Persistent nuclear actin filaments inhibit transcription by RNA polymerase II

Journal of Cell Science

Volumn 129, Issue 18, 2016, Pages 3412-3425

  Serebryannyy, Leonid A ^a   Parilla, Megan ^a   Annibale, Paolo ^b   Cruz, Christina M ^a   Laster, Kyle ^c   Gratton, Enrico ^b   Kudryashov, Dmitri ^d   Kosak, Steven T ^c   Gottardi, Cara J ^e   de Lanerolle, Primal ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d OHIO STATE UNIVERSITY   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Actin; Nuclear actin filaments; Nucleus; RNA polymerase II; Transcription

Indexed keywords

ACTIN; RNA POLYMERASE II; CROSS LINKING REAGENT; MESSENGER RNA;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FLUORESCENCE CORRELATION SPECTROSCOPY; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NONHUMAN; POINT MUTATION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SEDIMENTATION; UPREGULATION; ANIMAL; CELL NUCLEUS; CHLOROCEBUS AETHIOPS; COS CELL LINE; GENETICS; HELA CELL LINE; METABOLISM; PROTEIN TRANSPORT;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CELL NUCLEUS; CELL PROLIFERATION; CERCOPITHECUS AETHIOPS; COS CELLS; CROSS-LINKING REAGENTS; HELA CELLS; HUMANS; POLYMERIZATION; PROTEIN TRANSPORT; RNA POLYMERASE II; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84988447968     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.195867     Document Type: Article

References (67)

