Advertisement

Histochemistry and Cell Biology

, Volume 150, Issue 3, pp 235–244 | Cite as

Nuclear actin: ancient clue to evolution in eukaryotes?

  • Csaba Bajusz
  • Péter Borkúti
  • Ildikó Kristó
  • Zoltán Kovács
  • Csilla Abonyi
  • Péter Vilmos
Review

Abstract

Until recently it was widely accepted that the dynamic cytoskeletal matrix is exclusive to the cytoplasm of eukaryotes, evolving before the emergence of the cell nucleus to enable phagocytosis, cell motility and the sophisticated functioning of the endomembrane system within the cytosol. The discovery of the existence of a prokaryotic cytoskeleton has changed this picture significantly. As a result, the idea has taken shape that the appearance of actin occurred in the very first cell; therefore, the emergence of microfilaments precedes that of the eukaryotic cytoskeleton. The discovery of nuclear actin opened new perspective on the field, suggesting that the nuclear activities of actin reflect the functions of primordial actin-like proteins. In this paper, we review the recent literature to explore the evolutionary origin of nuclear actin. We conclude that both ancient and eukaryotic features of the actin world can be detected in the nucleus today, which supports the idea that the cytoskeleton attained significant eukaryotic innovations before the tandem evolution of the cytoskeleton and nucleus occurred.

Keywords

Actin Evolution Cytoskeleton Nucleus 

Abbreviations

NPC

Nuclear pore complex

ERM

Ezrin–radixin–moesin

LINC

Linker of nucleoskeleton and cytoskeleton

NLS

Nuclear localization signal

SRF

Serum response factor

ARP

Actin-related protein

MKL1

Megakaryoblastic leukemia protein 1

INM

Inner nuclear membrane protein

Notes

Acknowledgements

The authors acknowledge Miklós Erdélyi, József Mihály and Gabriel Fenteany (BRC Szeged) for the critical reading of the manuscript.

