Microtubule dynamics alter the interphase nucleus

Cellular and Molecular Life Sciences

Volumn 70, Issue 7, 2013, Pages 1255-1268

  Gerlitz, Gabi ^a,b,c   Reiner, Orly ^b   Bustin, Michael ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c ARIEL UNIVERSITY   (Israel)

Author keywords

Chromatin; Dynein; Lamins; Microtubules; Nuclear envelope

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; CELL COMPOSITION; CELL NUCLEUS MEMBRANE; CELL TRANSFER; COMPLEX FORMATION; CONTROLLED STUDY; DEPOLYMERIZATION; HETEROCHROMATIN; INTERPHASE; INTRACELLULAR SIGNALING; MECHANOTRANSDUCTION; MICROTUBULE ASSEMBLY; MICROTUBULE ORGANIZING CENTER; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEAR LAMINA; POLYMERIZATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW;

ANIMALS; CELL NUCLEUS; CHROMATIN; INTERPHASE; KINETICS; MICE; MICROSCOPY, VIDEO; MICROTUBULE-ORGANIZING CENTER; MICROTUBULES; NOCODAZOLE; NUCLEAR ENVELOPE; PROTEIN MULTIMERIZATION; TUBULIN MODULATORS; TUMOR CELLS, CULTURED;

EID: 84876676834     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1200-5     Document Type: Review

References (52)

