Emerging role for nuclear rotation and orientation in cell migration

Cell Adhesion and Migration

Volumn 8, Issue 1, 2014, Pages 42-48

  Maninová, Miloslava ^a   Iwanicki, Marcin P ^b   Vomastek, Tomáš ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Actin; Cell polarity; Dynein; FAK; Focal adhesions; LINC; Microtubules; Migration; Myosin; Nuclear reorientation

Indexed keywords

ACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; INTEGRIN; MOLECULAR MOTOR;

ACTIN FILAMENT; ADHERENT CELL; ARTICLE; CELL FUNCTION; CELL MIGRATION; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CYTOSKELETON; FIBROBLAST; FOCAL ADHESION; HUMAN; INTERMEDIATE FILAMENT; MICROTUBULE; NUCLEAR LAMINA; NUCLEAR PORE COMPLEX; SIGNAL TRANSDUCTION;

EID: 84897533668     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.27761     Document Type: Article

References (48)

1. Luxton GW, Gundersen GG. Orientation and function of the nuclear-centrosomal axis during cell migration. Curr Opin Cell Biol 2011; 23:579-88; PMID:21885270; http://dx.doi.org/10.1016/j. ceb.2011.08.001
2. Houben F, Willems CH, Declercq IL, Hochstenbach K, Kamps MA, Snoeckx LH, Ramaekers FC, Broers JL. Disturbed nuclear orientation and cellular migration in A-type lamin deficient cells. Biochim Biophys Acta 2009; 1793:312-24; PMID:19013199; http://dx.doi.org/10.1016/j.bbamcr.2008.10.003
3. Maninová M, Klímová Z, Parsons JT, Weber MJ, Iwanicki MP, Vomastek T. The reorientation of cell nucleus promotes the establishment of front-rear polarity in migrating fibroblasts. J Mol Biol 2013; 425:2039-55; PMID:23524135; http://dx.doi.org/10.1016/j.jmb.2013.02.034
4. Khatau SB, Hale CM, Stewart-Hutchinson PJ, Patel MS, Stewart CL, Searson PC, Hodzic D, Wirtz D. A perinuclear actin cap regulates nuclear shape. Proc Natl Acad Sci U S A 2009; 106:19017-22; PMID:19850871; http://dx.doi.org/10. 1073/pnas.0908686106
5. Luxton GW, Gomes ER, Folker ES, Vintinner E, Gundersen GG. Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science 2010; 329:956-9; PMID:20724637; http://dx.doi.org/10.1126/science. 1189072
6. Pomerat CM. Rotating nuclei in tissue cultures of adult human nasal mucosa. Exp Cell Res 1953; 5:191-6; PMID:13083628; http://dx.doi.org/10.1016/ 0014-4827(53)90104-9
7. Leone V, Hsu TC, Pomerat CM. Cytological studies on HeLa, a strain of human cervical carcinoma. II. On rotatory movements of the nuclei. Z Zellforsch Mikrosk Anat 1955; 41:481-92; PMID:14387135; http://dx.doi.org/10.1007/ BF00345357
8. Nakai J. Dissociated dorsal root ganglia in tissue culture. Am J Anat 1956; 99:81-129; PMID:13362126; http://dx.doi.org/10.1002/aja.1000990105
9. Capers CR. Multinucleation of skeletal muscle in vitro. J Biophys Biochem Cytol 1960; 7:559-66; PMID:13807523; http://dx.doi.org/10.1083/jcb.7.3.559
10. De Boni U, Mintz AH. Curvilinear, three-dimensional motion of chromatin domains and nucleoli in neuronal interphase nuclei. Science 1986; 234:863-6; PMID:3775367; http://dx.doi.org/10.1126/science.3775367
11. Paddock SW, Albrecht-Buehler G. Distribution of microfilament bundles during rotation of the nucleus in 3T3 cells treated with monensin. Exp Cell Res 1986; 163:525-38; PMID:3514249; http://dx.doi.org/10.1016/0014-4827(86)90083-2
12. Paddock SW, Albrecht-Buehler G. Rigidity of the nucleus during nuclear rotation in 3T3 cells. Exp Cell Res 1988; 175:409-13; PMID:3360061; http://dx.doi.org/10.1016/0014-4827(88)90205-4
13. Ji JY, Lee RT, Vergnes L, Fong LG, Stewart CL, Reue K, Young SG, Zhang Q, Shanahan CM, Lammerding J. Cell nuclei spin in the absence of lamin b1. J Biol Chem 2007; 282:20015-26; PMID:17488709; http://dx.doi.org/10.1074/jbc.M611094200