Funding

This work was supported by the National Research, Development and Innovation Office—NKFIH (GINOP-2.3.2-15-2016-00001, GINOP-2.3.2-15-2016-00032 and PD127968).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Baarlink C, Wang H, Grosse R (2013) Nuclear actin network assembly by formins regulates the SRF coactivator MAL. Science 340(6134):864–867.  https://doi.org/10.1126/science.1235038 PubMedCrossRefGoogle Scholar
  2. Baarlink C, Plessner M, Sherrard A, Morita K, Misu S, Virant D, Kleinschnitz EM, Harniman R, Alibhai D, Baumeister S, Miyamoto K, Endesfelder U, Kaidi A, Grosse R (2017) A transient pool of nuclear F-actin at mitotic exit controls chromatin organization. Nat Cell Biol 19(12):1389–1399.  https://doi.org/10.1038/ncb3641 PubMedCrossRefGoogle Scholar
  3. Bamburg JR, Bernstein BW, Davis RC, Flynn KC, Goldsbury C, Jensen JR, Maloney MT, Marsden IT, Minamide LS, Pak CW, Shaw AE, Whiteman I, Wiggan O (2010) ADF/cofilin actin rods in neurodegenerative diseases. Curr Alzheimer Res 7(3):241–250PubMedPubMedCentralCrossRefGoogle Scholar
  4. Barry RM, Gitai Z (2011) Self-assembling enzymes and the origins of the cytoskeleton. Curr Opin Microbiol 14:704–711PubMedPubMedCentralCrossRefGoogle Scholar
  5. Baum DA, Baum B (2014) An inside-out origin for the eukaryotic cell. BMC Biol 12:76.  https://doi.org/10.1186/s12915-014-0076-2 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Belin BJ, Cimini BA, Blackburn EH, Mullins RD (2013) Visualization of actin filaments and monomers in somatic cell nuclei. Mol Biol Cell 24:982–994PubMedPubMedCentralCrossRefGoogle Scholar
  7. Belin BJ, Lee T, Mullins RD (2015) DNA damage induces nuclear actin filament assembly by formin-2 and Spire-1/2 that promotes efficient DNA repair. Elife 4:e07735PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bork P, Sander C, Valencia A (1992) An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc Natl Acad Sci USA 89:7290–7294PubMedCrossRefGoogle Scholar
  9. Burdyniuk M, Callegari A, Mori M, Nédélec F, Lénárt P (2018) F-Actin nucleated on chromosomes coordinates their capture by microtubules in oocyte meiosis. J Cell Biol.  https://doi.org/10.1083/jcb.201802080 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Carlier MF (1990) Actin polymerization and ATP hydrolysis. Adv Biophys 26:51–73PubMedCrossRefGoogle Scholar
  11. Carlier MF, Pantaloni D, Evans JA, Lambooy PK, Korn ED, Webb MR (1988) The hydrolysis of ATP that accompanies actin polymerization is essentially irreversible. FEBS Lett 235(1–2):211–214PubMedCrossRefGoogle Scholar
  12. Castagnetti S, Oliferenko S, Nurse P (2010) Fission yeast cells undergo nuclear division in the absence of spindle microtubules. PLoS Biol 8(10):e1000512PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chan PC, Hsu RYC, Liu CW, Lai CC, Chen HC (2014) Adducin-1 is essential for mitotic spindle assembly through its interaction with myosin-X. J Cell Biol 204:19–28PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chuang C-H, Carpenter AE, Fuchsova B, Johnson T, de Lanerolle P, Belmont AS (2006) Long-range directional movement of an interphase chromosome site. Curr Biol 16:825–831PubMedCrossRefGoogle Scholar
  15. Clark TG, Merriam RW (1977) Diffusable and bound actin in nuclei of X. laevis oocytes. Cell 12:883–891PubMedCrossRefGoogle Scholar
  16. Collier S, Chan HY, Toda T, McKimmie C, Johnson G, Adler PN, O’Kane C, Ashburner M (2000) The Drosophila embargoed gene is required for larval progression and encodes the functional homolog of schizosaccharomyces Crm1. Genetics 155(4):1799–1807PubMedPubMedCentralGoogle Scholar