1. Salina D, Bodoor K, Eckley DM, Schroer TA, Rattner JB, Burke B (2002) Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108(1):97-107. pii:S0092867401006286 (Pubitemid 34137015)
2. Beaudouin J, Gerlich D, Daigle N, Eils R, Ellenberg J (2002) Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 108(1):83-96. pii:S0092867401006274 (Pubitemid 34137014)
3. Burke B, Ellenberg J (2002) Remodelling the walls of the nucleus. Nat Rev Mol Cell Biol 3(7):487-497. doi: 10.1038/nrm860 (Pubitemid 34733430)
4. Gatlin JC, Bloom K (2010) Microtubule motors in eukaryotic spindle assembly and maintenance. Semin Cell Dev Biol 21(3):248-254. doi: 10.1016/j.semcdb.2010.01.015
5. Walczak CE, Cai S, Khodjakov A (2010) Mechanisms of chromosome behaviour during mitosis. Nat Rev Mol Cell Biol 11(2):91-102. doi: 10.1038/nrm2832
6. Hiraoka Y, Dernburg AF (2009) The SUN rises on meiotic chromosome dynamics. Dev Cell 17(5):598-605. doi: 10.1016/j.devcel.2009.10.014
7. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, Xu R, Han M (2009) SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64(2):173-187. doi: 10.1016/j.neuron.2009.08.018
8. Malone CJ, Misner L, Le Bot N, Tsai MC, Campbell JM, Ahringer J, White JG (2003) The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115(7):825-836. S0092867403009851 [pii] (Pubitemid 38058495)
9. Fischer JA, Acosta S, Kenny A, Cater C, Robinson C, Hook J (2004) Drosophila klarsicht has distinct subcellular localization domains for nuclear envelope and microtubule localization in the eye. Genetics 168(3):1385-1393. doi: 10.1534/genetics.104.028662 (Pubitemid 40007354)
10. Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, Stewart CL, Burke B (2009) Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci USA 106(7):2194-2199. doi: 10.1073/pnas.0808602106
11. Fridolfsson HN, Ly N, Meyerzon M, Starr DA (2010) UNC-83 coordinates kinesin-1 and dynein activities at the nuclear envelope during nuclear migration. Dev Biol 338(2):237-250. doi: 10.1016/j.ydbio.2009.12.004
12. Wilson KL, Berk JM (2010) The nuclear envelope at a glance. J Cell Sci 123(Pt 12):1973-1978. doi: 10.1242/jcs.019042
13. Starr DA, Fridolfsson HN (2010) Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 26:421-444. doi: 10.1146/annurev-cellbio-100109-104037
14. Mejat A, Misteli T (2010) LINC complex in health and disease. Nucleus 1(1):40-52
15. Mattout A, Goldberg M, Tzur Y, Margalit A, Gruenbaum Y (2007) Specific and conserved sequences in D. melanogaster and C. elegans lamins and histone H2A mediate the attachment of lamins to chromosomes. J Cell Sci 120(Pt 1):77-85. doi: 10.1242/jcs.03325 (Pubitemid 46206651)
16. Taniura H, Glass C, Gerace L (1995) A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J Cell Biol 131(1):33-44
17. Kubben N, Voncken JW, Demmers J, Calis C, van Almen G, Pinto Y, Misteli T (2010) Identification of differential protein interactors of lamin A and progerin. Nucleus 1(6):513-525. doi: 10.4161/nucl.1.6.13512
18. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453(7197):948-951. doi: 10.1038/nature06947 (Pubitemid 351832561)
19. Polioudaki H, Kourmouli N, Drosou V, Bakou A, Theodoropoulos PA, Singh PB, Giannakouros T, Georgatos SD (2001) Histones H3/H4 form a tight complex with the inner nuclear membrane protein LBR and heterochromatin protein 1. EMBO Rep 2(10):920-925. doi: 10.1093/embo-reports/kve199 (Pubitemid 33040581)
20. Montes de Oca R, Lee KK, Wilson KL (2005) Binding of barrier to autointegration factor (BAF) to histone H3 and selected linker histones including H1.1. J Biol Chem 280(51):42252-42262. doi: 10.1074/jbc.M509917200 (Pubitemid 43023196)
21. Antoniacci LM, Kenna MA, Skibbens RV (2007) The nuclear envelope and spindle pole body-associated Mps3 protein bind telomere regulators and function in telomere clustering. Cell Cycle 6(1):75-79 (Pubitemid 46173884)
22. Chikashige Y, Tsutsumi C, Yamane M, Okamasa K, Haraguchi T, Hiraoka Y (2006) Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125(1):59-69. doi: 10.1016/j.cell.2006.01.048
23. Conrad MN, Lee CY, Wilkerson JL, Dresser ME (2007) MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 104(21):8863-8868. doi: 10.1073/pnas.0606165104 (Pubitemid 47175402)
24. King MC, Drivas TG, Blobel G (2008) A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 134(3):427-438. doi: 10.1016/j.cell.2008.06.022
25. Gerlitz G, Livnat I, Ziv C, Yarden O, Bustin M, Reiner O (2007) Migration cues induce chromatin alterations. Traffic 8(11):1521-1529. doi: 10.1111/j.1600-0854.2007.00638.x (Pubitemid 47578358)
26. Dahl KN, Scaffidi P, Islam MF, Yodh AG, Wilson KL, Misteli T (2006) Distinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 103(27):10271-10276. doi: 10.1073/pnas.0601058103 (Pubitemid 44051156)
27. Quintyne NJ, Schroer TA (2002) Distinct cell cycle-dependent roles for dynactin and dynein at centrosomes. J Cell Biol 159(2):245-254. doi: 10.1083/jcb.200203089 (Pubitemid 35283394)
