Nuclear molecular motors for active, directed chromatin movement in interphase nuclei

Advances in Nuclear Architecture

Volumn , Issue , 2011, Pages 149-172

  Bridger, Joanna M ^a   Mehta, Ishita S ^a,b  

^a BRUNEL UNIVERSITY   (United Kingdom)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

Actin; Actin related proteins; Arp6; Arps; Cajal body; Chromosome territories; Emerin; F actin; G actin; Gene re positioning; Lamin A; Mlp1; Molecular motors; MYO1C; Myosin; Myosin 1; Nuclear motors; Nuclear myosin 1 ; actin

Indexed keywords

EID: 81855201109     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-90-481-9899-3_5     Document Type: Chapter

References (122)

1. Pollard TD, Eisenberg E, Korn ED, Kielley WW (1973) Inhibition of Mg ++ ATPase activity of actin-activated Acanthamoeba myosin by muscle troponin-tropomyosin: implications for the mechanism of control of amoeba motility and muscle contraction. Biochem Biophys Res Commun 51:693-698
2. Pollard TD, Korn ED (1973) Acanthamoeba myosin. II. Interaction with actin and with a new cofactor protein required for actin activation of Mg 2+ adenosine triphosphatase activity. J Biol Chem 248:4691-4697
3. Berg JS, Powell BC, Cheney RE (2001) A millennial myosin census. Mol Biol Cell 12:780-794
4. Bahler M (2000) Are class III and class IX myosins motorized signalling molecules? Biochim Biophys Acta 1496:52-59
5. Yin H, Pruyne D, Huffaker TC, Bretscher A (2000) Myosin V orientates the mitotic spindle in yeast. Nature 406:1013-1015
6. Evangelista M, Klebl BM, Tong AH, Webb BA, Leeuw T et al (2000) A role for myosin-I in actin assembly through interactions with Vrplp, Beelp, and the Arp2/3 complex. J Cell Biol 148:353-362
7. Lechler T, Shevchenko A, Li R (2000) Direct involvement of yeast type I myosins in Cdc42-dependent actin polymerization. J Cell Biol 148:363-373
8. Lee WL, Bezanilla M, Pollard TD (2000) Fission yeast myosin-I, Myolp, stimulates actin assembly by Arp2/3 complex and shares functions with WASp. J Cell Biol 151:789-800
9. Sellers JR (2000) Myosins: a diverse superfamily. Biochim Biophys Acta 1496:3-22
10. Mermall V, Post PL, Mooseker MS (1998) Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279:527-533
11. McDonald D, Carrero G, Andrin C, de Vries G, Hendzel MJ (2006) Nucleoplasmic beta-actin exists in a dynamic equilibrium between low-mobility polymeric species and rapidly diffusing populations. J Cell Biol 172:541-552
12. de Lanerolle P, Johnson T, Hofmann WA (2005) Actin and myosin I in the nucleus: what next? Nat Struct Mol Biol 12:742-746
13. Hofmann WA, Johnson T, Klapczynski M, Fan JL, de Lanerolle P (2006a) From transcription to transport: emerging roles for nuclear myosin I. Biochem Cell Biol 84:418-426
14. Castano E, Philimonenko VV, Kahle M, Fukalova J, Kalendova A et al (2010) Actin complexes in the cell nucleus: new stones in an old field. Histochem Cell Biol 133:607-626
15. Dion V, Shimada K, Gasser SM (2010) Actin-related proteins in the nucleus: life beyond chromatin remodelers. Curr Opin Cell Biol
16. Branco MR, Pombo A (2006) Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol 4: el38
17. Osborne CS, Chakalova L, Mitchell JA, Horton A, Wood AL et al (2007) Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol 5: el92
18. Dundr M, Ospina JK, Sung MH, John S, Upender M et al (2007) Actin-dependent intranuclear repositioning of an active gene locus in vivo. J Cell Biol 179:1095-1103
19. Chuang CH, Carpenter AE, Fuchsova B, Johnson T, de Lanerolle P et al (2006) Long-range directional movement of an interphase chromosome site. Curr Biol 16:825-831
20. Mehta IS (2005) Genome organisation in senescent cells. Master's dissertation
21. Mehta IS, Elcock LS, Amira M, Kill IR, Bridger JM (2008) Nuclear motors and nuclear structures containing A-type lamins and emerin: is there a functional link? Biochem Soc Trans 36:1384-1388
22. Hu Q, Kwon YS, Nunez E, Cardamone MD, Hutt KR et al (2008) Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD 1-dependent gene networking in interchromatin granules. Proc Natl Acad Sci U S A 105:19199-19204