1. Baarlink, C., Wang, H. and Grosse, R. (2013). Nuclear actin network assembly by formins regulates the SRF coactivator MAL. Science 340, 864-867.
2. Belin, B. J., Cimini, B. A., Blackburn, E. H. and Mullins, R. D. (2013). Visualization of actin filaments and monomers in somatic cell nuclei. Mol. Biol. Cell 24, 982-994.
3. Belin, B. J., Lee, T. Mullins, R. D. (2015). DNA damage induces nuclear actin filament assembly by formin-2 and Spire-1/2 that promotes efficient DNA repair. eLife 4, e07735.
4. Berland, K. M., So, P. T. and Gratton, E. (1995). Two-photon fluorescence correlation spectroscopy: method and application to the intracellular environment. Biophys. J. 68, 694-701.
5. Bregman, D. B., Du, L., van der Zee, S. and Warren, S. L. (1995). Transcriptiondependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129, 287-298.
6. Brotschi, E. A., Hartwig, J. H. and Stossel, T. P. (1978). The gelation of actin by actin-binding protein. J. Biol. Chem. 253, 8988-8993.
7. Chang, L., Godinez, W. J., Kim, I.-H., Tektonidis, M., de Lanerolle, P., Eils, R., Rohr, K. and Knipe, D. M. (2011). PNAS Plus: Herpesviral replication compartments move and coalesce at nuclear speckles to enhance export of viral late mRNA. Proc. Natl. Acad. Sci. USA 108, E136-E144.
8. Chen, Y., Wei, L.-N. and Müller, J. D. (2003). Probing protein oligomerization in living cells with fluorescence fluctuation spectroscopy. Proc. Natl. Acad. Sci. USA 100, 15492-15497.
9. Cisterna, B., Necchi, D., Prosperi, E. and Biggiogera, M. (2006). Small ribosomal subunits associate with nuclear myosin and actin in transit to the nuclear pores. FASEB J. 20, 1901-1903.
10. Courtemanche, N., Pollard, T. D. and Chen, Q. (2016). Avoiding artefacts when counting polymerized actin in live cells with LifeAct fused to fluorescent proteins. Nat. Cell Biol. 18, 676-683.
11. Darzacq, X., Shav-Tal, Y., de Turris, V., Brody, Y., Shenoy, S. M., Phair, R. D. and Singer, R. H. (2007). In vivo dynamics of RNA polymerase II transcription. Nat. Struct. Mol. Biol. 14, 796-806.
12. Daugherty, R. L., Serebryannyy, L., Yemelyanov, A., Flozak, A. S., Yu, H.-J., Kosak, S. T., deLanerolle, P. and Gottardi, C. J. (2014). alpha-Catenin is an inhibitor of transcription. Proc. Natl. Acad. Sci. USA 111, 5260-5265.
13. de Lanerolle, P. (2012). Nuclear actin and myosins at a glance. J. Cell Sci. 125, 4945-4949.
14. de Lanerolle, P. and Serebryannyy, L. (2011). Nuclear actin and myosins: life without filaments. Nat. Cell Biol. 13, 1282-1288
15. Digman, M. A., Dalal, R., Horwitz, A. F. and Gratton, E. (2008). Mapping the number of molecules and brightness in the laser scanning microscope. Biophys. J. 94, 2320-2332.
16. Domazetovska, A., Ilkovski, B., Cooper, S. T., Ghoddusi, M., Hardeman, E. C., Minamide, L. S., Gunning, P. W., Bamburg, J. R. and North, K. N. (2007a). Mechanisms underlying intranuclear rod formation. Brain 130, 3275-3284.
17. Domazetovska, A., Ilkovski, B., Kumar, V., Valova, V. A., Vandebrouck, A., Hutchinson, D. O., Robinson, P. J., Cooper, S. T., Sparrow, J. C., Peckham, M. et al. (2007b). Intranuclear rod myopathy: molecular pathogenesis and mechanisms of weakness. Ann. Neurol. 62, 597-608.
18. Dopie, J., Skarp, K.-P., Rajakyla, E. K., Tanhuanpaa, K. and Vartiainen, M. K. (2012). Active maintenance of nuclear actin by importin 9 supports transcription. Proc. Natl. Acad. Sci. USA 109, E544-E552.
19. Dopie, J., Rajakyla, E. K., Joensuu, M. S., Huet, G., Ferrantelli, E., Xie, T., Jaalinoja, H., Jokitalo, E. and Vartiainen, M. K. (2015). Genome-wide RNAi screen for nuclear actin reveals a network of cofilin regulators. J. Cell Sci. 128, 2388-2400.
20. Du, J., Fan, Y. L., Chen, T. L. and Feng, X. Q. (2015). Lifeact and Utr230 induce distinct actin assemblies in cell nuclei. Cytoskeleton (Hoboken) 72, 570-575.
21. Egly, J. M., Miyamoto, N. G., Moncollin, V. and Chambon, P. (1984). Is actin a transcription initiation factor for RNA polymerase B? EMBO J. 3, 2363-2371.
22. Fang, Z. and Luna, E. J. (2013). Supervillin-mediated suppression of p53 protein enhances cell survival. J. Biol. Chem. 288, 7918-7929.
23. Feric, M. and Brangwynne, C. P. (2013). A nuclear F-actin scaffold stabilizes ribonucleoprotein droplets against gravity in large cells. Nat. Cell Biol. 15, 1253-1259.
