Keeping the LINC: The importance of nucleocytoskeletal coupling in intracellular force transmission and cellular function

Biochemical Society Transactions

Volumn 39, Issue 6, 2011, Pages 1729-1734

  Lombardi, Maria L ^a   Lammerding, Jan ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

Cell mechanics; Force transmission; Lamin; Nesprin; Nucleus; Sun protein

Indexed keywords

LAMIN; LINKER OF NUCLEOSKELETON AND CYTOSKELETON PROTEIN; NESPRIN 1 PROTEIN; NESPRIN 2 PROTEIN; NUCLEAR PROTEIN; SUN1 PROTEIN; SUN2 PROTEIN; UNCLASSIFIED DRUG;

CAENORHABDITIS ELEGANS; CARDIOMYOPATHY; CELL ACTIVITY; CELL FUNCTION; CELL MIGRATION; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL POLARITY; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONFERENCE PAPER; CYTOSKELETON; DROSOPHILA MELANOGASTER; HUMAN; MECHANOTRANSDUCTION; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION;

ANIMALS; BIOMECHANICS; CELL NUCLEUS; CYTOSKELETON; HUMANS; INTRACELLULAR SPACE; MEMBRANE PROTEINS; MULTIPROTEIN COMPLEXES;

EID: 81855212456     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20110686     Document Type: Conference Paper

References (48)