23. Mehta IS, Amira M, Harvey AJ, Bridger JM (2010) Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Genome Biolll: R5
24. Lane NJ (1969) Intranuclear fibrillar bodies in actinomycin D-treated oocytes. J Cell Biol 40:286-291
25. Clark TG, Rosenbaum JL (1979) An actin filament matrix in hand-isolated nuclei of X. laevis oocytes. Cell 18:1101-1108
26. Nakayasu H, Ueda K (1983) Association of actin with the nuclear matrix from bovine lymphocytes. Exp Cell Res 143:55-62
27. Jockusch BM, Becker M, Hindennach I, Jockusch E (1974) Slime mould actin: homology to vertebrate actin and presence in the nucleus. Exp Cell Res 89:241-246
28. Clark TG, Merriam RW (1977) Diffusible and bound actin nuclei of Xenopus laevis oocytes. Cell 12:883-891
29. Egly JM, Miyamoto NG, Moncollin V, Chambon P (1984) Is actin a transcription initiation factor for RNA polymerase B? Embo J 3:2363-2371
30. Rungger D, Rungger-Brandle E, Chaponnier C, Gabbiani G (1979) Intranuclear injection of anti-actin antibodies into Xenopus oocytes blocks chromosome condensation. Nature 282:320-321
31. Scheer U, Hinssen H, Franke WW, Jockusch BM (1984) Microinjection of actin-binding proteins and actin antibodies demonstrates involvement of nuclear actin in transcription of lampbrush chromosomes. Cell 39:111-122
32. Ankenbauer T, Kleinschmidt JA, Walsh MJ, Weiner OH, Franke WW (1989) Identification of a widespread nuclear actin binding protein. Nature 342:822-825
33. Zhao K, Wang W, Rando OJ, Xue Y, Swiderek K et al (1998) Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95:625-636
34. Gonsior SM, Platz S, Buchmeier S, Scheer U, Jockusch BM et al (1999) Conformational difference between nuclear and cytoplasmic actin as detected by a monoclonal antibody. J Cell Sci 112(Pt6):797-809
35. Schoenenberger CA, Buchmeier S, Boerries M, Sutterlin R, Aebi U et al (2005) Conformationspecific antibodies reveal distinct actin structures in the nucleus and the cytoplasm. J Struct Biol 152:157-168
36. Wang IF, Chang HY, Shen CK (2006) Actin-based modeling of a transcriptionally competent nuclear substructure induced by transcription inhibition. Exp Cell Res 312:3796-3807
37. Cruz JR, Diaz M, de la Espina S (2009) Subnuclear compartmentalization and function of actin and nuclear myosin I in plants. Chromosoma 118:193-207
38. Hofmann W, Reichart B, Ewald A, Muller E, Schmitt I et al (2001) Cofactor requirements for nuclear export of Rev response element (RRE) - and constitutive transport element (CTE) - containing retroviral RNAs. An unexpected role for actin. J Cell Biol 152:895-910
39. Kiseleva E, Drummond SP, Goldberg MW, Rutherford SA, Allen TD et al (2004) Actin- and protein-4.1-containing filaments link nuclear pore complexes to subnuclear organelles in Xenopus oocyte nuclei. J Cell Sci 117:2481-2490
40. Bohnsack MT, Stuven T, Kuhn C, Cordes VC, Gorlich D (2006) A selective block of nuclear actin export stabilizes the giant nuclei of Xenopus oocytes. Nat Cell Biol 8:257-263
41. Jockusch BM, Schoenenberger CA, Stetefeld J, Aebi U (2006) Tracking down the different forms of nuclear actin. Trends Cell Biol 16:391-396
42. Egelman EH (2003) A tale of two polymers: new insights into helical filaments. Nat Rev Mol Cell Biol 4:621-630
43. Gedge LJ, Morrison EE, Blair GE, Walker JH (2005) Nuclear actin is partially associated with Cajal bodies in human cells in culture and relocates to the nuclear periphery after infection of cells by adenovirus 5. Exp Cell Res 303:229-239
44. Muratani M, Gerlich D, Janicki SM, Gebhard M, Eils R et al (2002) Metabolic-energy-dependent movement of PML bodies within the mammalian cell nucleus. Nat Cell Biol 4:106-110
45. Olave IA, Reek-Peterson SL, Crabtree GR (2002) Nuclear actin and actin-related proteins in chromatin remodeling. Annu Rev Biochem 71:755-781
46. Pederson T (2000) Half a century of "the nuclear matrix". Mol Biol Cell 11:799-805