24. Fuchsova, B., Serebryannyy, L. A. and de Lanerolle, P. (2015). Nuclear actin and myosins in adenovirus infection. Exp. Cell Res. 338, 170-182.
25. Gettemans, J., Van Impe, K., Delanote, V., Hubert, T., Vandekerckhove, J. and De Corte, V. (2005). Nuclear actin-binding proteins as modulators of gene transcription. Traffic 6, 847-857.
26. Goley, E. D., Ohkawa, T., Mancuso, J., Woodruff, J. B., D'Alessio, J. A., Cande, W. Z., Volkman, L. E. andWelch, M. D. (2006). Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WASP-like protein. Science 314, 464-467.
27. Gonsior, S. M., Platz, S., Buchmeier, S., Scheer, U., Jockusch, B. M. and Hinssen, H. (1999). Conformational difference between nuclear and cytoplasmic actin as detected by a monoclonal antibody. J. Cell Sci. 112, 797-809.
28. Goodson, H. V. and Hawse, W. F. (2002). Molecular evolution of the actin family. J. Cell Sci. 115, 2619-2622.
29. Grosse, R. and Vartiainen, M. K. (2013). To be or not to be assembled: progressing into nuclear actin filaments. Nat. Rev. Mol. Cell Biol. 14, 693-697.
30. Halavatyi, A. A., Nazarov, P. V., Medves, S., van Troys, M., Ampe, C., Yatskou, M. and Friederich, E. (2009). An integrative simulation model linking major biochemical reactions of actin-polymerization to structural properties of actin filaments. Biophys. Chem. 140, 24-34.
31. Ho, C. Y., Jaalouk, D. E., Vartiainen, M. K. and Lammerding, J. (2013). Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature 497, 507-511.
32. 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.
33. Hofmann, W. A., Vargas, G. M., Ramchandran, R., Stojiljkovic, L., Goodrich, J. A. and de Lanerolle, P. (2006). Nuclear myosin I is necessary for the formation of the first phosphodiester bond during transcription initiation by RNA polymerase II. J. Cell Biochem. 99, 1001-1009.
34. Hofmann, W. A., Richards, T. A. and de Lanerolle, P. (2009). Ancient animal ancestry for nuclear myosin. J. Cell Sci. 122, 636-643.
35. Hu, P., Wu, S. and Hernandez, N. (2004). A role for beta-actin in RNA polymerase III transcription. Genes Dev. 18, 3010-3015.
36. Johnson, M. A., Sharma, M., Mok, M. T. S. and Henderson, B. R. (2013). Stimulation of in vivo nuclear transport dynamics of actin and its co-factors IQGAP1 and Rac1 in response to DNA replication stress. Biochim. Biophys. Acta 1833, 2334-2347.
37. Kapoor, P. and Shen, X. (2014). Mechanisms of nuclear actin in chromatinremodeling complexes. Trends Cell Biol. 24, 238-246.
38. Kokai, E., Beck, H., Weissbach, J., Arnold, F., Sinske, D., Sebert, U., Gaiselmann, G., Schmidt, V., Walther, P., Münch, J. et al. (2014). Analysis of nuclear actin by overexpression of wild-type and actin mutant proteins. Histochem. Cell Biol. 141, 123-135.
39. Kudryashov, D. S., Durer, Z. A. O., Ytterberg, A. J., Sawaya, M. R., Pashkov, I., Prochazkova, K., Yeates, T. O., Loo, R. R. O., Loo, J. A., Satchell, K. J. F. et al. (2008). Connecting actin monomers by iso-peptide bond is a toxicity mechanism of the Vibrio cholerae MARTX toxin. Proc. Natl. Acad. Sci. USA 105, 18537-18542.
40. Lin, S., Coutinho-Mansfield, G., Wang, D., Pandit, S. and Fu, X. D. (2008). The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol. 15, 819-826.
41. Lundquist, M. R., Storaska, A. J., Liu, T.-C., Larsen, S. D., Evans, T., Neubig, R. R. and Jaffrey, S. R. (2014). Redox modification of nuclear actin by MICAL-2 regulates SRF signaling. Cell 156, 563-576.
42. McDonald, D., Carrero, G., Andrin, C., de Vries, G. and Hendzel, M. J. (2006). Nucleoplasmic beta-actin exists in a dynamic equilibrium between low-mobility polymeric species and rapidly diffusing populations. J. Cell Biol. 172, 541-552.
43. Miyamoto, K., Pasque, V., Jullien, J. and Gurdon, J. B. (2011). Nuclear actin polymerization is required for transcriptional reprogramming of Oct4 by oocytes. Genes Dev. 25, 946-958.
44. Munsie, L., Caron, N., Atwal, R. S., Marsden, I., Wild, E. J., Bamburg, J. R., Tabrizi, S. J. and Truant, R. (2011). Mutant huntingtin causes defective actin remodeling during stress: defining a new role for transglutaminase 2 in neurodegenerative disease. Hum. Mol. Genet. 20, 1937-1951.
45. Nishida, E., Iida, K., Yonezawa, N., Koyasu, S., Yahara, I. and Sakai, H. (1987). Cofilin is a component of intranuclear and cytoplasmic actin rods induced in cultured cells. Proc. Natl. Acad. Sci. USA 84, 5262-5266.