28. Gonda MA, Aaronson SA, Ellmore N, Zeve VH, Nagashima K (1976) Ultrastructural studies of surface features of human normal and tumor cells in tissue culture by scanning and transmission electron microscopy. J Natl Cancer Inst 56(2):245-263
29. Daigle N, Beaudouin J, Hartnell L, Imreh G, Hallberg E, Lippincott-Schwartz J, Ellenberg J (2001) Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J Cell Biol 154(1):71-84 (Pubitemid 34289279)
30. Andres V, Gonzalez JM (2009) Role of A-type lamins in signaling, transcription, and chromatin organization. J Cell Biol 187(7):945-957. doi: 10.1083/jcb.200904124
31. Dittmer TA, Misteli T (2011) The lamin protein family. Genome Biol 12(5):222. doi: 10.1186/gb-2011-12-5-222
32. De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, Boccaccio I, Lyonnet S, Stewart CL, Munnich A, Le Merrer M, Levy N (2003) Lamin a truncation in Hutchinson-Gilford progeria. Science 300(5628):2055. doi: 10.1126/science.1084125 (Pubitemid 36760124)
33. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, Dutra A, Pak E, Durkin S, Csoka AB, Boehnke M, Glover TW, Collins FS (2003) Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423(6937):293-298. doi: 10.1038/nature01629 (Pubitemid 40852699)
34. Verstraeten VL, Ji JY, Cummings KS, Lee RT, Lammerding J (2008) Increased mechanosensitivity and nuclear stiffness in Hutchinson-Gilford progeria cells: effects of farnesyltransferase inhibitors. Aging Cell 7(3):383-393. doi: 10.1111/j.1474-9726.2008.00382.x (Pubitemid 351663907)
35. Hebbar S, Mesngon MT, Guillotte AM, Desai B, Ayala R, Smith DS (2008) Lis1 and Ndel1 influence the timing of nuclear envelope breakdown in neural stem cells. J Cell Biol 182(6):1063-1071. doi: 10.1083/jcb.200803071
36. Busson S, Dujardin D, Moreau A, Dompierre J, De Mey JR (1998) Dynein and dynactin are localized to astral microtubules and at cortical sites in mitotic epithelial cells. Curr Biol 8(9):541-544. S0960-9822(98)70208-8 [pii] (Pubitemid 28203076)
37. Schroer TA (2004) Dynactin. Annu Rev Cell Dev Biol 20:759-779. doi: 10.1146/annurev.cellbio.20.012103.094623 (Pubitemid 39488657)
38. Kardon JR, Vale RD (2009) Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol 10(12):854-865. doi: 10.1038/nrm2804
39. Brandt A, Papagiannouli F, Wagner N, Wilsch-Brauninger M, Braun M, Furlong EE, Loserth S, Wenzl C, Pilot F, Vogt N, Lecuit T, Krohne G, Grosshans J (2006) Developmental control of nuclear size and shape by Kugelkern and Kurzkern. Curr Biol 16(6):543-552. doi: 10.1016/j.cub.2006.01.051
40. Hampoelz B, Azou-Gros Y, Fabre R, Markova O, Puech PH, Lecuit T (2011) Microtubule-induced nuclear envelope fluctuations control chromatin dynamics in Drosophila embryos. Development 138(16):3377-3386. doi: 10.1242/dev.065706
41. Smetana K, Mikulenkova D, Klamova H (2011) Heterochromatin density (condensation) during cell differentiation and maturation using the human granulocytic lineage of chronic myeloid leukaemia as a convenient model. Folia Biol (Praha) 57(5):216-221. pii: FB2011A0031
42. Bainton DF, Ullyot JL, Farquhar MG (1971) The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. J Exp Med 134(4):907-934
43. Olins AL, Olins DE (2004) Cytoskeletal influences on nuclear shape in granulocytic HL-60 cells. BMC Cell Biol 5:30. doi: 10.1186/1471-2121-5-30 (Pubitemid 39637275)
44. Olins AL, Ernst A, Zwerger M, Herrmann H, Olins DE (2010) An in vitro model for Pelger-Huet anomaly: stable knockdown of lamin B receptor in HL-60 cells. Nucleus 1(6):506-512. doi: 10.4161/nucl.1.6.13271
45. Olins AL, Herrmann H, Lichter P, Kratzmeier M, Doenecke D, Olins DE (2001) Nuclear envelope and chromatin compositional differences comparing undifferentiated and retinoic acid- and phorbol ester-treated HL-60 cells. Exp Cell Res 268(2):115-127. doi: 10.1006/excr.2001.5269 (Pubitemid 32744643)
46. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D (2006) Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172(1):41-53. doi: 10.1083/jcb.200509124 (Pubitemid 43042628)
47. Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM, Fry AM, Trembath RC, Shackleton S (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(10):3738-3751. doi: 10.1128/MCB.26.10.3738-3751. 2006 (Pubitemid 43726392)
48. Haque F, Mazzeo D, Patel JT, Smallwood DT, Ellis JA, Shanahan CM, Shackleton S (2010) Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes. J Biol Chem 285(5):3487-3498. doi: 10.1074/jbc.M109.071910
49. Gregory WA, Edmondson JC, Hatten ME, Mason CA (1988) Cytology and neuron-glial apposition of migrating cerebellar granule cells in vitro. J Neurosci 8(5):1728-1738
50. Freitag M, Hickey PC, Raju NB, Selker EU, Read ND (2004) GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet Biol 41(10):897-910. doi: 10.1016/j.fgb.2004.06. 008 (Pubitemid 39165635)
51. Ingber DE (2006) Cellular mechanotransduction: putting all the pieces together again. FASEB J 20(7):811-827. doi: 10.1096/fj.05-5424rev (Pubitemid 44943939)
52. Wang N, Tytell JD, Ingber DE (2009) Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10(1):75-82. doi: 10.1038/nrm2594