  17. de Lanerolle P, Serebryannyy L (2011) Nuclear actin and myosins: life without filaments. Nat Cell Biol 13(11):1282–1288.  https://doi.org/10.1038/ncb2364 PubMedCrossRefGoogle Scholar
  18. Derman AI, Nonejuie P, Michel BC, Truong BD, Fujioka A, Erb ML, Pogliano J (2012) Alp7R regulates expression of the actin-like protein Alp7A in Bacillus subtilis. J Bacteriol 194:2715–2724PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dopie J, Skarp KP, Rajakylä EK, Tanhuanpää K, Vartiainen MK (2012) Active maintenance of nuclear actin by importin 9 supports transcription. Proc Natl Acad Sci USA 109(9):E544–E552.  https://doi.org/10.1073/pnas.1118880109 PubMedCrossRefGoogle Scholar
  20. Dopie J, Rajakylä EK, Joensuu MS, Huet G, Ferrantelli E, Xie T, Jäälinoja H, Jokitalo E, Vartiainen MK (2015) Genome-wide RNAi screen for nuclear actin reveals a network of cofilin regulators. J Cell Sci 128(13):2388–2400.  https://doi.org/10.1242/jcs.169441 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Dundr M, Ospina JK, Sung M-H, John S, Upender M, Ried T, Hager GL, Matera AG (2007) Actin-dependent intranuclear repositioning of an active gene locus in vivo. J Cell Biol 179:1095–1103PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dunn K, Chrysogelos S, Griffith J (1982) Electron microscopic visualization of RecA-DNA filaments: evidence for cyclic extension of duplex DNA. Cell 28:757–765PubMedCrossRefGoogle Scholar
  23. Erickson HP (2007) Evolution of the cytoskeleton. Bioessays 29(7):668–677PubMedPubMedCentralCrossRefGoogle Scholar
  24. Falahzadeh K, Banaei-Esfahani A, Shahhoseini M (2015) The potential roles of actin in the nucleus. Cell J 17(1):7–14PubMedPubMedCentralGoogle Scholar
  25. Farrants AK (2008) Chromatin remodelling and actin organisation. FEBS Lett 582(14):2041–2050.  https://doi.org/10.1016/j.febslet.2008.04.032 PubMedCrossRefGoogle Scholar
  26. Fenn S, Breitsprecher D, Gerhold CB, Witte G, Faix J, Hopfner KP (2011) Structural biochemistry of nuclear actin-related proteins 4 and 8 reveals their interaction with actin. EMBO J 30(11):2153–2166.  https://doi.org/10.1038/emboj.2011.118 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Feric M, Brangwynne CP (2013) A nuclear F-actin scaffold stabilizes ribonucleoprotein droplets against gravity in large cells. Nat Cell Biol 15(10):1253–1259.  https://doi.org/10.1038/ncb2830 PubMedPubMedCentralCrossRefGoogle Scholar
  28. Feric M, Broedersz CP, Brangwynne CP (2015) Soft viscoelastic properties of nuclear actin age oocytes due to gravitational creep. Sci Rep 5:16607.  https://doi.org/10.1038/srep16607 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fomproix N, Percipalle P (2004) An actin-myosin complex on actively transcribing genes. Exp Cell Res 294(1):140–148PubMedCrossRefGoogle Scholar
  30. Forer A, Jackson WT (1979) Actin in spindles of Haemanthus katherinae endosperm. I. General results using various glycerination methods. J Cell Sci 37:323–347PubMedGoogle Scholar
  31. Forer A, Pickett-Heaps JD, Spurck T (2008) What generates flux of tubulin in kinetochore microtubules? Protoplasma 232(3–4):137–141.  https://doi.org/10.1007/s00709-008-0286-y PubMedCrossRefGoogle Scholar
  32. Fujita J, Maeda Y, Nagao C, Tsuchiya Y, Miyazaki Y, Hirose M, Mizohata E, Matsumoto Y, Inoue T, Mizuguchi K, Matsumura H (2014) Crystal structure of FtsA from Staphylococcus aureus. FEBS Lett 588(10):1879–1885.  https://doi.org/10.1016/j.febslet.2014.04.008 PubMedCrossRefGoogle Scholar
