The distinct roles of the nucleus and nucleus-cytoskeleton connections in three-dimensional cell migration

Scientific Reports

Volumn 2, Issue , 2012, Pages

  Khatau, Shyam B ^a,b   Bloom, Ryan J ^a,e   Bajpai, Saumendra ^a,b,f   Razafsky, David ^c   Zang, Shu ^c   Giri, Anjil ^a,b   Wu, Pei Hsun ^a,b   Marchand, Jorge ^a,b   Celedon, Alfredo ^a,b,d   Hale, Christopher M ^a,b   Sun, Sean X ^a,b   Hodzic, Didier ^c   Wirtz, Denis ^a,c  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^e Stanford University   (United States)

^f Cornell University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; LAMIN A; MULTIPROTEIN COMPLEX;

ANIMAL; ARTICLE; CELL MOTION; CELL NUCLEUS; CYTOSKELETON; EXTRACELLULAR MATRIX; FIBROBLAST; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; PHENOTYPE; PHYSIOLOGY; RNA INTERFERENCE;

ACTINS; ANIMALS; CELL MOVEMENT; CELL NUCLEUS; CYTOSKELETON; EXTRACELLULAR MATRIX; FIBROBLASTS; LAMIN TYPE A; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MULTIPROTEIN COMPLEXES; PHENOTYPE; RNA INTERFERENCE;

EID: 84863809273     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep00488     Document Type: Article

References (59)

