The e3 SUMO ligase Nse2 regulates sumoylation and nuclear-tocytoplasmic translocation of skNAC-Smyd1 in myogenesis

Journal of Cell Science

Volumn 127, Issue 17, 2014, Pages 3794-3804

  Berkholz, Janine ^a   Michalick, Laura ^a   Munz, Barbara ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

M Bop; Mms21; Myogenic differentiation; Nse2; skNAC; Smyd1; Sumoylation

Indexed keywords

CHAPERONE; DNA BINDING PROTEIN; MUSCLE PROTEIN; NASCENT-POLYPEPTIDE-ASSOCIATED COMPLEX; SMYD1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE;

ANIMAL; CELL DIFFERENTIATION; CELL LINE; GENETICS; HEART MUSCLE; METABOLISM; MORPHOGENESIS; MOUSE; MUSCLE DEVELOPMENT; PHYSIOLOGY; SKELETAL MUSCLE; SUMOYLATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; DNA-BINDING PROTEINS; MICE; MOLECULAR CHAPERONES; MORPHOGENESIS; MUSCLE DEVELOPMENT; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOCARDIUM; SUMOYLATION; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 84906861958     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.150334     Document Type: Article

References (40)

1. Berger, F., Berkholz, J., Breustedt, T., Ploen, D. and Munz, B. (2012). Skeletal muscle-specific variant of nascent polypeptide associated complex alpha (skNAC): implications for a specific role in mammalian myoblast differentiation. Eur. J. Cell Biol. 91, 150-155.
2. Berkholz, J., Zakrzewicz, A. and Munz, B. (2013). skNAC depletion stimulates myoblast migration and perturbs sarcomerogenesis by enhancing calpain 1 and 3 activity. Biochem. J. 453, 303-310.
3. Brouwer, A. K., Schimmel, J., Wiegant, J. C., Vertegaal, A. C., Tanke, H. J. and Dirks, R. W. (2009). Telomeric DNA mediates de novo PML body formation. Mol. Biol. Cell 20, 4804-4815.
4. Chung, S. S., Ahn, B. Y., Kim, M., Kho, J. H., Jung, H. S. and Park, K. S. (2011). SUMO modification selectively regulates transcriptional activity of peroxisome-proliferator-activated receptor c in C2C12 myotubes. Biochem. J. 433, 155-161.
5. Chung, I., Leonhardt, H. and Rippe, K. (2011). De novo assembly of a PML nuclear subcompartment occurs through multiple pathways and induces telomere elongation. J. Cell Sci. 124, 3603-3618.
6. Garcia-Dominguez, M. and Reyes, J. C. (2009). SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim. Biophys. Acta 1789, 451-459.
7. Giorgino, F., de Robertis, O., Laviola, L., Montrone, C., Perrini, S., McCowen, K. C. and Smith, R. J. (2000). The sentrin-conjugating enzyme mUbc9 interacts with GLUT4 and GLUT1 glucose transporters and regulates transporter levels in skeletal muscle cells. Proc. Natl. Acad. Sci. USA 97, 1125-1130.
8. Glass, D. J. (2007). Two tales concerning skeletal muscle. J. Clin. Invest. 117, 2388-2391.
9. Grégoire, S. and Yang, X. J. (2005). Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol. Cell. Biol. 25, 2273-2287.
10. Hannoun, Z., Greenhough, S., Jaffray, E., Hay, R. T. and Hay, D. C. (2010). Post-translational modification by SUMO. Toxicology 278, 288-293.
11. Hsu, Y. H., Sarker, K. P., Pot, I., Chan, A., Netherton, S. J. and Bonni, S. (2006). Sumoylated SnoN represses transcription in a promoter-specific manner. J. Biol. Chem. 281, 33008-33018.
12. Just, S., Meder, B., Berger, I. M., Etard, C., Trano, N., Patzel, E., Hassel, D., Marquart, S., Dahme, T., Vogel, B. et al. (2011). The myosin-interacting protein SMYD1 is essential for sarcomere organization. J. Cell Sci. 124, 3127-3136.
13. Kampmann, U., Christensen, B., Nielsen, T. S., Pedersen, S. B., Ørskov, L., Lund, S., Møller, N. and Jessen, N. (2011). GLUT4 and UBC9 protein expression is reduced in muscle from type 2 diabetic patients with severe insulin resistance. PLoS ONE 6, e27854.
14. Kang, J., Gocke, C. B. and Yu, H. (2006). Phosphorylation-facilitated sumoylation of MEF2C negatively regulates its transcriptional activity. BMC Biochem. 7, 5.
15. Lallemand-Breitenbach, V. and de Thé, H. (2010). PML nuclear bodies. Cold Spring Harb. Perspect. Biol. 2, a000661.
16. 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.
17. Li, H., Randall, W. R. and Du, S. J. (2009). skNAC (skeletal Naca), a musclespecific isoform of Naca (nascent polypeptide-associated complex alpha), is required for myofibril organization. FASEB J. 23, 1988-2000.