1. Maniotis, A.J., Chen, C.S. and Ingber, D.E. (1997) Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl. Acad. Sci. U.S.A. 94, 849-854 (Pubitemid 27074410)
2. Crisp, M., Liu, Q., Roux, K., Rattner, J.B., Shanahan, C., Burke, B., Stahl, P.D. and Hodzic, D. (2006) Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172, 41-53 (Pubitemid 43042628)
3. Starr, D.A. and Fridolfsson, H.N. (2010) Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu. Rev. Cell Dev. Biol. 26, 421-444
4. Haque, F., Lloyd, D.J., Smallwood, D.T., Dent, C.L., Shanahan, C.M., Fry, A.M., Trembath, R.C. and 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, 3738-3751 (Pubitemid 43726392)
5. Wang, N., Tytell, J.D. and Ingber, D.E. (2009) Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75-82
6. Padmakumar, V.C., Abraham, S., Braune, S., Noegel, A.A., Tunggal, B., Karakesisoglou, I. and Korenbaum, E. (2004) Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp. Cell Res. 295, 330-339 (Pubitemid 38490489)
7. Zhen, Y.Y., Libotte, T., Munck, M., Noegel, A.A. and Korenbaum, E. (2002) NUANCE, a giant protein connecting the nucleus and actin cytoskeleton. J. Cell Sci. 115, 3207-3222
8. Wilhelmsen, K., Litjens, S.H., Kuikman, I., Tshimbalanga, N., Janssen, H., van den Bout, I., Raymond, K. and Sonnenberg, A. (2005) Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J. Cell Biol. 171, 799-810 (Pubitemid 41746582)
9. Roux, K.J., Crisp, M.L., Liu, Q., Kim, D., Kozlov, S., Stewart, C.L. and Burke, B. (2009) Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc. Natl. Acad. Sci. U.S.A. 106, 2194-2199
10. Zhang, Q., Ragnauth, C.D., Skepper, J.N., Worth, N.F., Warren, D.T., Roberts, R.G., Weissberg, P.L., Ellis, J.A. and Shanahan, C.M. (2005) Nesprin-2 is a multi-isomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle. J. Cell Sci. 118, 673-687 (Pubitemid 40372577)
11. Padmakumar, V.C., Libotte, T., Lu, W., Zaim, H., Abraham, S., Noegel, A.A., Gotzmann, J., Foisner, R. and Karakesisoglou, I. (2005) The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J. Cell Sci. 118, 3419-3430 (Pubitemid 41246097)
12. Ketema, M., Wilhelmsen, K., Kuikman, I., Janssen, H., Hodzic, D. and Sonnenberg, A. (2007) Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin. J. Cell Sci. 120, 3384-3394 (Pubitemid 350028346)
13. Stewart-Hutchinson, P.J., Hale, C.M., Wirtz, D. and Hodzic, D. (2008) Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp. Cell Res. 314, 1892-1905
14. Ostlund, C., Folker, E.S., Choi, J.C., Gomes, E.R., Gundersen, G.G. and Worman, H.J. (2009) Dynamics and molecular interactions of linker of nucleoskeleton and cytoskeleton (LINC) complex proteins. J. Cell Sci. 122, 4099-4108
15. Starr, D.A. and Han, M. (2002) Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 298, 406-409 (Pubitemid 35176347)
16. Malone, C.J., Fixsen, W.D., Horvitz, H.R. and Han, M. (1999) UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development 126, 3171-3181 (Pubitemid 29378180)
17. Schneider, M., Lu, W., Neumann, S., Brachner, A., Gotzmann, J., Noegel, A.A. and Karakesisoglou, I. (2011) Molecular mechanisms of centrosome and cytoskeleton anchorage at the nuclear envelope. Cell. Mol. Life Sci. 68, 1593-1610
18. Hale, C.M., Shrestha, A.L., Khatau, S.B., Stewart-Hutchinson, P.J., Hernandez, L., Stewart, C.L., Hodzic, D. and Wirtz, D. (2008) Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models. Biophys. J. 95, 5462-5475
19. Lee, J.S., Hale, C.M., Panorchan, P., Khatau, S.B., George, J.P., Tseng, Y., Stewart, C.L., Hodzic, D. and Wirtz, D. (2007) Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys. J. 93, 2542-2552 (Pubitemid 47511153)
20. Zhang, Q., Bethmann, C., Worth, N.F., Davies, J.D., Wasner, C., Feuer, A., Ragnauth, C.D., Yi, Q., Mellad, J.A., Warren, D.T. et al. (2007) Nesprin-1 and -2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum. Mol. Genet. 16, 2816-2833 (Pubitemid 350048381)
21. Chancellor, T.J., Lee, J., Thodeti, C.K. and Lele, T. (2010) Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys. J. 99, 115-123
22. Luxton, G.W., Gomes, E.R., Folker, E.S., Vintinner, E. and Gundersen, G.G. (2010) Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science 329, 956-959
23. Grady, R.M., Starr, D.A., Ackerman, G.L., Sanes, J.R. and Han, M. (2005) Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc. Natl. Acad. Sci. U.S.A. 102, 4359-4364 (Pubitemid 40397116)
24. Zhang, X., Xu, R., Zhu, B., Yang, X., Ding, X., Duan, S., Xu, T., Zhuang, Y. and Han, M. (2007) Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 134, 901-908 (Pubitemid 46795681)
25. Lei, K., Zhang, X., Ding, X., Guo, X., Chen, M., Zhu, B., Xu, T., Zhuang, Y., Xu, R. and Han, M. (2009) SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice. Proc. Natl. Acad. Sci. U.S.A. 106, 10207-10212
