Cited by 137Genomics and Chromatin DynamicsChromatin Remodeling and CancerNuclear Structure and Function

Mechanisms of nuclear actin in chromatin-remodeling complexes

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Kapoor, Prabodh, Shen, Xuetong·2014·Trends in Cell Biology

Abstract

The mystery of nuclear actin has puzzled biologists for decades largely due to the lack of defined experimental systems. However, the development of actin-containing chromatin-modifying complexes as a defined genetic and biochemical system in the past decade has provided an unprecedented opportunity to dissect the mechanism of actin in the nucleus. Although the established functions of actin mostly rely on its dynamic polymerization, the novel finding of the mechanism of action of actin in the INO80 chromatin-remodeling complex suggests a conceptually distinct mode of actin that functions as a monomer. In this review we highlight the new paradigm and discuss how actin interaction with chromatin suggests a fundamental divergence between conventional cytoplasmic actin and nuclear actin. Furthermore, we provide how this framework could be applied to investigations of nuclear actin in other actin-containing chromatin-modifying complexes.

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  • Specific nuclear events and gene transcription are regulated by the availability of monomeric actin, since various nuclear proteins, such as chromatin remodeling complexes, histone modifiers and RNA polymerases, require monomeric actin for their activity.

    “Notably, specific nuclear events and gene transcription are regulated by the availability of monomeric actin, since various nuclear proteins, such as chromatin remodeling complexes88, histone modifiers89 and RNA polymerases90,91, require monomeric actin for their activity.”

    From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [88]

