Actomyosin pulls to advance the nucleus in a migrating tissue cell

Biophysical Journal

Volumn 106, Issue 1, 2014, Pages 7-15

  Wu, Jun ^a,b   Kent, Ian A ^a   Shekhar, Nandini ^a,c   Chancellor, T J ^a   Mendonca, Agnes ^a,d   Dickinson, Richard B ^a   Lele, Tanmay P ^a  

^a J Crayton Pruitt Family Department of Biomedical Engineering   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; RAC1 PROTEIN;

3T3 CELL LINE; ANIMAL; ARTICLE; CELL MOTION; CELL NUCLEUS; METABOLISM; MICROTUBULE; MOTION; MOUSE; PHYSIOLOGY; PSEUDOPODIUM; ULTRASTRUCTURE;

ACTOMYOSIN; ANIMALS; CELL CYCLE PROTEINS; CELL MOVEMENT; CELL NUCLEUS; MICE; MICROTUBULES; MOTION; NIH 3T3 CELLS; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN;

EID: 84891867442     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.11.4489     Document Type: Article

References (40)

1. E.R. Gomes, S. Jani, and G.G. Gundersen Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells Cell 121 2005 451 463
2. P. Friedl, K. Wolf, and J. Lammerding Nuclear mechanics during cell migration Curr. Opin. Cell Biol. 23 2011 55 64
3. G.W. Luxton, and G.G. Gundersen Orientation and function of the nuclear-centrosomal axis during cell migration Curr. Opin. Cell Biol. 23 2011 579 588
4. P. Gönczy Mechanisms of asymmetric cell division: flies and worms pave the way Nat. Rev. Mol. Cell Biol. 9 2008 355 366
5. N. Minc, D. Burgess, and F. Chang Influence of cell geometry on division-plane positioning Cell 144 2011 414 426
6. S. Roth, and F.S. Neuman-Silberberg T. Schüpbach cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila Cell 81 1995 967 978
7. X. Zhang, and R. Xu M. Han Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation Development 134 2007 901 908
8. T. Zhao, and O.S. Graham D. St Johnston Growing microtubules push the oocyte nucleus to polarize the Drosophila dorsal-ventral axis Science 336 2012 999 1003
9. B. Burke, and K.J. Roux Nuclei take a position: managing nuclear location Dev. Cell 17 2009 587 597
10. I. Dupin, and S. Etienne-Manneville Nuclear positioning: mechanisms and functions Int. J. Biochem. Cell Biol. 43 2011 1698 1707
11. M. Crisp, and Q. Liu D. Hodzic Coupling of the nucleus and cytoplasm: role of the LINC complex J. Cell Biol. 172 2006 41 53
12. J.R. Levy, and E.L. Holzbaur Dynein drives nuclear rotation during forward progression of motile fibroblasts J. Cell Sci. 121 2008 3187 3195
13. V.C. Padmakumar, and T. Libotte I. Karakesisoglou The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope J. Cell Sci. 118 2005 3419 3430
14. K.J. Roux, and M.L. Crisp B. Burke Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization Proc. Natl. Acad. Sci. USA 106 2009 2194 2199
15. J.W. Tsai, K.H. Bremner, and R.B. Vallee Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue Nat. Neurosci. 10 2007 970 979
16. J. Wu, and K.C. Lee T.P. Lele How dynein and microtubules rotate the nucleus J. Cell. Physiol. 226 2011 2666 2674
17. M.H. Wilson, and E.L. Holzbaur Opposing microtubule motors drive robust nuclear dynamics in developing muscle cells J. Cell Sci. 125 2012 4158 4169
18. A.J. Maniotis, C.S. Chen, and D.E. Ingber Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure Proc. Natl. Acad. Sci. USA 94 1997 849 854
19. J.R. Sims, S. Karp, and D.E. Ingber Altering the cellular mechanical force balance results in integrated changes in cell, cytoskeletal and nuclear shape J. Cell Sci. 103 1992 1215 1222
20. N. Wang, J.D. Tytell, and D.E. Ingber Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus Nat. Rev. Mol. Cell Biol. 10 2009 75 82
21. D.A. Lauffenburger, and A.F. Horwitz Cell migration: a physically integrated molecular process Cell 84 1996 359 369
22. B. Szabó, and R. Ünnep A. Czirók Inhibition of myosin II triggers morphological transition and increased nuclear motility Cytoskeleton (Hoboken) 68 2011 325 339
23. E.S. Folker, and C. Ostlund G.G. Gundersen Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement Proc. Natl. Acad. Sci. USA 108 2011 131 136
24. G.W. Luxton, and E.R. Gomes G.G. Gundersen Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement Science 329 2010 956 959
25. M. Versaevel, T. Grevesse, and S. Gabriele Spatial coordination between cell and nuclear shape within micropatterned endothelial cells Nat. Commun 3 2012 671
26. C.J. Malone, and L. Misner J.G. White The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus Cell 115 2003 825 836
27. K. Patterson, and A.B. Molofsky J.A. Fischer The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye Mol. Biol. Cell 15 2004 600 610
28. S. Reinsch, and E. Karsenti Movement of nuclei along microtubules in Xenopus egg extracts Curr. Biol. 7 1997 211 214
29. H.N. Fridolfsson, and D.A. Starr Kinesin-1 and dynein at the nuclear envelope mediate the bidirectional migrations of nuclei J. Cell Biol. 191 2010 115 128
30. S.K. Vogel, and N. Pavin I.M. Tolić-Nu̧rrelykke Self-organization of dynein motors generates meiotic nuclear oscillations PLoS Biol. 7 2009 e1000087
31. J. Wu, and G. Misra R.B. Dickinson Effects of dynein on microtubule mechanics and centrosome positioning Mol. Biol. Cell 22 2011 4834 4841
32. K. Bhadriraju, and J.T. Elliott A.L. Plant Quantifying myosin light chain phosphorylation in single adherent cells with automated fluorescence microscopy BMC Cell Biol. 8 2007 43
33. W.T. Chen Mechanism of retraction of the trailing edge during fibroblast movement J. Cell Biol. 90 1981 187 200
34. T. Lämmermann, and B.L. Bader M. Sixt Rapid leukocyte migration by integrin-independent flowing and squeezing Nature 453 2008 51 55
35. M. Machacek, and L. Hodgson G. Danuser Coordination of Rho GTPase activities during cell protrusion Nature 461 2009 99 103
36. X. Wang, and L. He D.J. Montell Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo Nat. Cell Biol. 12 2010 591 597
37. Y.I. Wu, and D. Frey K.M. Hahn A genetically encoded photoactivatable Rac controls the motility of living cells Nature 461 2009 104 108
38. C.E. Schmidt, and A.F. Horwitz M.P. Sheetz Integrin-cytoskeletal interactions in migrating fibroblasts are dynamic, asymmetric, and regulated J. Cell Biol. 123 1993 977 991
39. T.J. Chancellor, and J. Lee T. Lele Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation Biophys. J. 99 2010 115 123
40. M.L. Lombardi, and D.E. Jaalouk J. Lammerding The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton J. Biol. Chem. 286 2011 26743 26753