  33. Gawadi N (1971) Actin in the mitotic spindle. Nature 234(5329):410PubMedCrossRefGoogle Scholar
  34. Ghosal D, Löwe J (2015) Collaborative protein filaments. EMBO J 34(18):2312–2320.  https://doi.org/10.15252/embj.201591756 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Gunning PW, Ghoshdastider U, Whitaker S, Popp D, Robinson RC (2015) The evolution of compositionally and functionally distinct actin filaments. J Cell Sci 128:2009–2019PubMedCrossRefGoogle Scholar
  36. Hofmann WA, Stojiljkovic L, Fuchsova B, Vargas GM, Mavrommatis E, Philimonenko V, Kysela K, Goodrich JA, Lessard JL, Hope TJ, Hozak P, de Lanerolle P (2004) Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II. Nat Cell Biol 6:1094–1101PubMedCrossRefGoogle Scholar
  37. Hofmann WA, Vargas GM, Ramchandran R, Stojiljkovic L, Goodrich JA, 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(4):1001–1009PubMedCrossRefGoogle Scholar
  38. Hu P, Wu S, Hernandez N (2004) A role for beta-actin in RNA polymerase III transcription. Genes Dev 18:3010–3015PubMedPubMedCentralCrossRefGoogle Scholar
  39. Hurley JH (1996) The sugar kinase/heat shock protein 70/actin superfamily: implications of conserved structure for mechanism. Annu Rev Biophys Biomol Struct 25:137–162PubMedCrossRefGoogle Scholar
  40. Jékely G (2014) Origin and evolution of the self-organizing cytoskeleton in the network of eukaryotic organelles. Cold Spring Harb Perspect Biol 6(9):a016030.  https://doi.org/10.1101/cshperspect.a016030 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Jiang S, Narita A, Popp D, Ghoshdastider U, Lee LJ, Srinivasan R, Balasubramanian MK, Oda T, Koh F, Larsson M, Robinson RC (2016) Novel actin filaments from Bacillus thuringiensis form nanotubules for plasmid DNA segregation. Proc Natl Acad Sci USA 113(9):E1200–E1205.  https://doi.org/10.1073/pnas.1600129113 PubMedCrossRefGoogle Scholar
  42. Johansen KM, Forer A, Yao C, Girton J, Johansen J (2011) Do nuclear envelope and intranuclear proteins reorganize during mitosis to form an elastic, hydrogel-like spindle matrix? Chromosome Res 19:345–365PubMedCrossRefGoogle Scholar
  43. Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC (1990) Atomic structure of the actin:DNase I complex. Nature 347(6288):37–44PubMedCrossRefGoogle Scholar
  44. Kandasamy MK, McKinney EC, Meagher RB (2010) Differential sublocalization of actin variants within the nucleus. Cytoskeleton (Hoboken) 67(11):729–743.  https://doi.org/10.1002/cm.20484 CrossRefGoogle Scholar
  45. Kapoor P, Shen X (2014) Mechanisms of nuclear actin in chromatin-remodeling complexes. Trends Cell Biol 24(4):238–246.  https://doi.org/10.1016/j.tcb.2013.10.007 PubMedCrossRefGoogle Scholar
  46. Kimura T, Hashimoto I, Yamamoto A, Nishikawa M, Fujisawa JI (2000) Rev-dependent association of the intro-containing HIV-1 gag mRNA with the nuclear actin bundles and the inhibition of its nucleocytoplasmic transport by latrunculin-B. Genes Cells 5:289–307PubMedCrossRefGoogle Scholar
  47. Kollmar M, Lbik D, Enge S (2012) Evolution of the eukaryotic ARP2/3 activators of the WASP family: WASP, WAVE, WASH, and WHAMM, and the proposed new family members WAWH and WAML. BMC Res Notes 5:88.  https://doi.org/10.1186/1756-0500-5-88 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Korn ED, Carlier MF, Pantaloni D (1987) Actin polymerization and ATP hydrolysis. Science 238(4827):638–644PubMedCrossRefGoogle Scholar
  49. Kristó I, Bajusz I, Bajusz C, Borkúti P, Vilmos P (2016) Actin, actin-binding proteins, and actin-related proteins in the nucleus. Histochem Cell Biol 145(4):373–388.  https://doi.org/10.1007/s00418-015-1400-9 PubMedCrossRefGoogle Scholar