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  1. [1]Pollard TD Assembly and dynamics of the actin filament system in nonmuscle cells. J Cell Biochem 1986 31 87 95 3525579
  2. [2]Pollard TD Actin. Curr Opin Cell Biol 1990 2 33 40 2183841
  3. [3]Pollard TD Borisy GG Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003 112 453 465 12600310
  4. [4]Pollard TD Cooper JA Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu Rev Biochem 1986 55 987 1035 3527055
  5. [5]Bettinger BT Actin up in the nucleus. Nat Rev Mol Cell Biol 2004 5 410 415 15122354
  6. [6]Blessing CA Actin and ARPs: action in the nucleus. Trends Cell Biol 2004 14 435 442 15308210
  7. [7]Olave IA Nuclear actin and actin-related proteins in chromatin remodeling. Annu Rev Biochem 2002 71 755 781 12045110
  8. [8]Shumaker DK The nucleoskeleton: lamins and actin are major players in essential nuclear functions. Curr Opin Cell Biol 2003 15 358 366 12787780
  9. [9]Egly JM Is actin a transcription initiation factor for RNA polymerase B? EMBO J 1984 3 2363 2371 6499833 PMC557695
  10. [10]Galarneau L Multiple links between the NuA4 histone acetyltransferase complex and epigenetic control of transcription. Mol Cell 2000 5 927 937 10911987
  11. [11]Gonsior SM Conformational difference between nuclear and cytoplasmic actin as detected by a monoclonal antibody. J Cell Sci 1999 112 Pt 6 797 809 10036230
  12. [12]Ikura T Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000 102 463 473 10966108
  13. [13]Mizuguchi G ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 2004 303 343 348 14645854
  14. [14]Papoulas O The Drosophila trithorax group proteins BRM, ASH1 and ASH2 are subunits of distinct protein complexes. Development 1998 125 3955 3966 9735357
  15. [15]Shen X A chromatin remodelling complex involved in transcription and DNA processing. Nature 2000 406 541 544 10952318
  16. [16]Wada A Nuclear export of actin: a novel mechanism regulating the subcellular localization of a major cytoskeletal protein. EMBO J 1998 17 1635 1641 9501085 PMC1170511
  17. [17]Zhao K Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 1998 95 625 636 9845365
  18. [18]Pendleton A Latrunculin B or ATP depletion induces cofilin-dependent translocation of actin into nuclei of mast cells. J Biol Chem 2003 278 14394 14400 12566455
  19. [19]Abe H Cytoplasmic localization and nuclear transport of cofilin in cultured myotubes. Exp Cell Res 1993 206 1 10 8482351
  20. [20]Fornerod M CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997 90 1051 1060 9323133
  21. [21]Stuven T Exportin 6: a novel nuclear export receptor that is specific for profilin.actin complexes. EMBO J 2003 22 5928 5940 14592989 PMC275422
  22. [22]Hofmann WA Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II. Nat Cell Biol 2004 6 1094 1101 15502823
  23. [23]Hu P A role for beta-actin in RNA polymerase III transcription. Genes Dev 2004 18 3010 3015 15574586 PMC535912
  24. [24]Miralles F Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 2003 113 329 342 12732141
  25. [25]Percipalle P An actin-ribonucleoprotein interaction is involved in transcription by RNA polymerase II. Proc Natl Acad Sci U S A 2003 100 6475 6480 12743363 PMC164471
  26. [26]Percipalle P Actin-associated hnRNP proteins as transacting factors in the control of mRNA transport and localization. RNA Biol 2009 6 171 174 19276667
  27. [27]Philimonenko VV Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat Cell Biol 2004 6 1165 1172 15558034
  28. [28]Clark TG Merriam RW Diffusible and bound actin nuclei of Xenopus laevis oocytes. Cell 1977 12 883 891 563771
  29. [29]Schoenenberger CA Conformation-specific antibodies reveal distinct actin structures in the nucleus and the cytoplasm. J Struct Biol 2005 152 157 168 16297639
  30. [30]Kapoor P Evidence for monomeric actin function in INO80 chromatin remodeling. Nat Struct Mol Biol 2013 PMC3618487 23524535
  31. [31]Scheer U Microinjection of actin-binding proteins and actin antibodies demonstrates involvement of nuclear actin in transcription of lampbrush chromosomes. Cell 1984 39 111 122 6386181
  32. [32]Nowak G Evidence for the presence of myosin I in the nucleus. J Biol Chem 1997 272 17176 17181 9202039
  33. [33]Pestic-Dragovich L A myosin I isoform in the nucleus. Science 2000 290 337 341 11030652
  34. [34]Baarlink C Nuclear actin network assembly by formins regulates the SRF coactivator MAL. Science 2013 340 864 867 23558171
  35. [35]Pollard TD Cooper JA Actin, a central player in cell shape and movement. Science 2009 326 1208 1212 19965462 PMC3677050
  36. [36]Falbo KB Involvement of a chromatin remodeling complex in damage tolerance during DNA replication. Nat Struct Mol Biol 2009 16 1167 1172 19855395 PMC2974178
  37. [37]Morrison AJ INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 2004 119 767 775 15607974
  38. [38]Morrison AJ Mec1/Tel1 phosphorylation of the INO80 chromatin remodeling complex influences DNA damage checkpoint responses. Cell 2007 130 499 511 17693258
  39. [39]Tsukuda T Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 2005 438 379 383 16292314 PMC1388271
  40. [40]Tsukuda T INO80-dependent chromatin remodeling regulates early and late stages of mitotic homologous recombination. DNA Repair (Amst) 2009 8 360 369 19095087
