Nesprins anchor kinesin-1 motors to the nucleus to drive nuclear distribution in muscle cells

Development (Cambridge)

Volumn 142, Issue 1, 2015, Pages 218-228

  Wilson, Meredith H ^a   Holzbaur, Erika L F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cargo adaptor; Kinesin 1; Mouse; Muscle development; Nesprin; Nuclear positioning

Indexed keywords

KINESIN 1; MOLECULAR MOTOR; ACTIN BINDING PROTEIN; KIF5B PROTEIN, HUMAN; KIF5B PROTEIN, MOUSE; KINESIN; TRYPTOPHAN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL SPECIFICITY; CELL TYPE; MICROTUBULE; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOTUBE; NONHUMAN; PROTEIN MOTIF; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CHEMISTRY; CONSERVED SEQUENCE; CYTOLOGY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; SKELETAL MUSCLE CELL;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELL NUCLEUS; CONSERVED SEQUENCE; HUMANS; KINESIN; MICE; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUSCLE CELLS; MUSCLE FIBERS, SKELETAL; MUTATION; NUCLEAR ENVELOPE; TRYPTOPHAN;

EID: 84918509860     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.114769     Document Type: Article

References (53)

1. Aoyama, T., Hata, S., Nakao, T., Tanigawa, Y., Oka, C. and Kawaichi, M. (2009). Cayman ataxia protein caytaxin is transported by kinesin along neurites through binding to kinesin light chains. J. Cell Sci. 122, 4177-4185.
2. Banerjee, I., Zhang, J., Moore-Morris, T., Pfeiffer, E., Buchholz, K. S., Liu, A., Ouyang, K., Stroud, M. J., Gerace, L., Evans, S. M. et al. (2014). Targeted ablation of nesprin-1 and nesprin-2 from murine myocardium results in cardiomyopathy, altered nuclear morphology and inhibition of the biomechanical gene response. PLoS Genet. 10, pe1004114.
3. Barlan, K., Lu, W. and Gelfand, V. I. (2013). The microtubule-binding protein ensconsin is an essential cofactor of kinesin-1. Curr. Biol. 23, 317-322.
4. Bruusgaard, J. C., Liestøl, K., Ekmark, M., Kollstad, K. and Gundersen, K. (2003). Number and spatial distribution of nuclei in the muscle fibres of normal mice studied in vivo. J. Physiol. 551, 467-478.
5. Cadot, B., Gache, V., Vasyutina, E., Falcone, S., Birchmeier, C. and Gomes, E. R. (2012). Nuclear movement during myotube formation is microtubule and dynein dependent and is regulated by Cdc42, Par6 and Par3. EMBO Rep. 13, 741-749.
6. Cai, Y., Singh, B. B., Aslanukov, A., Zhao, H. and Ferreira, P. A. (2001). The docking of kinesins, KIF5B and KIF5C, to Ran-binding protein 2 (RanBP2) is mediated via a novel RanBP2 domain. J. Biol. Chem. 276, 41594-41602.
7. Capers, C. R. (1960). Multinucleation of skeletal muscle in vitro. J. Biophys. Biochem. Cytol. 7, 559-565.
8. Chapman, M. A., Zhang, J., Banerjee, I., Guo, L. T., Zhang, Z., Shelton, G. D., Ouyang, K., Lieber, R. L. and Chen, J. (2014). Disruption of both nesprin-1 and desmin results in nuclear anchorage defects and fibrosis in skeletal muscle. Hum. Mol. Genet. 23, 5879-5892.
9. Cho, K.-i., Cai, Y., Yi, H., Yeh, A., Aslanukov, A. and Ferreira, P. A. (2007). Association of the kinesin-binding domain of RanBP2 to KIF5B and KIF5C determines mitochondria localization and function. Traffic 8, 1722-1735.
10. Clackson, T., Yang, W., Rozamus, L. W., Hatada, M., Amara, J. F., Rollins, C. T., Stevenson, L. F., Magari, S. R., Wood, S. A., Courage, N. L. et al. (1998). Redesigning an FKBP-ligand interface to generate chemical dimerizers with novel specificity. Proc. Natl. Acad. Sci. USA 95, 10437-10442.
11. Dodding, M. P., Mitter, R., Humphries, A. C. and Way, M. (2011). A kinesin-1 binding motif in vaccinia virus that is widespread throughout the human genome. EMBO J. 30, 4523-4538.
12. Duong, N. T., Morris, G. E., Lam, L. T., Zhang, Q., Sewry, C. A., Shanahan, C. M. and Holt, I. (2014). Nesprins: tissue-specific expression of epsilon and other short isoforms. PLoS ONE 9, e94380.