1. Pollard, T. D. & Borisy, G. G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465 (2003). (Pubitemid 36263079)
2. Ridley, A. J. et al. Cell migration: integrating signals from front to back. Science 302, 1704-1709 (2003). (Pubitemid 37505725)
3. Sahai, E. & Marshall, C. J. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCKsignalling and extracellular proteolysis. Nat Cell Biol 5, 711-719 (2003). (Pubitemid 36986778)
4. Symons, M.&Segall, J. E. Rac and Rho driving tumor invasion: who's at the wheel? Genome Biol 10, 213 (2009).
5. Kedrin, D., van Rheenen, J., Hernandez, L., Condeelis, J.&Segall, J. E. Cell motility and cytoskeletal regulation in invasion and metastasis. J Mammary Gland Biol Neoplasia 12, 143-152 (2007). (Pubitemid 47215432)
6. Crisp, M. et al. Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172, 41-53 (2006). (Pubitemid 43042628)
7. Stewart, C. L., Roux, K. J. & Burke, B. Blurring the boundary: the nuclear envelope extends its reach. Science 318, 1408-1412 (2007). (Pubitemid 350208920)
8. Zaman, M. H. et al.Migration of tumor cells in 3D matrices is governed bymatrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci USA 103, 10889-10894 (2006). (Pubitemid 44148391)
9. Bloom, R. J., George, J. P.,Celedon,A., Sun, S. X.&Wirtz, D. Mapping local matrix remodeling induced by a migrating tumor cell using three-dimensional multipleparticle tracking. Biophys J 95, 4077-4088 (2008).
10. Meshel, A. S., Wei, Q., Adelstein, R. S. & Sheetz, M. P. Basic mechanism of threedimensional collagen fibre transport by fibroblasts. Nat Cell Biol 7, 157-164 (2005). (Pubitemid 40268130)
11. Sabeh, F., Shimizu-Hirota, R. & Weiss, S. J. Protease-dependent versus-independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 185, 11-19 (2009).
12. Walpita, D. & Hay, E. Studying actin-dependent processes in tissue culture. Nat Rev Mol Cell Biol 3, 137-141 (2002).
13. Zhou, X. et al. Fibronectin fibrillogenesis regulates three-dimensional neovessel formation. Genes Dev 22, 1231-1243 (2008). (Pubitemid 351656581)
14. Hotary, K. B. et al. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114, 33-45 (2003). (Pubitemid 36859839)
15. Wolf, K. et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 9, 893-904 (2007). (Pubitemid 47190444)
16. Starr, D. A. & Han, M. ANChors away: an actin based mechanism of nuclear positioning. J Cell Sci 116, 211-216 (2003). (Pubitemid 36163862)
17. Starr, D. A. et al. unc-83 encodes a novel component of the nuclear envelope and is essential for proper nuclear migration. Development 128, 5039-5050 (2001). (Pubitemid 34083031)
18. McGee, M. D., Rillo, R., Anderson, A. S. & Starr, D. A. UNC-83 IS a KASH protein required for nuclear migration and is recruited to the outer nuclear membrane by a physical interaction with the SUN protein UNC-84. Mol Biol Cell 17, 1790-1801 (2006). (Pubitemid 44011595)
19. Malone, C. J. et al. The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115, 825-836 (2003). (Pubitemid 38058495)
20. Kracklauer, M. P., Banks, S. M., Xie, X.,Wu, Y. & Fischer, J. A. Drosophila klaroid encodes a SUN domain protein required for Klarsicht localization to the nuclear envelope and nuclear migration in the eye. Fly (Austin) 1, 75-85 (2007).
21. Technau, M. & Roth, S. The Drosophila KASH domain proteins Msp-300 and Klarsicht and the SUN domain protein klaroid have no essential function during oogenesis. Fly (Austin) 2, (2008).
22. Padmakumar, V. C. et al. The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J Cell Sci 118, 3419-3430 (2005). (Pubitemid 41246097)
23. Stewart-Hutchinson, P. J., Hale, C. M., Wirtz, D. & Hodzic, D. Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp Cell Res 314, 1892-1905 (2008).
24. Mejat, A. et al. Lamin A/C-mediated neuromuscular junction defects in Emery-Dreifuss muscular dystrophy. J Cell Biol 184, 31-44 (2009).
25. Hale, C. M. et al. Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models. Biophys J 95, 5462-5475 (2008).
26. Khatau, S. B. et al. A perinuclear actin cap regulates nuclear shape. Proc Natl Acad Sci USA 106, 19017-19022 (2009).
27. Khatau, S. B., Kim, D. H., Hale, C. M., Bloom, R. J. & Wirtz, D. The perinuclear actin cap in health and disease. Nucleus 1, 337-342 (2010).
28. Khatau, S. B., Khatau, S. B., K, S., Hanjaya-Putra, D., Mali, P., Cheng, L., Lee, J. S. H., Gerecht, S. & Wirtz, D. The differential formation of the LINC-mediated perinuclear actin cap in pluripotent and somatic cells PLoS ONE (2012).
29. Lee, J. S. et al. Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys J 93, 2542-2552 (2007). (Pubitemid 47511153)
30. Hale, C. M. et al. SMRT analysis ofMTOCand nuclear positioning reveals the role of EB1 and LIC1 in single-cell polarization. J Cell Sci 124, 4267-4285 (2011).