46. Obrdlik, A. and Percipalle, P. (2011). The F-actin severing protein cofilin-1 is required for RNA polymerase II transcription elongation. Nucleus 2, 72-79.
47. Philimonenko, V. V., Zhao, J., Iben, S., Dingová, H., Kyselá, K., Kahle, M., Zentgraf, H., Hofmann,W. A., de Lanerolle, P., Hozak, P. et al. (2004). Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat. Cell Biol. 6, 1165-1172.
48. Plessner, M. and Grosse, R. (2015). Extracellular signaling cues for nuclear actin polymerization. Eur. J. Cell Biol. 94, 359-362.
49. Plessner, M., Melak, M., Chinchilla, P., Baarlink, C. and Grosse, R. (2015). Nuclear F-actin formation and reorganization upon cell spreading. J. Biol. Chem. 290, 11209-11216.
50. Pollard, T. D. and Cooper, J. A. (2009). Actin, a central player in cell shape and movement. Science 326, 1208-1212.
51. Posern, G., Sotiropoulos, A. and Treisman, R. (2002). Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol. Biol. Cell 13, 4167-4178.
52. Rungger, D., Rungger-Brändle, E., Chaponnier, C. and Gabbiani, G. (1979). Intranuclear injection of anti-actin antibodies into Xenopus oocytes blocks chromosome condensation. Nature 282, 320-321.
53. Sacco-Bubulya, P. and Spector, D. L. (2002). Disassembly of interchromatin granule clusters alters the coordination of transcription and pre-mRNA splicing. J. Cell Biol. 156, 425-436.
54. Scheer, U., Hinssen, H., Franke,W.W. and Jockusch, B. M. (1984). Microinjection of actin-binding proteins and actin antibodies demonstrates involvement of nuclear actin in transcription of lampbrush chromosomes. Cell 39, 111-122.
55. Sen, B., Xie, Z., Uzer, G., Thompson, W. R., Styner, M., Wu, X. and Rubin, J. (2015). Intranuclear actin regulates osteogenesis. Stem Cells 33, 3065-3076.
56. Serebryannyy, L. A., Cruz, C. M. and de Lanerolle, P. (2016). A role for nuclear actin in HDAC 1 and 2 regulation. Sci. Rep. 6, 28460
57. Spencer, V. A., Costes, S., Inman, J. L., Xu, R., Chen, J., Hendzel, M. J. and Bissell, M. J. (2011). Depletion of nuclear actin is a key mediator of quiescence in epithelial cells. J. Cell Sci. 124, 123-132.
58. Spracklen, A. J., Fagan, T. N., Lovander, K. E. and Tootle, T. L. (2014). The pros and cons of common actin labeling tools for visualizing actin dynamics during Drosophila oogenesis. Dev. Biol. 393, 209-226.
59. Stenzel, W., Preusse, C., Allenbach, Y., Pehl, D., Junckerstorff, R., Heppner, F. L., Nolte, K., Aronica, E., Kana, V., Rushing, E. et al. (2015). Nuclear actin aggregation is a hallmark of anti-synthetase syndrome-induced dysimmune myopathy. Neurology 84, 1346-1354.
60. Storti, B., Bizzarri, R., Cardarelli, F. and Beltram, F. (2012). Intact microtubules preserve transient receptor potential vanilloid 1 (TRPV1) functionality through receptor binding. J. Biol. Chem. 287, 7803-7811.
61. Sugaya, K., Vigneron, M. and Cook, P. R. (2000). Mammalian cell lines expressing functional RNA polymerase II tagged with the green fluorescent protein. J. Cell Sci. 113, 2679-2683.
62. Ting, H.-J., Yeh, S., Nishimura, K. and Chang, C. (2002). Supervillin associates with androgen receptor and modulates its transcriptional activity. Proc. Natl. Acad. Sci. USA 99, 661-666.
63. Vartiainen, M. K., Guettler, S., Larijani, B. and Treisman, R. (2007). Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316, 1749-1752.
64. Wang, I.-F., Chang, H.-Y. and James Shen, C.-K. (2006). Actin-based modeling of a transcriptionally competent nuclear substructure induced by transcription inhibition. Exp. Cell Res. 312, 3796-3807.
65. Wulfkuhle, J. D., Donina, I. E., Stark, N. H., Pope, R. K., Pestonjamasp, K. N., Niswonger, M. L. and Luna, E. J. (1999). Domain analysis of supervillin, an F-actin bundling plasma membrane protein with functional nuclear localization signals. J. Cell Sci. 112, 2125-2136.
66. Yahara, I., Harada, F., Sekita, S., Yoshihira, K. and Natori, S. (1982). Correlation between effects of 24 different cytochalasins on cellular structures and cellular events and those on actin in vitro. J. Cell Biol. 92, 69-78.
67. Ye, J., Zhao, J., Hoffmann-Rohrer, U. and Grummt, I. (2008). Nuclear myosin I acts in concert with polymeric actin to drive RNA polymerase I transcription. Genes Dev. 22, 322-330.