Heterocomplex formation by Arp4 and β-actin is involved in the integrity of the Brg1 chromatin remodeling complex

Journal of Cell Science

Volumn 125, Issue 16, 2012, Pages 3870-3882

  Nishimoto, Naoki ^a   Watanabe, Masanori ^a   Watanabe, Shinya ^b   Sugimoto, Nozomi ^b   Yugawa, Takashi ^a   Ikura, Tsuyoshi ^c   Koiwai, Osamu ^d   Kiyono, Tohru ^a   Fujita, Masatoshi ^a,b  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

Actin; Arp4; Arp4 actin heterocomplex; Brg1 chromatin remodeling complex

Indexed keywords

ACTIN RELATED PROTEIN; ACTIN RELATED PROTEIN 4; BETA ACTIN; BRG1 PROTEIN; HISTONE ACETYLTRANSFERASE; MYC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA INTERFERENCE;

ACTINS; AMINO ACID SEQUENCE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA HELICASES; DNA-BINDING PROTEINS; HEK293 CELLS; HELA CELLS; HISTONES; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84869118895     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.104349     Document Type: Article

References (51)

1. Ayscough, K. R., Stryker, J., Pokala, N., Sanders, M., Crews, P. and Drubin, D. G. (1997). High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J. Cell Biol. 137, 399-416.
2. Bettinger, B. T., Gilbert, D. M. and Amberg, D. C. (2004). Actin up in the nucleus. Nat. Rev. Mol. Cell Biol. 5, 410-415.
3. Blessing, C. A., Ugrinova, G. T. and Goodson, H. V. (2004). Actin and ARPs: action in the nucleus. Trends Cell Biol. 14, 435-442.
4. Boyer, L. A. and Peterson, C. L. (2000). Actin-related proteins (Arps): conformational switches for chromatin-remodeling machines? Bioessays 22, 666-672.
5. Cai, Y., Jin, J., Tomomori-Sato, C., Sato, S., Sorokina, I., Parmely, T. J., Conaway, R. C. and Conaway, J. W. (2003). Identification of new subunits of the multiprotein mammalian TRRAP/TIP60-containing histone acetyltransferase complex. J. Biol. Chem. 278, 42733-42736.
6. Cairns, B. R., Erdjument-Bromage, H., Tempst, P., Winston, F. and Kornberg, R. D. (1998). Two actin-related proteins are shared functional components of the chromatin-remodeling complexes RSC and SWI/SNF. Mol. Cell 2, 639-651.
7. Chen, X., Peng, J., Pedram, M., Swenson, C. A. and Rubenstein, P. A. (1995). The effect of the S14A mutation on the conformation and thermostability of Saccharomyces cerevisiae G-actin and its interaction with adenine nucleotides. J. Biol. Chem. 270, 11415-11423.
8. Cui, K., Tailor, P., Liu, H., Chen, X., Ozato, K. and Zhao, K. (2004). The chromatin- remodeling BAF complex mediates cellular antiviral activities by promoter priming. Mol. Cell. Biol. 24, 4476-4486.
9. De La Cruz, E. M. and Pollard, T. D. (2001). Structural biology. Actin' up. Science 293, 616-618.
10. Fenn, S., Breitsprecher, D., Gerhold, C. B., Witte, G., Faix, J. and Hopfner, K.-P. (2011). Structural biochemistry of nuclear actin-related proteins 4 and 8 reveals their interaction with actin. EMBO J. 30, 2153-2166.
11. Fomproix, N. and Percipalle, P. (2004). An actin-myosin complex on actively transcribing genes. Exp. Cell Res. 294, 140-148.
12. Fujita, M., Ichinose, S., Kiyono, T., Tsurumi, T. and Omori, A. (2003). Establishment of latrunculin-A resistance in HeLa cells by expression of R183A D184A mutant β-actin. Oncogene 22, 627-631.
13. Galarneau, L., Nourani, A., Boudreault, A. A., Zhang, Y., Héliot, L., Allard, S., Savard, J., Lane, W. S., Stillman, D. J. and Côté, J. (2000). Multiple links between the NuA4 histone acetyltransferase complex and epigenetic control of transcription. Mol. Cell 5, 927-937.