  50. Kukalev A, Nord Y, Palmberg C, Bergman T, Percipalle P (2005) Actin and hnRNP U cooperate for productive transcription by RNA polymerase II. Nat Struct Mol Biol 12(3):238–244PubMedCrossRefGoogle Scholar
  51. Kumeta M, Yoshimura SH, Hejna J, Takeyasu K (2012) Nucleocytoplasmic shuttling of cytoskeletal proteins: molecular mechanism and biological significance. Int J Cell Biol 2012:494902.  https://doi.org/10.1155/2012/494902 PubMedCrossRefGoogle Scholar
  52. Le HQ, Ghatak S, Yeung C-YC, Tellkamp F, Günschmann C, Dieterich C, Yeroslaviz A, Habermann B, Pombo A, Niessen CM, Wickström SA (2016) Mechanical regulation of transcription controls polycomb-mediated gene silencing during lineage commitment. Nat Cell Biol 18:864–875PubMedCrossRefGoogle Scholar
  53. Lo YS, Cheng N, Hsiao LJ, Annamalai A, Jauh GY, Wen TN, Dai H, Chiang KS (2011) Actin in mung bean mitochondria and implications for its function. Plant Cell 23(10):3727–3744.  https://doi.org/10.1105/tpc.111.087403 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lundquist MR, Storaska AJ, Liu TC, Larsen SD, Evans T, Neubig RR, Jaffrey SR (2014) Redox modification of nuclear actin by MICAL-2 regulates SRF signaling. Cell 156(3):563–576.  https://doi.org/10.1016/j.cell.2013.12.035 PubMedPubMedCentralCrossRefGoogle Scholar
  55. Maciver SK, Hussey PJ (2002) The ADF/cofilin family: actin-remodeling proteins. Genome Biol 3(5):reviews3007PubMedPubMedCentralCrossRefGoogle Scholar
  56. Maupin P, Pollard TD (1986) Arrangement of actin filaments and myosin-like filaments in the contractile ring and of actin-like filaments in the mitotic spindle of dividing HeLa cells. J Ultrastruct Mol Struct Res 94:92–103PubMedCrossRefGoogle Scholar
  57. Miyamoto K, Pasque V, Jullien J, Gurdon JB (2011) Nuclear actin polymerization is required for transcriptional reprogramming of Oct4 by oocytes. Genes Dev 25(9):946–958.  https://doi.org/10.1101/gad.615211 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Møller-Jensen J, Jensen RB, Löwe J, Gerdes K (2002) Prokaryotic DNA segregation by an actin-like filament. EMBO J 21(12):3119–3127PubMedPubMedCentralCrossRefGoogle Scholar
  59. Møller-Jensen J, Borch J, Dam M, Jensen RB, Roepstorff P, Gerdes K (2003) Bacterial mitosis: ParM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. Mol Cell 12:1477–1487PubMedCrossRefGoogle Scholar
  60. Muller J, Oma Y, Vallar L, Friederich E, Poch O, Winsor B (2005) Sequence and comparative genomic analysis of actin-related proteins. Mol Biol Cell 16(12):5736–5748PubMedPubMedCentralCrossRefGoogle Scholar
  61. Neumann N, Lundin D, Poole AM (2010) Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS One 5(10):e13241.  https://doi.org/10.1371/journal.pone.0013241 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Nevzorov I, Sidorenko E, Wang W, Zhao H, Vartiainen MK (2018) Myosin-1C uses a novel phosphoinositide-dependent pathway for nuclear localization. EMBO Rep 19(2):290–304.  https://doi.org/10.15252/embr.201744296 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Obrdlik A, Percipalle P (2014) The F-actin severing protein cofilin-1 is required for RNA polymerase II transcription elongation. Nucleus 2:72–79CrossRefGoogle Scholar
  64. Obrdlik A, Kukalev A, Louvet E, Farrants A-KO, Caputo L, Percipalle P (2008) The histone acetyltransferase PCAF associates with actin and hnRNP U for RNA polymerase II transcription. Mol Cell Biol 28:6342–6357PubMedPubMedCentralCrossRefGoogle Scholar
