T. and Buckingham, M. (2005). Direct isolation of satellite cells for skeletal muscle regeneration. Science 309, 2064-2067.
38. Osada, S., Ohmori, S. Y. and Taira, M. (2003). XMAN1, an inner nuclear membrane protein, antagonizes BMP signaling by interacting with Smad1 in Xenopus embryos. Development 130, 1783-1794.
39. Oustanina, S., Hause, G. and Braun, T. (2004). Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J. 23, 3430-3439.
40. Pan, D., Estevez-Salmeron, L. D., Stroschein, S. L., Zhu, X., He, J., Zhou, S. and Luo, K. (2005). The integral inner nuclear membrane protein MAN1 physically interacts with the R-Smad proteins to repress signaling by the transforming growth factor-{beta} superfamily of cytokines. J. Biol. Chem. 280, 15992-16001.
41. Pedraza-Alva, G., Zingg, J. M. and Jost, J. P. (1994). AP-1 binds to a putative cAMP response element of the MyoD1 promoter and negatively modulates MyoD1 expression in dividing myoblasts. J. Biol. Chem. 269, 6978-6985.
42. Pownall, M. E., Gustafsson, M. K. and Emerson, C. P., Jr (2002). Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 18, 747-783.
43. Raju, G. P., Dimova, N., Klein, P. S. and Huang, H. C. (2003). SANE, a novel LEM domain protein, regulates bone morphogenetic protein signaling through interaction with Smad1. J. Biol. Chem. 278, 428-437.
44. Relaix, F., Rocancourt, D., Mansouri, A. and Buckingham, M. (2004). Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes Dev. 18, 1088-1105.
45. Relaix, F., Montarras, D., Zaffran, S., Gayraud-Morel, B., Rocancourt, D., Tajbakhsh, S., Mansouri, A., Cumano, A. and Buckingham, M. (2006). Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 172, 91-102.
46. Roberts, R. C., Sutherland-Smith, A. J., Wheeler, M. A., Jensen, O. N., Emerson, L. J., Spiliotis, I. I., Tate, C. G., Kendrick-Jones, J. and Ellis, J. A. (2006). The Emery-Dreifuss muscular dystrophy associated-protein emerin is phosphorylated on serine 49 by protein kinase A. FEBS J. 273, 4562-4575.
47. Rozenblum, E., Vahteristo, P., Sandberg, T., Bergthorsson, J. T., Syrjakoski, K., Weaver, D., Haraldsson, K., Johannsdottir, H. K., Vehmanen, P., Nigam, S. et al. (2002). A genomic map of a 6-Mb region at 13q21-q22 implicated in cancer development: identification and characterization of candidate genes. Hum. Genet. 110, 111-121.
48. Rudnicki, M. A., Le Grand, F., McKinnell, I. and Kuang, S. (2008). The molecular regulation of muscle stem cell function. Cold Spring Harb. Symp. Quant. Biol. 73, 323-331.
49. Schlosser, A., Amanchy, R. and Otto, H. (2006). Identification of tyrosine-phosphorylation sites in the nuclear membrane protein emerin. FEBS J. 273, 3204-3215.
50. Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruss, P. and Rudnicki, M. A. (2000). Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777-786.
51. Semenova, E., Wang, X., Jablonski, M. M., Levorse, J. and Tilghman, S. M. (2003). An engineered 800 kilobase deletion of Uchl3 and Lmo7 on mouse chromosome 14 causes defects in viability, postnatal growth and degeneration of muscle and retina. Hum. Mol. Genet. 12, 1301-1312.
52. Shumaker, D. K., Lee, K. K., Tanhehco, Y. C., Craigie, R. and Wilson, K. L. (2001). LAP2 binds to BAF-DNA complexes: requirement for the LEM domain and modulation by variable regions. EMBO J. 20, 1754-1764.
53. Somech, R., Shaklai, S., Geller, O., Amariglio, N., Simon, A. J., Rechavi, G. and Gal-Yam, E. N. (2005). The nuclear-envelope protein and transcriptional repressor LAP2beta interacts with HDAC3 at the nuclear periphery, and induces histone H4 deacetylation. J. Cell Sci. 118, 4017-4025.
54. Sorokin, A. V., Kim, E. R. and Ovchinnikov, L. P. (2007). Nucleocytoplasmic transport of proteins. Biochemistry (Mosc.) 72, 1439-1457.
55. Squarzoni, S., Sabatelli, P., Capanni, C., Lattanzi, G., Rutigliano, C., Columbaro, M., Mattioli, E., Rocca, M. and Maraldi, N. M. (2005). Emerin increase in regenerating muscle fibers. Eur. J. Histochem. 49, 355-362.
56. Tajbakhsh, S. and Buckingham, M. (2000). The birth of muscle progenitor cells in the mouse: spatiotemporal considerations. Curr. Top. Dev. Biol. 48, 225-268.
57. Tajbakhsh, S., Rocancourt, D., Cossu, G. and Buckingham, M. (1997). Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89, 127-138.
58. Tapscott, S. J., Lassar, A. B. and Weintraub, H. (1992). A novel myoblast enhancer element mediates MyoD transcription. Mol. Cell. Biol. 12, 4994-5003.
59. Tifft, K. E., Bradbury, K. A. and Wilson, K. L. (2009). Tyrosine phosphorylation of nuclear-membrane protein emerin by Src, Abl and other kinases. J. Cell Sci. 122, 3780-3790.
60. Tilgner, K., Wojciechowicz, K., Jahoda, C., Hutchison, C. and Markiewicz, E. (2009). Dynamic complexes of A-type lamins and emerin influence adipogenic capacity of the cell via nucleocytoplasmic distribution of beta-catenin. J. Cell Sci. 122, 401-413.
61. Vlcek, S. and Foisner, R. (2007). Lamins and lamin-associated proteins in aging and disease. Curr. Opin. Cell Biol. 19, 298-304.
62. Zhu, B. K. and Pruitt, S. C. (2005). Determination of transcription factors and their possible roles in the regulation of Pax3 gene expression in the mouse B16 F1 melanoma cell line. Melanoma Res. 15, 363-373.