Maintenance of muscle myosin levels in adult C. elegans requires both the double bromodomain protein BET-1 and sumoylation

Biology Open

Volumn 2, Issue 12, 2013, Pages 1354-1363

  Fisher, Kate ^a   Gee, Fiona ^a   Wang, Siyao ^a   Xue, Feng ^a   Knapp, Stefan ^b   Philpott, Martin ^b   Wells, Christopher ^b   Rodriguez, Miriam ^c   Snoek, L Basten ^c   Kammenga, Jan ^c   Poulin, Gino B ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Body wall muscle; Bromodomain; C. elegans; Sumo

Indexed keywords

EID: 84979639627     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20136007     Document Type: Article

References (53)

1. Andersen, E. C. and Horvitz, H. R. (2007). Two C. elegans histone methyltransferases repress lin-3 EGF transcription to inhibit vulval development. Development 134, 2991-2999.
2. Andersen, E. C., Saffer, A. M. and Horvitz, H. R. (2008). Multiple levels of redundant processes inhibit Caenorhabditis elegans vulval cell fates. Genetics 179, 2001-2012.
3. Bisgrove, D. A., Mahmoudi, T., Henklein, P. and Verdin, E. (2007). Conserved P-TEFb-interacting domain of BRD4 inhibits HIV transcription. Proc. Natl. Acad. Sci. USA 104, 13690-13695.
4. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
5. Broday, L., Kolotuev, I., Didier, C., Bhoumik, A., Gupta, B. P., Sternberg, P. W., Podbilewicz, B. and Ronai, Z. (2004). The small ubiquitin-like modifier (SUMO) is required for gonadal and uterine-vulval morphogenesis in Caenorhabditis elegans. Genes Dev. 18, 2380-2391.
6. Ceol, C. J. and Horvitz, H. R. (2001). dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C. elegans vulval development. Mol. Cell 7, 461-473.
7. Coustham, V., Bedet, C., Monier, K., Schott, S., Karali, M. and Palladino, F. (2006). The C. elegans HP1 homologue HPL-2 and the LIN-13 zinc finger protein form a complex implicated in vulval development. Dev. Biol. 297, 308-322.
8. Cubeñas-Potts, C. and Matunis, M. J. (2013). SUMO: a multifaceted modifier of chromatin structure and function. Dev. Cell 24, 1-12.
9. Cui, M., Chen, J., Myers, T. R., Hwang, B. J., Sternberg, P. W., Greenwald, I. and Han, M. (2006). SynMuv genes redundantly inhibit lin-3/EGF expression to prevent inappropriate vulval induction in C. elegans. Dev. Cell 10, 667-672.
10. Dawson, M. A., Prinjha, R. K., Dittmann, A., Giotopoulos, G., Bantscheff, M., Chan, W. I., Robson, S. C., Chung, C. W., Hopf, C., Savitski, M. M. et al. (2011). Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 478, 529-533.
11. Delmore, J. E., Issa, G. C., Lemieux, M. E., Rahl, P. B., Shi, J., Jacobs, H. M., Kastritis, E., Gilpatrick, T., Paranal, R. M., Qi, J. et al. (2011). BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 146, 904-917.
12. DeVore, D. L., Horvitz, H. R. and Stern, M. J. (1995). An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites. Cell 83, 611-620.
13. Du, J., Wang, X., Miereles, C., Bailey, J. L., Debigare, R., Zheng, B., Price, S. R. and Mitch, W. E. (2004). Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J. Clin. Invest. 113, 115-123.
14. Ellis, H. M. and Horvitz, H. R. (1986). Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817-829.
15. Etheridge, T., Oczypok, E. A., Lehmann, S., Fields, B. D., Shephard, F., Jacobson, L. A. and Szewczyk, N. J. (2012). Calpains mediate integrin attachment complex maintenance of adult muscle in Caenorhabditis elegans. PLoS Genet. 8, e1002471.
16. Fay, D. S. and Yochem, J. (2007). The SynMuv genes of Caenorhabditis elegans in vulval development and beyond. Dev. Biol. 306, 1-9.
17. Filippakopoulos, P., Qi, J., Picaud, S., Shen, Y., Smith, W. B., Fedorov, O., Morse, E. M., Keates, T., Hickman, T. T., Felletar, I. et al. (2010). Selective inhibition of BET bromodomains. Nature 468, 1067-1073.
18. Fisher, K., Southall, S. M., Wilson, J. R. and Poulin, G. B. (2010). Methylation and demethylation activities of a C. elegans MLL-like complex attenuate RAS signalling. Dev. Biol. 341, 142-153.
19. Gareau, J. R. and Lima, C. D. (2010). The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell Biol. 11, 861-871.
20. Geiss-Friedlander, R. and Melchior, F. (2007). Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 8, 947-956.
21. Herndon, L. A., Schmeissner, P. J., Dudaronek, J. M., Brown, P. A., Listner, K. M., Sakano, Y., Paupard, M. C., Hall, D. H. and Driscoll, M. (2002). Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419, 808-814.
22. Huang, P. and Stern, M. J. (2004). FGF signaling functions in the hypodermis to regulate fluid balance in C. elegans. Development 131, 2595-2604.
23. Johnson, E. S. (2004). Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382.
24. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