  41. [41]Shen X Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol Cell 2003 12 147 155 12887900
  42. [42]Novick P Botstein D Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell 1985 40 405 416 3967297
  43. [43]Udugama M The INO80 ATP-dependent chromatin remodeling complex is a nucleosome spacing factor. Mol Cell Biol 2011 31 662 673 21135121 PMC3028646
  44. [44]Gerhold CB Structure of Actin-related protein 8 and its contribution to nucleosome binding. Nucleic Acids Res 2012 40 11036 11046 22977180 PMC3510490
  45. [45]Szerlong H The HSA domain binds nuclear actin-related proteins to regulate chromatin-remodeling ATPases. Nat Struct Mol Biol 2008 15 469 476 18408732 PMC2810487
  46. [46]Rando OJ Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc Natl Acad Sci U S A 2002 99 2824 2829 11880634 PMC122432
  47. [47]Schafer DA Schroer TA Actin-related proteins. Annu Rev Cell Dev Biol 1999 15 341 363 10611965
  48. [48]Fenn S Structural biochemistry of nuclear actin-related proteins 4 and 8 reveals their interaction with actin. EMBO J 2011 30 2153 2166 21499228 PMC3117639
  49. [49]Tosi A Structure and Subunit Topology of the INO80 Chromatin Remodeler and Its Nucleosome Complex. Cell 2013 154 1207 1219 24034245
  50. [50]Goley ED Welch MD The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 2006 7 713 726 16990851
  51. [51]Harata M The nuclear actin-related protein of Saccharomyces cerevisiae, Act3p/Arp4, interacts with core histones. Mol Biol Cell 1999 10 2595 2605 10436015 PMC25491
  52. [52]Kudryashov DS Reisler E ATP and ADP actin states. Biopolymers 2013 99 245 256 23348672 PMC3670783
  53. [53]Reisler E Actin molecular structure and function. Curr Opin Cell Biol 1993 5 41 47 8448029
  54. [54]Belmont LD A change in actin conformation associated with filament instability after Pi release. Proc Natl Acad Sci U S A 1999 96 29 34 9874766 PMC15087
  55. [55]Otterbein LR The crystal structure of uncomplexed actin in the ADP state. Science 2001 293 708 711 11474115
  56. [56]Moraczewska J Divalent cation-, nucleotide-, and polymerization-dependent changes in the conformation of subdomain 2 of actin. Biophys J 1999 77 373 385 10388764 PMC1300336
  57. [57]Graceffa P Dominguez R Crystal structure of monomeric actin in the ATP state. Structural basis of nucleotide-dependent actin dynamics. J Biol Chem 2003 278 34172 34180 12813032
  58. [58]Zheng X Nucleotide effects on the structure and dynamics of actin. Biophys J 2007 93 1277 1283 17526584 PMC1929039
  59. [59]Pfaendtner J Nucleotide-dependent conformational states of actin. Proc Natl Acad Sci U S A 2009 106 12723 12728 19620726 PMC2722336
  60. [60]Rould MA Crystal structures of expressed non-polymerizable monomeric actin in the ADP and ATP states. J Biol Chem 2006 281 31909 31919 16920713
  61. [61]Sunada R The nuclear actin-related protein Act3p/Arp4p is involved in the dynamics of chromatin-modulating complexes. Yeast 2005 22 753 768 16088870
  62. [62]Wu WH N terminus of Swr1 binds to histone H2AZ and provides a platform for subunit assembly in the chromatin remodeling complex. J Biol Chem 2009 284 6200 6207 19088068 PMC2649089
  63. [63]Almer A Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J 1986 5 2689 2696 3536481 PMC1167170
  64. [64]Li B Reese JC Ssn6-Tup1 regulates RNR3 by positioning nucleosomes and affecting the chromatin structure at the upstream repression sequence. J Biol Chem 2001 276 33788 33797 11448965
  65. [65]Lohr D Nucleosome transactions on the promoters of the yeast GAL and PHO genes. J Biol Chem 1997 272 26795 26798 9341105
  66. [66]Perez-Ortin JE Fine analysis of the chromatin structure of the yeast SUC2 gene and of its changes upon derepression. Comparison between the chromosomal and plasmid-inserted genes. Nucleic Acids Res 1987 15 6937 6956 2821486 PMC306185
  67. [67]Ravindra A High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating-type locus HMRa. Mol Cell Biol 1999 19 7944 7950 10567520 PMC84879
  68. [68]Venters BJ Pugh BF How eukaryotic genes are transcribed. Crit Rev Biochem Mol Biol 2009 44 117 141 19514890 PMC2718758
  69. [69]Cairns BR Chromatin remodeling: insights and intrigue from single-molecule studies. Nat Struct Mol Biol 2007 14 989 996 17984961 PMC2788559
  70. [70]Saha A Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 2006 7 437 447 16723979
  71. [71]Whitehouse I Chromatin remodelling at promoters suppresses antisense transcription. Nature 2007 450 1031 1035 18075583
  72. [72]Georgieva M The nuclear actin-related protein Act3p/Arp4 influences yeast cell shape and bulk chromatin organization. J Cell Biochem 2008 104 59 67 18004728
  73. [73]Gorzer I The nuclear actin-related protein Act3p/Arp4p of Saccharomyces cerevisiae is involved in transcription regulation of stress genes. Mol Microbiol 2003 50 1155 1171 14622406
  74. [74]Jiang YW Stillman DJ Epigenetic effects on yeast transcription caused by mutations in an actin-related protein present in the nucleus. Genes Dev 1996 10 604 619 8598290
  75. [75]Ogiwara H Role of Elg1 protein in double strand break repair. Nucleic Acids Res 2007 35 353 362 17170004 PMC1802592
  76. [76]Breitkreutz BJ The GRID: The General Repository for Interaction Datasets. Genome Biol 2002 3 PREPRINT0013 12537553