47. Zhang S, Buder K, Burkhardt C, Schlott B, Gorlach M et al (2002) Nuclear DNA helicase II/RNA helicase A binds to filamentous actin. J Biol Chem 277:843-853
48. Hofmann WA, Stojiljkovic L, Fuchsova B, Vargas GM, Mavrommatis E 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
49. Philimonenko VV, Zhao J, Iben S, Dingova H, Kysela K et al (2004) Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat Cell Biol 6:1165-1172
50. Hu P, Wu S, Hernandez N (2004) A role for beta-actin in RNA polymerase III transcription. Genes Dev 18:3010-3015
51. 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 12:238-244
52. Percipalle P, Jonsson A, Nashchekin D, Karlsson C, Bergman T et al (2002) Nuclear actin is associated with a specific subset of hnRNP A/B-type proteins. Nucleic Acids Res 30:1725-1734
53. Percipalle P, Zhao J, Pope B, Weeds A, Lindberg U et al (2001) Actin bound to the heterogeneous nuclear ribonucleoprotein hrp36 is associated with Balbiani ring mRNA from the gene to polysomes. J Cell Biol 153:229-236
54. Kimura T, Hashimoto I, Yamamoto A, Nishikawa M, Fujisawa JI (2000) Rev-dependent association of the intron-containing HIV-1 gag mRNA with the nuclear actin bundles and the inhibition of its nucleocytoplasmic transport by latrunculin-B. Genes Cells 5:289-307
55. Lee K, Song K (2007) Actin dysfunction activates ERK1/2 and delays entry into mitosis in mammalian cells. Cell Cycle 6:1487-1495
56. Andrin C, Hendzel MJ (2004) F-actin-dependent insolubility of chromatin-modifying components. J Biol Chem 279:25017-25023
57. Gieni RS, Hendzel MJ (2008) Mechanotransduction from the ECM to the genome: are the pieces now in place? J CeU Biochem 104:1964-1987
58. Gieni RS, Hendzel MJ (2009) Actin dynamics and functions in the interphase nucleus: moving toward an understanding of nuclear polymeric actin. Biochem Cell Biol 87:283-306
59. Holaska JM, Kowalski AK, Wilson KL (2004) Emerin caps the pointed end of actin filaments: evidence for an actin cortical network at the nuclear inner membrane. PLoS Biol 2:E231
60. Holaska JM, Wilson KL (2007) An emerin "proteome": purification of distinct emerin-containing complexes from HeLa cells suggests molecular basis for diverse roles including gene regulation, mRNA splicing, signaling, mechanosensing, and nuclear architecture. Biochemistry 46:8897-8908
61. Lee K, Kang MJ, Kwon SJ, Kwon YK, Kim KW et al (2007) Expansion of chromosome territories with chromatin decompaction in BAF53-depleted interphase cells. Mol Biol Cell 18:4013-4023
62. Sasseville AM, Langelier Y (1998) In vitro interaction of the carboxy-terminal domain of lamin A with actin. FEBS Lett 425:485-489
63. Dingova H, Fukalova J, Maninova M, Philimonenko VV, Hozak P (2009) Ultrastructural localization of actin and actin-binding proteins in the nucleus. Histochem Cell Biol 131:425-434
64. Hagen SJ, Kiehart DP, Kaiser DA, Pollard TD (1986) Characterization of monoclonal antibodies to Acanthamoeba myosin-I that cross-react with both myosin-II and low molecular mass nuclear proteins. J Cell Biol 103:2121-2128
65. Berrios M, Fisher PA, Matz EC (1991) Localization of a myosin heavy chain-like polypeptide to Drosophila nuclear pore complexes. Proc Natl Acad Sci USA 88:219-223
66. Pederson T, Aebi U (2002) Actin in the nucleus: what form and what for? J Struct Biol 140:3-9
67. Nowak G, Pestic-Dragovich L, Hozak P, Philimonenko A, Simerly C et al (1997) Evidence for the presence of myosin I in the nucleus. J Biol Chem 272:17176-17181
68. Pestic-Dragovich L, Stojiljkovic L, Philimonenko AA, Nowak G, Ke Y et al (2000) A myosin I isoform in the nucleus. Science 290:337-341
69. Kahle M, Pridalova J, Spacek M, Dzijak R, Hozak P (2007) Nuclear myosin is ubiquitously expressed and evolutionary conserved in vertebrates. Histochem Cell Biol 127:139-148
70. Vreugde S, Ferrai C, Miluzio A, Hauben E, Marchisio PC et al (2006) Nuclear myosin VI enhances RNA polymerase Il-dependent transcription. Mol Cell 23:749-755
71. Jung EJ, Liu G, Zhou W, Chen X (2006) Myosin VI is a mediator of the p53-dependent cell survival pathway. Mol Cell Biol 26:2175-2186