  65. Olave IA, Reck-Peterson SL, Crabtree GR (2002) Nuclear actin and actin-related proteins in chromatin remodeling. Annu Rev Biochem 71:755–781PubMedCrossRefGoogle Scholar
  66. Parisis N, Krasinska L, Harker B, Urbach S, Rossignol M, Camasses A, Dewar J, Morin N, Fisher D (2017) Initiation of DNA replication requires actin dynamics and formin activity. EMBO J 36(21):3212–3231.  https://doi.org/10.15252/embj.201796585 PubMedCrossRefGoogle Scholar
  67. Pederson T, Aebi U (2003) Actin in the nucleus: what form and what for? J Struct Biol 140:3–9CrossRefGoogle Scholar
  68. Percipalle P (2013) Co-transcriptional nuclear actin dynamics. Nucleus 4(1):43–52.  https://doi.org/10.4161/nucl.22798 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Percipalle P, Zhao J, Pope B, Weeds A, Lindberg U, Daneholt B (2001) Actin bound to the heterogeneous nuclear ribonucleo-protein hrp36 is associated with Balbiani ring mRNA from the gene to polysomes. J Cell Biol 153:229–235PubMedPubMedCentralCrossRefGoogle Scholar
  70. Percipalle P, Fomproix N, Kylberg K, Miralles F, Bjorkroth B, Daneholt B, Visa N (2003) An actin-ribonucleoprotein interaction is involved in transcription by RNA polymerase II. Proc Natl Acad Sci USA 100(11):6475–6480PubMedCrossRefGoogle Scholar
  71. Philimonenko VV, Zhao J, Iben S, Dingova H, Kysela K, Kahle M, Zentgraf H, Hofmann WA, de Lanerolle P, Hozak P, Grummt I (2004) Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat Cell Biol 6:1165–1172PubMedCrossRefGoogle Scholar
  72. Plessner M, Melak M, Chinchilla P, Baarlink C, Grosse R (2015) Nuclear F-actin formation and reorganization upon cell spreading. J Biol Chem 290(18):11209–11216.  https://doi.org/10.1074/jbc.M114.627166 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Polka JK, Kollman JM, Agard DA, Mullins RD (2009) The structure and assembly dynamics of plasmid actin AlfA imply a novel mechanism of DNA segregation. J Bacteriol 191(20):6219–6230.  https://doi.org/10.1128/JB.00676-09 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Qi T, Tang W, Wang L, Zhai L, Guo L, Zeng X (2011) G-actin participates in RNA polymerase II-dependent transcription elongation by recruiting positive transcription elongation factor b (P-TEFb). J Biol Chem 286:15171–15181PubMedPubMedCentralCrossRefGoogle Scholar
  75. Reyes A, He J, Mao CC, Bailey LJ, Di Re M, Sembongi H, Kazak L, Dzionek K, Holmes JB, Cluett TJ, Harbour ME, Fearnley IM, Crouch RJ, Conti MA, Adelstein RS, Walker JE, Holt IJ (2011) Actin and myosin contribute to mammalian mitochondrial DNA maintenance. Nucleic Acids Res 39(12):5098–5108.  https://doi.org/10.1093/nar/gkr052 PubMedPubMedCentralCrossRefGoogle Scholar
  76. Rose AS, Hildebrand PW (2015) NGL viewer: a web application for molecular visualization. Nucleic Acids Res 43(Web Server issue):W576–W579.  https://doi.org/10.1093/nar/gkv402 CrossRefGoogle Scholar
  77. Sandquist JC, Kita AM, Bement WM (2011) And the dead shall rise: actin and myosin return to the spindle. Dev Cell 21(3):410–419PubMedPubMedCentralCrossRefGoogle Scholar
  78. Sanger JW, Sanger JM, Kreis TE, Jockusch BM (1980) Reversible translocation of cytoplasmic actin into the nucleus caused by dimethyl sulfoxide. Proc Natl Acad Sci USA 77(9):5268–5272PubMedCrossRefGoogle Scholar
  79. Schleicher M, Jockusch BM (2008) Actin: its cumbersome pilgrimage through cellular compartments. Histochem Cell Biol 129(6):695–704.  https://doi.org/10.1007/s00418-008-0430-y PubMedPubMedCentralCrossRefGoogle Scholar
  80. Schmid VJ, Cremer M, Cremer T (2017) Quantitative analyses of the 3D nuclear landscape recorded with super-resolved fluorescence microscopy. Methods 123:33–46.  https://doi.org/10.1016/j.ymeth.2017.03.013 PubMedCrossRefGoogle Scholar