25. Kerscher, O. (2007). SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 8, 550-555.
26. Kokel, M., Borland, C. Z., DeLong, L., Horvitz, H. R. and Stern, M. J. (1998). clr-1 encodes a receptor tyrosine phosphatase that negatively regulates an FGF receptor signaling pathway in Caenorhabditis elegans. Genes Dev. 12, 1425-1437.
27. Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693-705.
28. Leight, E. R., Glossip, D. and Kornfeld, K. (2005). Sumoylation of LIN-1 promotes transcriptional repression and inhibition of vulval cell fates. Development 132, 1047-1056.
29. Lipsick, J. S. (2004). synMuv verite - Myb comes into focus. Genes Dev. 18, 2837-2844.
30. Lovén, J., Hoke, H. A., Lin, C. Y., Lau, A., Orlando, D. A., Vakoc, C. R., Bradner, J. E., Lee, T. I. and Young, R. A. (2013). Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 153, 320-334.
31. Lu, X. and Horvitz, H. R. (1998). lin-35 and lin-53, two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48. Cell 95, 981-991.
32. Mitch, W. E. and Goldberg, A. L. (1996). Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N. Engl. J. Med. 335, 1897-1905.
33. Miura, M., Zhu, H., Rotello, R., Hartwieg, E. A. and Yuan, J. (1993). Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75, 653-660.
34. Moerman, D. G. and Williams, B. D. (2006). Sarcomere assembly in C. elegans muscle. WormBook 2006, 1-16.
35. Morgan, C. T., Lee, M. H. and Kimble, J. (2010). Chemical reprogramming of Caenorhabditis elegans germ cell fate. Nat. Chem. Biol. 6, 102-104.
36. Müller, J., Ory, S., Copeland, T., Piwnica-Worms, H. and Morrison, D. K. (2001). C-TAK1 regulates Ras signaling by phosphorylating the MAPK scaffold, KSR1. Mol. Cell 8, 983-993.
37. Nicodeme, E., Jeffrey, K. L., Schaefer, U., Beinke, S., Dewell, S., Chung, C. W., Chandwani, R., Marazzi, I., Wilson, P., Coste, H. et al. (2010). Suppression of inflammation by a synthetic histone mimic. Nature 468, 1119-1123.
38. Owen, D. J., Ornaghi, P., Yang, J. C., Lowe, N., Evans, P. R., Ballario, P., Neuhaus, D., Filetici, P. and Travers, A. A. (2000). The structural basis for the recognition of acetylated histone H4 by the bromodomain of histone acetyltransferase gcn5p. EMBO J. 19, 6141-6149.
39. Poulin, G., Dong, Y., Fraser, A. G., Hopper, N. A. and Ahringer, J. (2005). Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans. EMBO J. 24, 2613-2623.
40. Qadota, H., Inoue, M., Hikita, T., Köppen, M., Hardin, J. D., Amano, M., Moerman, D. G. and Kaibuchi, K. (2007). Establishment of a tissue-specific RNAi system in C. elegans. Gene 400, 166-173.
41. Rual, J. F., Ceron, J., Koreth, J., Hao, T., Nicot, A. S., Hirozane-Kishikawa, T., Vandenhaute, J., Orkin, S. H., Hill, D. E., van den Heuvel, S. et al. (2004). Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 14 10B, 2162-2168.
42. Sandri, M. (2013). Protein breakdown in muscle wasting: Role of autophagy-lysosome and ubiquitin-proteasome. Int. J. Biochem. Cell Biol. 45, 2121-2129.
43. Shibata, Y., Takeshita, H., Sasakawa, N. and Sawa, H. (2010). Double bromodomain protein BET-1 and MYST HATs establish and maintain stable cell fates in C. elegans. Development 137, 1045-1053.
44. Smyth, G. K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3.
45. Solari, F. and Ahringer, J. (2000). NURD-complex genes antagonise Ras-induced vulval development in Caenorhabditis elegans. Curr. Biol. 10, 223-226.
46. Sorimachi, H. and Ono, Y. (2012). Regulation and physiological roles of the calpain system in muscular disorders. Cardiovasc. Res. 96, 11-22.
47. Sundaram, M. V. (2006). RTK/Ras/MAPK signaling. WormBook 2006, 1-19.
48. Szewczyk, N. J. and Jacobson, L. A. (2003). Activated EGL-15 FGF receptor promotes protein degradation in muscles of Caenorhabditis elegans. EMBO J. 22, 5058-5067.
49. Szewczyk, N. J., Peterson, B. K. and Jacobson, L. A. (2002). Activation of Ras and the mitogen-activated protein kinase pathway promotes protein degradation in muscle cells of Caenorhabditis elegans. Mol. Cell. Biol. 22, 4181-4188.
50. Szewczyk, N. J., Peterson, B. K., Barmada, S. J., Parkinson, L. P. and Jacobson, L. A. (2007). Opposed growth factor signals control protein degradation in muscles of Caenorhabditis elegans. EMBO J. 26, 935-943.
51. Wang, S., Fisher, K. and Poulin, G. B. (2011). Lineage specific trimethylation of H3 on lysine 4 during C. elegans early embryogenesis. Dev. Biol. 355, 227-238.
52. Yoder, J. H., Chong, H., Guan, K. L. and Han, M. (2004). Modulation of KSR activity in Caenorhabditis elegans by Zn ions, PAR-1 kinase and PP2A phosphatase. EMBO J. 23, 111-119.
53. Zuber, J., Shi, J., Wang, E., Rappaport, A. R., Herrmann, H., Sison, E. A., Magoon, D., Qi, J., Blatt, K., Wunderlich, M. et al. (2011). RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia. Nature 478, 524-528.