72. Cameron RS, Liu C, Mixon AS, Pihkala JP, Rahn RJ et al (2007) Myosinl6b: The COOH-tail region directs localization to the nucleus and overexpression delays S-phase progression. Cell Motil Cytoskeleton 64:19-48
73. Pranchevicius MC, Baqui MM, Ishikawa-Ankerhold HC, Lourenco EV, Leao RM et al (2008) Myosin Va phosphorylated on Serl650 is found in nuclear speckles and redistributes to nucleoli upon inhibition of transcription. Cell Motil Cytoskeleton 65:441-456
74. Lindsay AJ, McCaffrey MW (2009a) Myosin Vb localises to nucleoli and associates with the RNA polymerase I transcription complex. Cell Motil Cytoskeleton 66:1057-1072
75. Hofmann WA, Richards TA, de Lanerolle P (2009) Ancient animal ancestry for nuclear myosin. J Cell Sci 122:636-643
76. Roberts R, Lister I, Schmitz S, Walker M, Veigel C et al (2004) Myosin VI: cellular functions and motor properties. Philos Trans R Soc Lond B Biol Sci 359:1931-1944
77. Gillespie PG, Albanesi JP, Bahler M, Bement WM, Berg JS et al (2001) Myosin-I nomenclature. J Cell Biol 155:703-704
78. Hofmann WA, Vargas GM, Ramchandran R, Stojiljkovic L, Goodrich JA et al (2006b) 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
79. Lindsay AJ, McCaffrey MW (2009) Myosin Vb localises to nucleoli and associates with the RNA polymerase I transcription complex. Cell Motil Cytoskeleton
80. Fomproix N, Percipalle P (2004) An actin-myosin complex on actively transcribing genes. Exp Cell Res 294:140-148
81. Grummt I (2003) Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17:1691-1702
82. Cavellan E, Asp P, Percipalle P, Farrants AK (2006) The WSTF-SNF2h chromatin remodeling complex interacts with several nuclear proteins in transcription. J Biol Chem 281:16264-16271
83. Percipalle P, Farrants AK (2006) Chromatin remodelling and transcription: be-WICHed by nuclear myosin 1. Curr Opin Cell Biol 18:267-274
84. Percipalle P, Fomproix N, Cavellan E, Voit R, Reimer G et al (2006) The chromatin remodelling complex WSTF-SNF2h interacts with nuclear myosin 1 and has a role in RNA polymerase I transcription. EMBO Rep 7:525-530
85. Kysela K, Philimonenko AA, Philimonenko VV, Janacek J, Kahle M et al (2005) Nuclear distribution of actin and myosin I depends on transcriptional activity of the cell. Histochem Cell Biol 124:347-358
86. Obrdlik A, Louvet E, Naschekin D, Kiseleva E, Fahrenkrog B et al (2010) Nuclear myosin 1 is in a complex with mature rRNA transcripts and associates with the nuclear pore basket. FASEB J 24:146-157
87. Zhang Q, Ragnauth CD, Skepper JN, Worth NF, Warren DT et al (2005) Nesprin-2 is a multiisomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle. J Cell Sci 118:673-687
88. Chubb JR, Boyle S, Perry P, Bickmore WA (2002) Chromatin motion is constrained by association with nuclear compartments in human cells. Curr Biol 12:439-445
89. Sullivan KF, Shelby RD (1999) Using time-lapse confocal microscopy for analysis of centromere dynamics in human cells. Methods Cell Biol 58:183-202
90. Weipoltshammer K, Schofer C, Almeder M, Philimonenko VV, Frei K et al (1999) Intranuclear anchoring of repetitive DNA sequences: centromeres, telomeres, and ribosomal DNA. J Cell Biol 147:1409-1418
91. Foster HA, Bridger JM (2005) The genome and the nucleus: a marriage made by evolution. Genome organisation and nuclear architecture. Chromosoma 114:212-229
92. Volpi EV, Chevret E, Jones T, Vatcheva R, Williamson J et al (2000) Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J Cell Sci 113(Pt 9):1565-1576
93. Bridger JM, Boyle S, Kill IR, Bickmore WA (2000) Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts. Curr Biol 10:149-152
94. Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher AG (1999) Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 3:207-217
95. Skalnikova M, Kozubek S, Lukasova E, Bartova E, Jirsova P et al (2000) Spatial arrangement of genes, centromeres and chromosomes in human blood cell nuclei and its changes during the cell cycle, differentiation and after irradiation. Chromosome Res 8:487-499