  81. Schoenenberger CA, Buchmeier S, Boerries M, Sütterlin R, Aebi U, Jockusch BM (2005) Conformation-specific antibodies reveal distinct actin structures in the nucleus and the cytoplasm. J Struct Biol 152(3):157–168PubMedCrossRefGoogle Scholar
  82. Schuh M, Ellenberg JJ (2008) A new model for asymmetric spindle positioning in mouse oocytes. Curr Biol 18:1986–1992PubMedCrossRefGoogle Scholar
  83. Schweizer N, Weiss M, Maiato H (2014) The dynamic spindle matrix. Curr Opin Cell Biol 28:1–7.  https://doi.org/10.1016/j.ceb.2014.01.002 PubMedCrossRefGoogle Scholar
  84. Sebé-Pedrós A, Grau-Bové X, Richards TA, Ruiz-Trillo I (2014) Evolution and classification of myosins, a paneukaryotic whole-genome approach. Genome Biol Evol 6(2):290–305.  https://doi.org/10.1093/gbe/evu013 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Serebryannyy LA, Parilla M, Annibale P, Cruz CM, Laster K, Gratton E, Kudryashov D, Kosak ST, Gottardi CJ, de Lanerolle P (2016a) Persistent nuclear actin filaments inhibit transcription by RNA polymerase II. J Cell Sci 129(18):3412–3425.  https://doi.org/10.1242/jcs.195867 PubMedPubMedCentralCrossRefGoogle Scholar
  86. Serebryannyy LA, Cruz CM, de Lanerolle P (2016b) A role for nuclear actin in HDAC 1 and 2 regulation. Sci Rep 6:28460.  https://doi.org/10.1038/srep28460 PubMedPubMedCentralCrossRefGoogle Scholar
  87. Siebrasse JP, Veith R, Dobay A, Leonhardt H, Daneholt B, Kubitscheck U (2008) Discontinuous movement of mRNP particles in nucleoplasmic regions devoid of chromatin. Proc Natl Acad Sci USA 105(51):20291–20296.  https://doi.org/10.1073/pnas.0810692105 PubMedCrossRefGoogle Scholar
  88. Singh AP, Galland R, Finch-Edmondson ML, Grenci G, Sibarita JB, Studer V, Viasnoff V, Saunders TE (2017) 3D protein dynamics in the cell nucleus. Biophys J 112(1):133–142.  https://doi.org/10.1016/j.bpj.2016.11.3196 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Sriram M, Osipiuk J, Freeman B, Morimoto R, Joachimiak A (1997) Human Hsp70 molecular chaperone binds two calcium ions within the ATPase domain. Structure 5(3):403–414PubMedCrossRefGoogle Scholar
  90. Stoddard PR, Williams TA, Garner E, Baum B (2017) Evolution of polymer formation within the actin superfamily. Mol Biol Cell 28(19):2461–2469.  https://doi.org/10.1091/mbc.E15-11-0778 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Straub FB (1942) Actin. Stud Inst Med Chem Univ Szeged 2:3–15. http://actin.aok.pte.hu/archives/pdf/StudiesII_1.pdf. Accessed 28 Feb 2018
  92. Szwedziak P, Wang Q, Freund SM, Löwe J (2012) FtsA forms actin-like protofilaments. EMBO J 31:2249–2260PubMedPubMedCentralCrossRefGoogle Scholar
  93. Ungricht R, Klann M, Horvath P, Kutay U (2015) Diffusion and retention are major determinants of protein targeting to the inner nuclear membrane. J Cell Biol 209(5):687–703.  https://doi.org/10.1083/jcb.201409127 PubMedPubMedCentralCrossRefGoogle Scholar
  94. van den Ent F, Amos LA, Löwe J (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413(6851):39–44PubMedCrossRefGoogle Scholar
  95. Viita T, Vartiainen MK (2017) From cytoskeleton to gene expression: actin in the nucleus. Handb Exp Pharmacol 235:311–329.  https://doi.org/10.1007/164_2016_27 PubMedCrossRefGoogle Scholar
  96. Vilmos P, Jankovics F, Szathmári M, Lukácsovich T, Henn L, Erdélyi M (2009) Live imaging reveals that the Drosophila actin-binding ERM protein, moesin, co-localizes with the mitotic spindle. Eur J Cell Biol 88(10):609–619.  https://doi.org/10.1016/j.ejcb.2009.05.006 PubMedCrossRefGoogle Scholar
