Emerging role for nuclear rotation and orientation in cell migration
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
24589621
PubMed Central
PMC3974792
DOI
10.4161/cam.27761
PII: 27761
Knihovny.cz E-zdroje
- Klíčová slova
- FAK, LINC, actin, cell polarity, dynein, focal adhesions, microtubules, migration, myosin, nuclear reorientation,
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Nucleus movement, positioning, and orientation is precisely specified and actively regulated within cells, and it plays a critical role in many cellular and developmental processes. Mutation of proteins that regulate the nucleus anchoring and movement lead to diverse pathologies, laminopathies in particular, suggesting that the nucleus correct positioning and movement is essential for proper cellular function. In motile cells that polarize toward the direction of migration, the nucleus undergoes controlled rotation promoting the alignment of the nucleus with the axis of migration. Such spatial organization of the cell appears to be optimal for the cell migration. Nuclear reorientation requires the cytoskeleton to be anchored to the nuclear envelope, which exerts pulling or pushing torque on the nucleus. Here we discuss the possible molecular mechanisms regulating the nuclear rotation and reorientation and the significance of this type of nuclear movement for cell migration.
Cell and Molecular Microbiology Division; Institute of Microbiology; Prague Czech Republic
Department of Cell Biology; Harvard Medical School; Boston MA USA
Zobrazit více v PubMed
Luxton GW, Gundersen GG. Orientation and function of the nuclear-centrosomal axis during cell migration. Curr Opin Cell Biol. 2011;23:579–88. doi: 10.1016/j.ceb.2011.08.001. PubMed DOI PMC
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. doi: 10.1016/j.bbamcr.2008.10.003. PubMed DOI
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. doi: 10.1016/j.jmb.2013.02.034. PubMed DOI
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. doi: 10.1073/pnas.0908686106. PubMed DOI PMC
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. doi: 10.1126/science.1189072. PubMed DOI PMC
Pomerat CM. Rotating nuclei in tissue cultures of adult human nasal mucosa. Exp Cell Res. 1953;5:191–6. doi: 10.1016/0014-4827(53)90104-9. PubMed DOI
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. doi: 10.1007/BF00345357. PubMed DOI
Nakai J. Dissociated dorsal root ganglia in tissue culture. Am J Anat. 1956;99:81–129. doi: 10.1002/aja.1000990105. PubMed DOI
Capers CR. Multinucleation of skeletal muscle in vitro. J Biophys Biochem Cytol. 1960;7:559–66. doi: 10.1083/jcb.7.3.559. PubMed DOI PMC
De Boni U, Mintz AH. Curvilinear, three-dimensional motion of chromatin domains and nucleoli in neuronal interphase nuclei. Science. 1986;234:863–6. doi: 10.1126/science.3775367. PubMed DOI
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. doi: 10.1016/0014-4827(86)90083-2. PubMed DOI
Paddock SW, Albrecht-Buehler G. Rigidity of the nucleus during nuclear rotation in 3T3 cells. Exp Cell Res. 1988;175:409–13. doi: 10.1016/0014-4827(88)90205-4. PubMed DOI
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. doi: 10.1074/jbc.M611094200. PubMed DOI
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. doi: 10.1111/j.1768-322X.1985.tb00388.x. PubMed DOI
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. doi: 10.1016/0014-4827(91)90425-T. PubMed DOI
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. doi: 10.1091/mbc.E03-12-0910. PubMed DOI PMC
Levy JR, Holzbaur EL. Dynein drives nuclear rotation during forward progression of motile fibroblasts. J Cell Sci. 2008;121:3187–95. doi: 10.1242/jcs.033878. PubMed DOI PMC
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. doi: 10.1016/j.biocel.2010.07.001. PubMed DOI
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. doi: 10.1016/j.cellbi.2009.06.020. PubMed DOI
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. doi: 10.1002/cm.970180107. PubMed DOI
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. doi: 10.1083/jcb.200612043. PubMed DOI PMC
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. doi: 10.1038/ncb1762. PubMed DOI
Dahl KN, Ribeiro AJ, Lammerding J. Nuclear shape, mechanics, and mechanotransduction. Circ Res. 2008;102:1307–18. doi: 10.1161/CIRCRESAHA.108.173989. PubMed DOI PMC
Starr DA, Fridolfsson HN. Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol. 2010;26:421–44. doi: 10.1146/annurev-cellbio-100109-104037. PubMed DOI PMC
Dupin I, Etienne-Manneville S. Nuclear positioning: mechanisms and functions. Int J Biochem Cell Biol. 2011;43:1698–707. doi: 10.1016/j.biocel.2011.09.004. PubMed DOI
Gundersen GG, Worman HJ. Nuclear positioning. Cell. 2013;152:1376–89. doi: 10.1016/j.cell.2013.02.031. PubMed DOI PMC
Starr DA. A nuclear-envelope bridge positions nuclei and moves chromosomes. J Cell Sci. 2009;122:577–86. doi: 10.1242/jcs.037622. PubMed DOI PMC
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. doi: 10.1073/pnas.0808602106. PubMed DOI PMC
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. doi: 10.1529/biophysj.106.102426. PubMed DOI PMC
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. doi: 10.1074/jbc.M111.233700. PubMed DOI PMC
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 nucleus-cytoskeleton connections in three-dimensional cell migration. Sci Rep. 2012;2:488. doi: 10.1038/srep00488. PubMed DOI PMC
Joseph J, Dasso M. The nucleoporin Nup358 associates with and regulates interphase microtubules. FEBS Lett. 2008;582:190–6. doi: 10.1016/j.febslet.2007.11.087. PubMed DOI PMC
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. doi: 10.1083/jcb.200702026. PubMed DOI PMC
Dupin I, Sakamoto Y, Etienne-Manneville S. Cytoplasmic intermediate filaments mediate actin-driven positioning of the nucleus. J Cell Sci. 2011;124:865–72. doi: 10.1242/jcs.076356. PubMed DOI
Vallee RB, Stehman SA. How dynein helps the cell find its center: a servomechanical model. Trends Cell Biol. 2005;15:288–94. doi: 10.1016/j.tcb.2005.04.005. PubMed DOI
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. doi: 10.1038/nn1934. PubMed DOI
Wu J, Lee KC, Dickinson RB, Lele TP. How dynein and microtubules rotate the nucleus. J Cell Physiol. 2011;226:2666–74. doi: 10.1002/jcp.22616. PubMed DOI
Khatau SB, Kim DH, Hale CM, Bloom RJ, Wirtz D. The perinuclear actin cap in health and disease. Nucleus. 2010;1:337–42. doi: 10.4161/nucl.1.4.12331. PubMed DOI PMC
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. doi: 10.1016/j.ceb.2009.05.006. PubMed DOI PMC
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. doi: 10.1073/pnas.94.3.849. PubMed DOI PMC
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. doi: 10.1038/nrm2594. PubMed DOI
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. doi: 10.1371/journal.pone.0036689. PubMed DOI PMC
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. doi: 10.1083/jcb.200310097. PubMed DOI PMC
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. doi: 10.1038/srep00555. PubMed DOI PMC
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. doi: 10.1083/jcb.134.5.1209. PubMed DOI PMC
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. doi: 10.1083/jcb.201004118. PubMed DOI PMC
Friedl P, Wolf K, Lammerding J. Nuclear mechanics during cell migration. Curr Opin Cell Biol. 2011;23:55–64. doi: 10.1016/j.ceb.2010.10.015. PubMed DOI PMC
Mili S, Moissoglu K, Macara IG. Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature. 2008;453:115–9. doi: 10.1038/nature06888. PubMed DOI PMC