96. Belmont AS (2001) Visualizing chromosome dynamics with GFP. Trends Cell Biol 11:250-257
97. Tumbar T, Belmont AS (2001) Interphase movements of a DNA chromosome region modulated by VP16 transcriptional activator. Nat Cell Biol 3:134-139
98. Levi V, Ruan Q, Plutz M, Belmont AS, Gratton E (2005) Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys J 89:4275-4285
99. Chuang CH, Belmont AS (2007) Moving chromatin within the interphase nucleus-controlled transitions? Semin Cell Dev Biol 18:698-706
100. Rubtsov MA, Terekhov SM, Razin SV, Iarovaia OV (2008) Repositioning of ETO gene in cells treated with VP-16, an inhibitor of DNA-topoisomerase II. J Cell Biochem 104:692-699
101. Ondrej V, Lukasova E, Falk M, Kozubek S (2007) The role of actin and microtubule networks in plasmid DNA intracellular trafficking. Acta Biochim Pol 54:657-663
102. Ondrej V, Lukasova E, Krejci J, Matula P, Kozubek S (2008a) Lamin A/C and polymeric actin in genome organization. Mol Cells 26:356-361
103. Ondrej V, Lukasova E, Krejci J, Kozubek S (2008b) Intranuclear trafficking of plasmid DNA is mediated by nuclear polymeric proteins lamins and actin. Acta Biochim Pol 55:307-315
104. Barr ML, Bertram EG (1951) The behaviour of nuclear structures during depletion and restoration of Nissl material in motor neurons. J Anat 85:171-181
105. Borden J, Manuehdis L (1988) Movement of the X chromosome in epilepsy. Science 242:1687-1691
106. Croft JA, Bridger JM, Boyle S, Perry P, Teague P et al (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145:1119-1131
107. Meaburn KJ, Newbold RF, Bridger JM (2008) Positioning of human chromosomes in murine cell hybrids according to synteny. Chromosoma 117:579-591
108. Meaburn KJ, Cabuy E, Bonne G, Levy N, Morris GE et al (2007) Primary laminopathy fibroblasts display altered genome organization and apoptosis. Aging Cell 6:139-153
109. Mehta IS, Figgitt M, Clements CS, Kill IR, Bridger JM (2007) Alterations to nuclear architecture and genome behavior in senescent cells. Ann N Y Acad Sci 1100:250-263
110. Bridger JM Volpi (2010) Fluorescence in situ Hybridization (FISH), Molecular methods in molecular biology. Humana Press, USA
111. Wiegant JB, Raap AK; Tanke HJ, Dirks RW (2010) Visualizing nucleic acids in living cells by fluorescence in vivo hybridization. In: Bridger JM, Volpi EV (eds) Fluorescence in situ Hybridization (FISH), Methods in molecular biology. Humana Press, USA
112. Kocanova S, Kerr EA, Rafique S, Boyle S, Katz E et al (2010) Activation of estrogen-responsive genes does not require their nuclear co-localization. PLoS Genet 6: el000922
113. Brickner JH, Walter P (2004) Gene recruitment of the activated INOl locus to the nuclear membrane. PLoS Biol 2:e342
114. Casolari JM, Brown CR, Komili S, West J, Hieronymus H et al (2004) Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117:427-439
115. Taddei A, Van Houwe G, Hediger F, Kalck V, Cubizolles F et al (2006) Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441:774-778
116. Tan-Wong SM, Wijayatilake HD, Proudfoot NJ (2009) Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev 23:2610-2624
117. Laine JP, Singh BN, Krishnamurthy S, Hampsey M (2009) A physiological role for gene loops in yeast. Genes Dev 23:2604-2609
118. Yoshida T, Shimada K, Oma Y, Kalck V, Akimura K et al (2010) Actin-related protein Arp6 influences H2A. Z-dependent and -independent gene expression and links ribosomal protein genes to nuclear pores. PLoS Genet 6: el000910
119. Hofmann WA, de Lanerolle P (2006) Nuclear actin: to polymerize or not to polymerize. J Cell Biol 172:495-496
120. Chikashige Y, Haraguchi T, Hiraoka Y (2007) Another way to move chromosomes. Chromosoma 116:497-505
121. Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM et al (2006) SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 26:3738-3751
122. Starr DA (2009) A nuclear-envelope bridge positions nuclei and moves chromosomes. J Cell Sci 122:577-586