  97. Vilmos P, Kristó I, Szikora SZ, Jankovics F, Lukácsovich T, Kari B, Erdélyi M (2016) The actin-binding ERM protein moesin directly regulates spindle assembly and function during mitosis. Cell Biol Int 40(6):696–707.  https://doi.org/10.1002/cbin.10607 PubMedCrossRefGoogle Scholar
  98. Virtanen JA, Vartiainen MK (2017) Diverse functions for different forms of nuclear actin. Curr Opin Cell Biol 46:33–38.  https://doi.org/10.1016/j.ceb.2016.12.004 PubMedCrossRefGoogle Scholar
  99. Visa N, Percipalle P (2010) Nuclear functions of actin. Cold Spring Harb Perspect Biol 2(4):a000620.  https://doi.org/10.1101/cshperspect.a000620 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Wang H, Robinson RC, Burtnick LD (2010) The structure of native G-actin. Cytoskeleton (Hoboken) 67(7):456–465.  https://doi.org/10.1002/cm.20458 CrossRefGoogle Scholar
  101. Wickstead B, Gull K (2011) The evolution of the cytoskeleton. J Cell Biol 194(4):513–525.  https://doi.org/10.1083/jcb.201102065 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Wilson KL, Holaska JM, Montes de Oca R, Tifft K, Zastrow M, Segura-Totten M, Mansharamani M, Bengtsson L (2005) Nuclear membrane protein emerin: roles in gene regulation, actin dynamics and human disease. Novartis Found Symp 264:51–58 (discussion 58–62) PubMedGoogle Scholar
  103. Woolner S, Brien LL, Wiese C, Bement WB (2008) Myosin-10 and actin filaments are essential for mitotic spindle function. J Cell Biol 182(1):77–88PubMedPubMedCentralCrossRefGoogle Scholar
  104. Wu X, Kocher B, Wei Q, Hammer JA III (1998) Myosin Va associates with microtubule-rich domains in both interphase and dividing cells. Cell Motil Cytoskeleton 40:286–303PubMedCrossRefGoogle Scholar
  105. Wu X, Yoo Y, Okuhama NN, Tucker PW, Liu G, Guan J-L (2006) Regulation of RNA-polymerase-II-dependent transcription by N-WASP and its nuclear-binding partners. Nat Cell Biol 8:756–763PubMedCrossRefGoogle Scholar
  106. Xie X, Percipalle P (2017) An actin-based nucleoskeleton involved in gene regulation and genome organization. Biochem Biophys Res Commun.  https://doi.org/10.1016/j.bbrc.2017.11.206 CrossRefPubMedGoogle Scholar
  107. Xie X, Almuzzaini B, Drou N, Kremb S, Yousif A, Farrants A, Gunsalus K, Percipalle P (2018a) β-Actin-dependent global chromatin organization and gene expression programs control cellular identity. FASEB J 32(3):1296–1314.  https://doi.org/10.1096/fj.201700753R PubMedCrossRefGoogle Scholar
  108. Xie X, Venit T, Drou N, Percipalle P (2018b) In mitochondria β-Actin regulates mtDNA transcription and is required for mitochondrial quality control. iScience 3:226–237CrossRefGoogle Scholar
  109. Yoo Y, Wu X, Guan J-L (2007) A novel role of the actin-nucleating Arp2/3 complex in the regulation of RNA polymerase II-dependent transcription. J Biol Chem 282:7616–7623PubMedCrossRefGoogle Scholar
  110. Yu M, Yuan M, Ren H (2006) Visualization of actin cytoskeletal dynamics during the cell cycle in tobacco (Nicotiana tabacum L. cv Bright Yellow) cells. Biol Cell 98:295–306PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Csaba Bajusz
    • 1
    • 2
  • Péter Borkúti
    • 1
    • 3
  • Ildikó Kristó
    • 1
  • Zoltán Kovács
    • 1
  • Csilla Abonyi
    • 1
  • Péter Vilmos
    • 1
  1. 1.Biological Research Centre of the Hungarian Academy of SciencesSzegedHungary
  2. 2.Doctoral School of BiologyUniversity of SzegedSzegedHungary
  3. 3.Doctoral School of Multidisciplinary Medical ScienceUniversity of SzegedSzegedHungary

Personalised recommendations