26. Mejat, A., Decostre, V., Li, J., Renou, L., Kesari, A., Hantai, D., Stewart, C.L., Xiao, X., Hoffman, E., Bonne, G. and Misteli, T. (2009) Lamin A/C-mediated neuromuscular junction defects in Emery-Dreifuss muscular dystrophy. J. Cell Biol. 184, 31-44
27. Friedl, P., Wolf, K. and Lammerding, J. (2011) Nuclear mechanics during cell migration. Curr. Opin. Cell Biol. 23, 55-64
28. Lombardi, M.L., Jaalouk, D.E., Shanahan, C.M., Burke, B., Roux, K.J. and Lammerding, J. (2011) 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, 26743-26753
29. Jaalouk, D.E. and Lammerding, J. (2009) Mechanotransduction gone awry. Nat. Rev. Mol. Cell Biol. 10, 63-73
30. - /- cells is caused by defective nucleo-cytoskeletal integrity: implications for the development of laminopathies. Hum. Mol. Genet. 13, 2567-2580
31. Lammerding, J., Schulze, P.C., Takahashi, T., Kozlov, S., Sullivan, T., Kamm, R.D., Stewart, C.L. and Lee, R.T. (2004) Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Invest. 113, 370-378 (Pubitemid 38544181)
32. Lammerding, J., Hsiao, J., Schulze, P.C., Kozlov, S., Stewart, C.L. and Lee, R.T. (2005) Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J. Cell Biol. 170, 781-791 (Pubitemid 41242110)
33. Gonzalez, J.M., Navarro-Puche, A., Casar, B., Crespo, P. and Andres, V. (2008) Fast regulation of AP-1 activity through interaction of lamin A/C, ERK1/2, and c-Fos at the nuclear envelope. J. Cell Biol. 183, 653-666
34. Brosig, M., Ferralli, J., Gelman, L., Chiquet, M. and Chiquet-Ehrismann, R. (2010) Interfering with the connection between the nucleus and the cytoskeleton affects nuclear rotation, mechanotransduction and myogenesis. Int. J. Biochem. Cell Biol. 42, 1717-1728
35. Roux, K.J. and Burke, B. (2007) Nuclear envelope defects in muscular dystrophy. Biochim. Biophys. Acta 1772, 118-127 (Pubitemid 46123912)
36. Emery, A.E. (2002) The muscular dystrophies. Lancet 359, 687-695
37. Bione, S., Maestrini, E., Rivella, S., Mancini, M., Regis, S., Romeo, G. and Toniolo, D. (1994) Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat. Genet. 8, 323-327 (Pubitemid 24375595)
38. Bonne, G., Di Barletta, M.R., Varnous, S., Becane, H.M., Hammouda, E.H., Merlini, L., Muntoni, F., Greenberg, C.R., Gary, F., Urtizberea, J.A. et al. (1999) Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet. 21, 285-288 (Pubitemid 29124935)
39. Fatkin, D., MacRae, C., Sasaki, T., Wolff, M.R., Porcu, M., Frenneaux, M., Atherton, J., Vidaillet, Jr, H.J., Spudich, S., De Girolami, U. et al. (1999) Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease. N. Engl. J. Med. 341, 1715-1724
40. Slominsky, P.A., Markova, E.D., Shadrina, M.I., Illarioshkin, S.N., Miklina, N.I., Limborska, S.A. and Ivanova-Smolenskaya, I.A. (1999) A common 3-bp deletion in the DYT1 gene in Russian families with early-onset torsion dystonia. Hum. Mutat. 14, 269
41. Folker, E.S., Ostlund, C., Luxton, G.W., Worman, H.J. and Gundersen, G.G. (2011) Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement. Proc. Natl. Acad. Sci. U.S.A. 108, 131-136
42. Worman, H.J., Fong, L.G., Muchir, A. and Young, S.G. (2009) Laminopathies and the long strange trip from basic cell biology to therapy. J. Clin. Invest. 119, 1825-1836
43. Dawe, H.R., Adams, M., Wheway, G., Szymanska, K., Logan, C.V., Noegel, A.A., Gull, K. and Johnson, C.A. (2009) Nesprin-2 interacts with meckelin and mediates ciliogenesis via remodelling of the actin cytoskeleton. J. Cell Sci. 122, 2716-2726
44. Dupre, N., Bouchard, J.P., Gros-Louis, F. and Rouleau, G.A. (2007) Mutations in SYNE-1 lead to a newly discovered form of autosomal recessive cerebellar ataxia. Med. Sci. (Paris) 23, 261-262 (Pubitemid 46472649)
45. Padiath, Q.S., Saigoh, K., Schiffmann, R., Asahara, H., Yamada, T., Koeppen, A., Hogan, K., Ptacek, L.J. and Fu, Y.H. (2006) Lamin B1 duplications cause autosomal dominant leukodystrophy. Nat. Genet. 38, 1114-1123 (Pubitemid 44470356)
46. Ji, J.Y., Lee, R.T., Vergnes, L., Fong, L.G., Stewart, C.L., Reue, K., Young, S.G., Zhang, Q., Shanahan, C.M. and Lammerding, J. (2007) Cell nuclei spin in the absence of lamin B1. J. Biol. Chem. 282, 20015-20026 (Pubitemid 47100106)
47. Coffinier, C., Chang, S.Y., Nobumori, C., Tu, Y., Farber, E.A., Toth, J.I., Fong, L.G. and Young, S.G. (2010) Abnormal development of the cerebral cortex and cerebellum in the setting of lamin B2 deficiency. Proc. Natl. Acad. Sci. U.S.A. 107, 5076-5081
48. Yu, J., Lei, K., Zhou, M., Craft, C.M., Xu, G., Xu, T., Zhuang, Y., Xu, R. and Han, M. (2011) KASH protein Syne-2/Nesprin-2 and SUN proteins SUN1/2 mediate nuclear migration during mammalian retinal development. Hum. Mol. Genet. 20, 1061-1073