14. Bard F, Bourgeois CA, Costagliola D, Bouteille M. Rotation of the cell nucleus in living cells: A quantitative analysis. Biol Cell 1985; 54:135-42; PMID:2933103; http://dx.doi.org/10.1111/j.1768-322X.1985.tb00388.x
15. Park PC, De Boni U. Dynamics of nucleolar fusion in neuronal interphase nuclei in vitro: Association with nuclear rotation. Exp Cell Res 1991; 197:213-21; PMID:1959557; http://dx.doi.org/10.1016/0014-4827(91)90425-T
16. Lee JS, Chang MI, Tseng Y, Wirtz D. Cdc42 mediates nucleus movement and MTOC polarization in Swiss 3T3 fibroblasts under mechanical shear stress. Mol Biol Cell 2005; 16:871-80; PMID:15548602; http://dx.doi.org/10.1091/mbc.E03-12- 0910
17. Levy JR, Holzbaur EL. Dynein drives nuclear rotation during forward progression of motile fibroblasts. J Cell Sci 2008; 121:3187-95; PMID:18782860; http://dx.doi.org/10.1242/jcs.033878
18. Brosig M, Ferralli J, Gelman L, Chiquet M, Chiquet-Ehrismann R. Interfering with the connection between the nucleus and the cytoskeleton affects nuclear rotation, mechanotransduction and myogenesis. Int J Biochem Cell Biol 2010; 42:1717-28; PMID:20621196; http://dx.doi.org/10.1016/j. biocel.2010.07.001
19. Gerashchenko MV, Chernoivanenko IS, Moldaver MV, Minin AA. Dynein is a motor for nuclear rotation while vimentin IFs is a "brake". Cell Biol Int 2009; 33:1057-64; PMID:19560548; http://dx.doi.org/10.1016/j.cellbi.2009.06. 020
20. Hay M, De Boni U. Chromatin motion in neuronal interphase nuclei: Changes induced by disruption of intermediate filaments. Cell Motil Cytoskeleton 1991; 18:63-75; PMID:2004434; http://dx.doi.org/10.1002/cm.970180107
21. Vicente-Manzanares M, Zareno J, Whitmore L, Choi CK, Horwitz AF. Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J Cell Biol 2007; 176:573-80; PMID:17312025; http://dx.doi.org/10.1083/jcb.200612043
22. Simpson KJ, Selfors LM, Bui J, Reynolds A, Leake D, Khvorova A, Brugge JS. Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat Cell Biol 2008; 10:1027-38; PMID:19160483; http://dx.doi.org/10.1038/ncb1762
23. Dahl KN, Ribeiro AJ, Lammerding J. Nuclear shape, mechanics, and mechanotransduction. Circ Res 2008; 102:1307-18; PMID:18535268; http://dx.doi.org/10.1161/CIRCRESAHA.108.173989
24. Starr DA, Fridolfsson HN. Interactions between nuclei and the cytoskeleton are mediated by SUNKASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 2010; 26:421-44; PMID:20507227; http://dx.doi.org/10.1146/annurev-cellbio- 100109-104037
25. Dupin I, Etienne-Manneville S. Nuclear positioning: Mechanisms and functions. Int J Biochem Cell Biol 2011; 43:1698-707; PMID:21959251; http://dx.doi.org/10.1016/j.biocel.2011.09.004
26. Gundersen GG, Worman HJ. Nuclear positioning. Cell 2013; 152:1376-89; PMID:23498944; http://dx.doi.org/10.1016/j.cell.2013.02.031
27. Starr DA. A nuclear-envelope bridge positions nuclei and moves chromosomes. J Cell Sci 2009; 122:577-86; PMID:19225124; http://dx.doi.org/10. 1242/jcs.037622
28. Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, Stewart CL, Burke B. Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci U S A 2009; 106:2194-9; PMID:19164528; http://dx.doi.org/10.1073/pnas.0808602106
29. Lee JS, Hale CM, Panorchan P, Khatau SB, George JP, Tseng Y, Stewart CL, Hodzic D, Wirtz D. Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys J 2007; 93:2542-52; PMID:17631533; http://dx.doi.org/10.1529/biophysj.106.102426
30. Lombardi ML, Jaalouk DE, Shanahan CM, Burke B, Roux KJ, Lammerding J. The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J Biol Chem 2011; 286:26743-53; PMID:21652697; http://dx.doi.org/10.1074/jbc. M111.233700