31. Kim, H. D. et al. Epidermal growth factor-induced enhancement of glioblastoma cell migration in 3D arises from an intrinsic increase in speed but an extrinsic matrix-and proteolysis-dependent increase in persistence. Mol Biol Cell 19, 4249-4259 (2008).
32. Fraley, S. I., Feng, Y., Wirtz, D. & Longmore, G. D. Reply: reducing background fluorescence reveals adhesions in 3D matrices. Nat Cell Biol 13, 5-7 (2011).
33. Bloom, R. J., George, J. P.,Celedon,A., Sun, S. X.&Wirtz, D. Mapping local matrix remodeling induced by a migrating tumor cell using three-dimensional multipleparticle tracking. Biophysical Journal 95, 4077-4088 (2008).
34. Fraley, S. I., Feng, Y., Giri, A., Longmore, G. D. & Wirtz, D. Dimensional and temporal controls of three-dimensional cell migration by zyxin and binding partners. Nat Commun 3, 719 (2012).
35. Fraley, S. I. et al.Adistinctive role for focal adhesion proteins in three-dimensional cell motility. Nat Cell Biol 12, 598-604 (2010).
36. Libotte, T. et al. Lamin A/C-dependent localization of Nesprin-2, a giant scaffolder at the nuclear envelope. Mol Biol Cell 16, 3411-3424 (2005). (Pubitemid 40962609)
37. Ketema, M. et al. Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin. J Cell Sci 120, 3384-3394 (2007). (Pubitemid 350028346)
38. Ostlund, C. et al.Dynamics and molecular interactions of linker of nucleoskeleton and cytoskeleton (LINC) complex proteins. J Cell Sci 122, 4099-4108 (2009).
39. Peyton, S. R. & Putnam, A. J. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J Cell Physiol 204, 198-209 (2005). (Pubitemid 40776823)
40. Ulrich, T. A., de Juan Pardo, E. M. & Kumar, S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res 69, 4167-4174 (2009).
41. Rehfeldt, F. et al. Hyaluronic acid matrices show matrix stiffness in 2D and 3D dictates cytoskeletal order and myosin-II phosphorylation within stem cells. Integr Biol (Camb) 4, 422-430 (2012).
42. Jaalouk, D. E. & Lammerding, J. Mechanotransduction gone awry. Nat Rev Mol Cell Biol 10, 63-73 (2009).
43. Crisp, M. & Burke, B. The nuclear envelope as an integrator of nuclear and cytoplasmic architecture. FEBS Lett 582, 2023-2032 (2008).
44. Razafsky, D. & Hodzic, D. Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J Cell Biol 186, 461-472 (2009).
45. Postel, R., Ketema, M., Kuikman, I., de Pereda, J. M. & Sonnenberg, A. Nesprin-3 augments peripheral nuclear localization of intermediate filaments in zebrafish. J Cell Sci 124, 755-764.
46. Dupin, I., Sakamoto, Y. & Etienne-Manneville, S. Cytoplasmic intermediate filaments mediate actin-driven positioning of the nucleus. J Cell Sci 124, 865-872 (2011).
47. Lee, J. S., Chang, M. I., Tseng, Y. &Wirtz, D. Cdc42 mediates nucleus movement and MTOC polarization in Swiss 3T3 fibroblasts under mechanical shear stress. Mol Biol Cell 16, 871-880 (2005). (Pubitemid 40165578)
48. Emerson, L. J. et al. Defects in cell spreading and ERK1/2 activation in fibroblasts with lamin A/C mutations. Biochim Biophys Acta 1792, 810-821 (2009).
49. Scharner, J. et al. Novel LMNA mutations in patients with Emery-Dreifuss muscular dystrophy and functional characterization of four LMNA mutations. Hum Mutat 32, 152-167 (2011).
50. Tseng, Y., Lee, J. S., Kole, T. P., Jiang, I. &Wirtz, D. Micro-organization and viscoelasticity of the interphase nucleus revealed by particle nanotracking. J Cell Sci 117, 2159-2167 (2004). (Pubitemid 38745148)
51. Tseng, Y. et al. How actin crosslinking and bundling proteins cooperate to generate an enhanced cell mechanical response. Biochem Biophys Res Commun 334, 183-192 (2005). (Pubitemid 40978524)
52. Celedon, A., Hale, C. M. & Wirtz, D. Magnetic manipulation of nanorods in the nucleus of living cells. Biophys J 101, 1880-1886 (2011).
53. Dahl, K. N., Kahn, S. M., Wilson, K. L. & Discher, D. E. The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of amolecular shock absorber. J Cell Sci Pt (2004).
54. Sullivan, T. et al. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147, 913-920 (1999).
55. Panorchan, P., Tseng, Y. &Wirtz, D. Structure-function relationship of biological gels revealed by multiple particle tracking and differential interference contrast microscopy: The case of human lamin networks. Phys Rev E 70, 041906 (2004).
56. Apgar, J. et al. Multiple-particle tracking measurements of heterogeneities in solutions of actin filaments and actin bundles. Biophys. J. 79, 1095-1106 (2000). (Pubitemid 30626200)
57. Amsden, B. An obstruction-scaling model for diffusion in homogeneous hydrogels. Macromolecules 32, (1999).
58. Westerweel, J., Vol. PhD (Delft University of Technology, Delft, 1993).
59. Adrian, R. J. Particle-imaging techniques for experimental fluid mechanics. Annual Review of Fluid Mechanics 23, 261-304 (1991).