  77. [77]Breitkreutz BJ Osprey: a network visualization system. Genome Biol 2002 3 PREPRINT0012 12537552
  78. [78]Collins SR Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 2007 446 806 810 17314980
  79. [79]Haarer B Modeling complex genetic interactions in a simple eukaryotic genome: actin displays a rich spectrum of complex haploinsufficiencies. Genes Dev 2007 21 148 159 17167106 PMC1770898
  80. [80]Krogan NJ A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 2003 12 1565 1576 14690608
  81. [81]Lin YY A comprehensive synthetic genetic interaction network governing yeast histone acetylation and deacetylation. Genes Dev 2008 22 2062 2074 18676811 PMC2492751
  82. [82]Jin J A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex. J Biol Chem 2005 280 41207 41212 16230350
  83. [83]Ebbert R The product of the SNF2/SWI2 paralogue INO80 of Saccharomyces cerevisiae required for efficient expression of various yeast structural genes is part of a high-molecular-weight protein complex. Mol Microbiol 1999 32 741 751 10361278
  84. [84]Kobor MS A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2004 2 E131 15045029 PMC374244
  85. [85]Wu WH Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat Struct Mol Biol 2005 12 1064 1071 16299513
  86. [86]Doyon Y Cote J The highly conserved and multifunctional NuA4 HAT complex. Curr Opin Genet Dev 2004 14 147 154 15196461
  87. [87]Sterner DE Berger SL Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev 2000 64 435 459 10839822 PMC98999
  88. [88]Roth SY Histone acetyltransferases. Annu Rev Biochem 2001 70 81 120 11395403
  89. [89]Carrozza MJ The diverse functions of histone acetyltransferase complexes. Trends Genet 2003 19 321 329 12801725
  90. [90]Le Masson I Yaf9, a novel NuA4 histone acetyltransferase subunit, is required for the cellular response to spindle stress in yeast. Mol Cell Biol 2003 23 6086 6102 12917332 PMC180919
  91. [91]Utley RT Cote J The MYST family of histone acetyltransferases. Curr Top Microbiol Immunol 2003 274 203 236 12596909
  92. [92]Cai Y The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J Biol Chem 2005 280 13665 13670 15647280
  93. [93]Allard S NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J 1999 18 5108 5119 10487762 PMC1171581
  94. [94]Bird AW Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 2002 419 411 415 12353039
  95. [95]Percipalle P The chromatin remodelling complex WSTF-SNF2h interacts with nuclear myosin 1 and has a role in RNA polymerase I transcription. EMBO Rep 2006 7 525 530 16514417 PMC1479564
  96. [96]Percipalle P Visa N Molecular functions of nuclear actin in transcription. J Cell Biol 2006 172 967 971 16549500 PMC2063754
  97. [97]Favot L Cytoplasmic YY1 is associated with increased smooth muscle-specific gene expression: implications for neonatal pulmonary hypertension. Am J Pathol 2005 167 1497 1509 16314465 PMC1613200
  98. [98]Haller K Subcellular localization of multiple PREP2 isoforms is regulated by actin, tubulin, and nuclear export. J Biol Chem 2004 279 49384 49394 15339927
  99. [99]Posern G Mutant actins that stabilise F-actin use distinct mechanisms to activate the SRF coactivator MAL. EMBO J 2004 23 3973 3983 15385960 PMC524340
  100. [100]Martens JH Scaffold/matrix attachment region elements interact with a p300-scaffold attachment factor A complex and are bound by acetylated nucleosomes. Mol Cell Biol 2002 22 2598 2606 11909954 PMC133732
  101. [101]Percipalle P Nuclear actin is associated with a specific subset of hnRNP A/B-type proteins. Nucleic Acids Res 2002 30 1725 1734 11937625 PMC113215
  102. [102]Percipalle P Actin bound to the heterogeneous nuclear ribonucleoprotein hrp36 is associated with Balbiani ring mRNA from the gene to polysomes. J Cell Biol 2001 153 229 236 11285288 PMC2185526
  103. [103]Sjolinder M The growing pre-mRNA recruits actin and chromatin-modifying factors to transcriptionally active genes. Genes Dev 2005 19 1871 1884 16103215 PMC1186187
  104. [104]Boyer LA Peterson CL Actin-related proteins (Arps): conformational switches for chromatin-remodeling machines? Bioessays 2000 22 666 672 10878579

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Authors
Kapoor, P., & Shen, X.
Affiliations
The University of Texas MD Anderson Cancer Center (US)
Corresponding author
Shen, Xuetong
Venue
Trends in Cell Biology
Publisher
Elsevier BV
Published
2014-04
Volume
24
Issue
4
Pages
238-246
ISSN
0962-8924 (ISSN-L)
OpenAlex
W2170720737
Cited by
137
References
0
Citations by year
2026: 5 · 2025: 7 · 2024: 14 · 2023: 11 · 2022: 6 · 2021: 14 · 2020: 14 · 2019: 15 · 2018: 12 · 2017: 11 · 2016: 13 · 2015: 12 · 2014: 2
FWCI
0.85
Type
journal article
Language
en
Open access
Locations
  • Trends in Cell Biology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Cancer Institute (K22CA100017, P30CA016672)
  • National Institute of General Medical Sciences (R01GM093104)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
Keywords
nuclear actin, chromatin remodeling complexes, INO80 complex, actin polymerization, actin monomer, chromatin remodeling, cytoplasmic actin
MeSH terms
Actins, Animals, Cell Nucleus, Chromatin, Histones, Humans, Models, Biological, Chromatin Assembly and Disassembly

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