14. Görzer, I., Schüller, C., Heidenreich, E., Krupanska, L., Kuchler, K. and Wintersberger, U. (2003). The nuclear actin-related protein Act3p/Arp4p of Saccharomyces cerevisiae is involved in transcription regulation of stress genes. Mol. Microbiol. 50, 1155-1171.
15. Harata, M., Oma, Y., Mizuno, S., Jiang, Y. W., Stillman, D. J. and Wintersberger, U. (1999). The nuclear actin-related protein of Saccharomyces cerevisiae, Act3p/ Arp4, interacts with core histones. Mol. Biol. Cell 10, 2595-2605.
16. Hertzog, M., van Heijenoort, C., Didry, D., Gaudier, M., Coutant, J., Gigant, B., Didelot, G., Préat, T., Knossow, M., Guittet, E. et al. (2004). The b-thymosin/WH2 domain; structural basis for the switch from inhibition to promotion of actin assembly. Cell 117, 611-623.
17. Hofmann, W. A., Stojiljkovic, L., Fuchsova, B., Vargas, G. M., Mavrommatis, E., Philimonenko, V., Kysela, K., Goodrich, J. A., Lessard, J. L., Hope, T. J. et al. (2004). Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II. Nat. Cell Biol. 6, 1094-1101.
18. Hu, P., Wu, S. and Hernandez, N. (2004). A role for β-actin in RNA polymerase III transcription. Genes Dev. 18, 3010-3015.
19. Kabsch, W. and Holmes, K. C. (1995). The actin fold. FASEB J. 9, 167-174.
20. Kabsch, W., Mannherz, H. G., Suck, D., Pai, E. F. and Holmes, K. C. (1990). Atomic structure of the actin:DNase I complex. Nature 347, 37-44.
21. Kukalev, A., Nord, Y., Palmberg, C., Bergman, T. and Percipalle, P. (2005). Actin and hnRNP U cooperate for productive transcription by RNA polymerase II. Nat. Struct. Mol. Biol. 12, 238-244.
22. Kundu, T. K., Wang, Z. and Roeder, R. G. (1999). Human TFIIIC relieves chromatin- mediated repression of RNA polymerase III transcription and contains an intrinsic histone acetyltransferase activity. Mol. Cell. Biol. 19, 1605-1615.
23. Kuroda, Y., Oma, Y., Nishimori, K., Ohta, T. and Harata, M. (2002). Brain-specific expression of the nuclear actin-related protein ArpNa and its involvement in mammalian SWI/SNF chromatin remodeling complex. Biochem. Biophys. Res. Commun. 299, 328-334.
24. Lee, J. H., Lee, J. Y., Chang, S. H., Kang, M. J. and Kwon, H. (2005). Effects of Ser2 and Tyr6 mutants of BAF53 on cell growth and p53-dependent transcription. Mol. Cells 19, 289-293.
25. Lee, K., Kang, M. J., Kwon, S. J., Kwon, Y. K., Kim, K. W., Lim, J.-H. and Kwon, H. (2007). Expansion of chromosome territories with chromatin decompaction in BAF53-depleted interphase cells. Mol. Biol. Cell 18, 4013-4023.
26. Liu, R., Liu, H., Chen, X., Kirby, M., Brown, P. O. and Zhao, K. (2001). Regulation of CSF1 promoter by the SWI/SNF-like BAF complex. Cell 106, 309-318.
27. Muller, J., Oma, Y., Vallar, L., Friederich, E., Poch, O. and Winsor, B. (2005). Sequence and comparative genomic analysis of actin-related proteins. Mol. Biol. Cell 16, 5736-5748.
28. Mullins, R. D., Heuser, J. A. and Pollard, T. D. (1998). The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl. Acad. Sci. USA 95, 6181-6186.
29. Nolen, B. J., Littlefield, R. S. and Pollard, T. D. (2004). Crystal structures of actin- related protein 2/3 complex with bound ATP or ADP. Proc. Natl. Acad. Sci. USA 101, 15627-15632.
30. Olave, I. A., Reck-Peterson, S. L. and Crabtree, G. R. (2002a). Nuclear actin and actin-related proteins in chromatin remodeling. Annu. Rev. Biochem. 71, 755-781.
31. Olave, I., Wang, W., Xue, Y., Kuo, A. and Crabtree, G. R. (2002b). Identification of a polymorphic, neuron-specific chromatin remodeling complex. Genes Dev. 16, 2509-2517.