18. Li, H., Xu, J., Bian, Y. H., Rotllant, P., Shen, T., Chu, W., Zhang, J., Schneider, M. and Du, S. J. (2011). Smyd1b_tv1, a key regulator of sarcomere assembly, is localized on the M-line of skeletal muscle fibers. PLoS ONE 6, e28524.
19. Li, H., Zhong, Y., Wang, Z., Gao, J., Xu, J., Chu, W., Zhang, J., Fang, S. and Du, S. J. (2013). Smyd1b is required for skeletal and cardiac muscle function in zebrafish. Mol. Biol. Cell 24, 3511-3521.
20. Luan, Z., Liu, Y., Stuhlmiller, T. J., Marquez, J. and Garcia-Castro, M. I. (2013). SUMOylation of Pax7 is essential for neural crest and muscle development. Cell. Mol. Life Sci. 70, 1793-1806.
21. Munz, B., Wiedmann, M., Lochmüller, H. and Werner, S. (1999). Cloning of novel injury-regulated genes. Implications for an important role of the musclespecific protein skNAC in muscle repair. J. Biol. Chem. 274, 13305-13310.
22. Munz, B., Hildt, E., Springer, M. L. and Blau, H. M. (2002). RIP2, a checkpoint in myogenic differentiation. Mol. Cell. Biol. 22, 5879-5886.
23. Park, C. Y., Pierce, S. A., von Drehle, M., Ivey, K. N., Morgan, J. A., Blau, H. M. and Srivastava, D. (2010). skNAC, a Smyd1-interacting transcription factor, is involved in cardiac development and skeletal muscle growth and regeneration. Proc. Natl. Acad. Sci. USA 107, 20750-20755.
24. Potthoff, M. J. and Olson, E. N. (2007). MEF2: a central regulator of diverse developmental programs. Development 134, 4131-4140.
25. Potts, P. R. (2009). The Yin and Yang of the MMS21-SMC5/6 SUMO ligase complex in homologous recombination. DNA Repair (Amst.) 8, 499-506.
26. Potts, P. R. and Yu, H. (2007). The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat. Struct. Mol. Biol. 14, 581-590.
27. Riquelme, C., Barthel, K. K. and Liu, X. (2006). SUMO-1 modification of MEF2A regulates its transcriptional activity. J. Cell. Mol. Med. 10, 132-144.
28. Riquelme, C., Barthel, K. K. B., Qin, X.-F. and Liu, X. (2006). Ubc9 expression is essential for myotube formation in C2C12. Exp. Cell Res. 312, 2132-2141.
29. Rothenbusch, U., Sawatzki, M., Chang, Y., Caesar, S. and Schlenstedt, G. (2012). Sumoylation regulates Kap114-mediated nuclear transport. EMBO J. 31, 2461-2472.
30. Simpson-Lavy, K. J. and Johnston, M. (2013). SUMOylation regulates the SNF1 protein kinase. Proc. Natl. Acad. Sci. USA 110, 17432-17437.
31. Sims, R. J., III, Weihe, E. K., Zhu, L., O'Malley, S., Harriss, J. V. and Gottlieb, P. D. (2002). m-Bop, a repressor protein essential for cardiogenesis, interacts with skNAC, a heart- and muscle-specific transcription factor. J. Biol. Chem. 277, 26524-26529.
32. Sorimachi, H. and Ono, Y. (2012). Regulation and physiological roles of the calpain system in muscular disorders. Cardiovasc. Res. 96, 11-22.
33. Stephan, A. K., Kliszczak, M. and Morrison, C. G. (2011). The Nse2/Mms21 SUMO ligase of the Smc5/6 complex in the maintenance of genome stability. FEBS Lett. 585, 2907-2913.
34. Tan, X., Rotllant, J., Li, H., De Deyne, P. and Du, S. J. (2006). SmyD1, a histone methyltransferase, is required for myofibril organization and muscle contraction in zebrafish embryos. Proc. Natl. Acad. Sci. USA 103, 2713-2718.
35. Wang, Y., Shankar, S. R., Kher, D., Ling, B. M. T. and Taneja, R. (2013). Sumoylation of the basic helix-loop-helix transcription factor sharp-1 regulates recruitment of the histone methyltransferase G9a and function in myogenesis. J. Biol. Chem. 288, 17654-17662.
36. Werner, A. and Melchior, F. (2012). SUMO unloads the Kap114 cab. EMBO J. 31, 2439-2440.
37. Wiedmann, B., Sakai, H., Davis, T. A. and Wiedmann, M. (1994). A protein complex required for signal-sequence-specific sorting and translocation. Nature 370, 434-440.
38. Wrighton, K. H., Liang, M., Bryan, B., Luo, K., Liu, M., Feng, X. H. and Lin, X. (2007). Transforming growth factor-beta-independent regulation of myogenesis by SnoN sumoylation. J. Biol. Chem. 282, 6517-6524.
39. Yotov, W. V. and St-Arnaud, R. (1996). Differential splicing-in of a proline-rich exon converts alphaNAC into a muscle-specific transcription factor. Genes Dev. 10, 1763-1772.
40. Zhao, J. (2007). Sumoylation regulates diverse biological processes. Cell. Mol. Life Sci. 64, 3017-3033.