31. Khatau SB, Bloom RJ, Bajpai S, Razafsky D, Zang S, Giri A, Wu PH, Marchand J, Celedon A, Hale CM, et al. The distinct roles of the nucleus and nucleuscytoskeleton connections in three-dimensional cell migration. Sci Rep 2012; 2:488; PMID:22761994; http://dx.doi.org/10.1038/srep00488
32. Joseph J, Dasso M. The nucleoporin Nup358 associates with and regulates interphase microtubules. FEBS Lett 2008; 582:190-6; PMID:18070602; http://dx.doi.org/10.1016/j.febslet.2007.11.087
33. Salpingidou G, Smertenko A, Hausmanowa-Petrucewicz I, Hussey PJ, Hutchison CJ. A novel role for the nuclear membrane protein emerin in association of the centrosome to the outer nuclear membrane. J Cell Biol 2007; 178:897-904; PMID:17785515; http://dx.doi.org/10.1083/jcb.200702026
34. Dupin I, Sakamoto Y, Etienne-Manneville S. Cytoplasmic intermediate filaments mediate actindriven positioning of the nucleus. J Cell Sci 2011; 124:865-72; PMID:21378307; http://dx.doi.org/10.1242/jcs.076356
35. Vallee RB, Stehman SA. How dynein helps the cell find its center: A servomechanical model. Trends Cell Biol 2005; 15:288-94; PMID:15953546; http://dx.doi.org/10.1016/j.tcb.2005.04.005
36. Tsai JW, Bremner KH, Vallee RB. Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci 2007; 10:970-9; PMID:17618279; http://dx.doi.org/10.1038/nn1934
37. Wu J, Lee KC, Dickinson RB, Lele TP. How dynein and microtubules rotate the nucleus. J Cell Physiol 2011; 226:2666-74; PMID:21792925; http://dx.doi.org/10.1002/jcp.22616
38. Khatau SB, Kim DH, Hale CM, Bloom RJ, Wirtz D. The perinuclear actin cap in health and disease. Nucleus 2010; 1:337-42; PMID:21327082; http://dx.doi.org/10.4161/nucl.1.4.12331
39. Tomar A, Schlaepfer DD. Focal adhesion kinase: Switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol 2009; 21:676-83; PMID:19525103; http://dx.doi.org/10.1016/j. ceb.2009.05.006
40. Maniotis AJ, Chen CS, Ingber DE. Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci U S A 1997; 94:849-54; PMID:9023345; http://dx.doi.org/10.1073/pnas.94.3.849
41. Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: Mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009; 10:75-82; PMID:19197334; http://dx.doi.org/10.1038/nrm2594
42. Khatau SB, Kusuma S, Hanjaya-Putra D, Mali P, Cheng L, Lee JS, Gerecht S, Wirtz D. The differential formation of the LINC-mediated perinuclear actin cap in pluripotent and somatic cells. PLoS One 2012; 7:e36689; PMID:22574215; http://dx.doi.org/10.1371/journal.pone.0036689
43. Dujardin DL, Barnhart LE, Stehman SA, Gomes ER, Gundersen GG, Vallee RB. A role for cytoplasmic dynein and LIS1 in directed cell movement. J Cell Biol 2003; 163:1205-11; PMID:14691133; http://dx.doi.org/10.1083/jcb.200310097
44. Kim DH, Khatau SB, Feng Y, Walcott S, Sun SX, Longmore GD, Wirtz D. Actin cap associated focal adhesions and their distinct role in cellular mechanosensing. Sci Rep 2012; 2:555; PMID:22870384; http://dx.doi.org/10.1038/ srep00555
45. Anderson KI, Wang YL, Small JV. Coordination of protrusion and translocation of the keratocyte involves rolling of the cell body. J Cell Biol 1996; 134:1209-18; PMID:8794862; http://dx.doi.org/10.1083/jcb.134.5.1209
46. Fridolfsson HN, Starr DA. Kinesin-1 and dynein at the nuclear envelope mediate the bidirectional migrations of nuclei. J Cell Biol 2010; 191:115-28; PMID:20921138; http://dx.doi.org/10.1083/jcb.201004118
47. Friedl P, Wolf K, Lammerding J. Nuclear mechanics during cell migration. Curr Opin Cell Biol 2011; 23:55-64; PMID:21109415; http://dx.doi.org/10.1016/j. ceb.2010.10.015
48. Mili S, Moissoglu K, Macara IG. Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 2008; 453:115-9; PMID:18451862; http://dx.doi.org/10.1038/nature06888