32. Oliver, F. J., de la Rubia, G., Rolli, V., Ruiz-Ruiz, M. C., de Murcia, G. and Murcia, J. M. (1998). Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J. Biol. Chem. 273, 33533-33539.
33. Park, J., Wood, M. A. and Cole, M. D. (2002). BAF53 forms distinct nuclear complexes and functions as a critical c-Myc-interacting nuclear cofactor for oncogenic transformation. Mol. Cell. Biol. 22, 1307-1316.
34. Peterson, C. L., Zhao, Y. and Chait, B. T. (1998). Subunits of the yeast SWI/SNF complex are members of the actin-related protein (ARP) family. J. Biol. Chem. 273, 23641-23644.
35. Phelan, M. L., Sif, S., Narlikar, G. J. and Kingston, R. E. (1999). Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Mol. Cell 3, 247-253.
36. Philimonenko, V. V., Zhao, J., Iben, S., Dingová, H., Kyselá, K., Kahle, M., Zentgraf, H., Hofmann, W. A., de Lanerolle, P., Hozák, P. et al. (2004). Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat. Cell Biol. 6, 1165-1172.
37. Poch, O. and Winsor, B. (1997). Who's who among the Saccharomyces cerevisiae actin-related proteins? A classification and nomenclature proposal for a large family. Yeast 13, 1053-1058.
38. Rando, O. J., Zhao, K., Janmey, P. and Crabtree, G. R. (2002). Phosphatidylinositol- dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc. Natl. Acad. Sci. USA 99, 2824-2829.
39. Robinson, R. C., Turbedsky, K., Kaiser, D. A., Marchand, J. B., Higgs, H. N., Choe, S. and Pollard, T. D. (2001). Crystal structure of Arp2/3 complex. Science 294, 1679-1684.
40. Shen, X., Mizuguchi, G., Hamiche, A. and Wu, C. (2000). A chromatin remodelling complex involved in transcription and DNA processing. Nature 406, 541-544.
41. Shen, X., Ranallo, R., Choi, E. and Wu, C. (2003). Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell 12, 147-155.
42. Sohn, D. H., Lee, K. Y., Lee, C., Oh, J., Chung, H., Jeon, S. H. and Seong, R. H. (2007). SRG3 interacts directly with the major components of the SWI/SNF chromatin remodeling complex and protects them from proteasomal degradation. J. Biol. Chem. 282, 10614-10624.
43. Cdh1. Mol. Biol. Cell 19, 1007-1021.
44. Szerlong, H., Saha, A. and Cairns, B. R. (2003). The nuclear actin-related proteins Arp7 and Arp9: a dimeric module that cooperates with architectural proteins for chromatin remodeling. EMBO J. 22, 3175-3187.
45. Szerlong, H., Hinata, K., Viswanathan, R., Erdjument-Bromage, H., Tempst, P. and Cairns, B. R. (2008). The HSA domain binds nuclear actin-related proteins to regulate chromatin-remodeling ATPases. Nat. Struct. Mol. Biol. 15, 469-476.
46. Tatsumi, Y., Sugimoto, N., Yugawa, T., Narisawa-Saito, M., Kiyono, T. and Fujita, M. (2006). Deregulation of Cdt1 induces chromosomal damage without rereplication and leads to chromosomal instability. J. Cell Sci. 119, 3128-3140.
47. Welch, M. D., DePace, A. H., Verma, S., Iwamatsu, A. and Mitchison, T. J. (1997). The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J. Cell Biol. 138, 375-384.
48. Wertman, K. F. and Drubin, D. G. (1992). Actin constitution: guaranteeing the right to assemble. Science 258, 759-760.
49. Wertman, K. F., Drubin, D. G. and Botstein, D. (1992). Systematic mutational analysis of the yeast ACT1 gene. Genetics 132, 337-350.
50. Wu, J. I., Lessard, J., Olave, I. A., Qiu, Z., Ghosh, A., Graef, I. A. and Crabtree, G. R. (2007). Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56, 94-108.
51. Zhao, K., Wang, W., Rando, O. J., Xue, Y., Swiderek, K., Kuo, A. and Crabtree, G. R. (1998). Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95, 625-636.