13. Englander, L. L. and Rubin, L. L. (1987). Acetylcholine receptor clustering and nuclear movement in muscle fibers in culture. J. Cell Biol. 104, 87-95.
14. Falcone, S., Roman, W., Hnia, K., Gache, V., Didier, N., Lainé, J., Auradé, F., Marty, I., Nishino, I., Charlet-Berguerand, N. et al. (2014). N-WASP is required for Amphiphysin-2/BIN1-dependent nuclear positioning and triad organization in skeletal muscle and is involved in the pathophysiology of centronuclear myopathy. EMBO Mol. Med. 6, 1455-1475.
15. Folker, E. S., Schulman, V. K. and Baylies, M. K. (2012). Muscle length and myonuclear position are independently regulated by distinct Dynein pathways. Development 139, 3827-3837.
16. Folker, E. S., Schulman, V. K. and Baylies, M. K. (2014). Translocating myonuclei have distinct leading and lagging edges that require kinesin and dynein. Development 141, 355-366.
17. Fridolfsson, H. N. and Starr, D. A. (2010). Kinesin-1 and dynein at the nuclear envelope mediate the bidirectional migrations of nuclei. J. Cell. Biol. 191, 115-128.
18. 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. USA 102, 4359-4364.
19. Gundersen, G. G. and Worman, H. J. (2013). Nuclear positioning. Cell 152, 1376-1389.
20. Horn, H. F., Brownstein, Z., Lenz, D. R., Shivatzki, S., Dror, A. A., Dagan-Rosenfeld, O., Friedman, L. M., Roux, K. J., Kozlov, S., Jeang, K. T. et al. (2013). The LINC complex is essential for hearing. J. Clin. Invest. 123, 740-750.
21. Jamison, D. K., Driver, J.W., Rogers, A. R., Constantinou, P. E. and Diehl, M. R. (2010). Two kinesins transport cargo primarily via the action of one motor: implications for intracellular transport. Biophys. J. 99, 2967-2977.
22. Kaan, H. Y. K., Hackney, D. D. and Kozielski, F. (2011). The structure of the kinesin-1 motor-tail complex reveals the mechanism of autoinhibition. Science 333, 883-885.
23. Kapitein, L. C., Schlager, M. A., Kuijpers, M., Wulf, P. S., van Spronsen, M., MacKintosh, F. C. and Hoogenraad, C. C. (2010a). Mixed microtubules steer dynein-driven cargo transport into dendrites. Curr. Biol. 20, 290-299.
24. Kapitein, L. C., Schlager, M. A., van der Zwan, W. A., Wulf, P. S., Keijzer, N. and Hoogenraad, C. C. (2010b). Probing intracellular motor protein activity using an inducible cargo trafficking assay. Biophys. J. 99, 2143-2152.
25. Konecna, A., Frischknecht, R., Kinter, J., Ludwig, A., Steuble, M., Meskenaite, V., Indermühle, M., Engel, M., Cen, C., Mateos, J.-M. et al. (2006). Calsyntenin-1 docks vesicular cargo to kinesin-1. Mol. Biol. Cell 17, 3651-3663.
26. Mattioli, E., Columbaro, M., Capanni, C., Maraldi, N. M., Cenni, V., Scotlandi, K., Marino, M. T., Merlini, L., Squarzoni, S. and Lattanzi, G. (2011). Prelamin A-mediated recruitment of SUN1 to the nuclear envelope directs nuclear positioning in human muscle. Cell Death Differ. 18, 1305-1315.
27. Metzger, T., Gache, V., Xu, M., Cadot, B., Folker, E. S., Richardson, B. E., Gomes, E. R. and Baylies, M. K. (2012). MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function. Nature 484, 120-124.
28. Meyerzon, M., Fridolfsson, H. N., Ly, N., McNally, F. J. and Starr, D. A. (2009). UNC-83 is a nuclear-specific cargo adaptor for kinesin-1-mediated nuclear migration. Development 136, 2725-2733.
29. Mislow, J. M. K., Holaska, J. M., Kim, M. S., Lee, K. K., Segura-Totten, M., Wilson, K. L. and McNally, E. M. (2002). Nesprin-1alpha self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett. 525, 135-140.
30. Pernigo, S., Lamprecht, A., Steiner, R. A. and Dodding, M. P. (2013). Structural basis for kinesin-1:cargo recognition. Science 340, 356-359.
31. Puckelwartz, M. J., Kessler, E., Zhang, Y., Hodzic, D., Randles, K. N., Morris, G., Earley, J. U., Hadhazy, M., Holaska, J. M., Mewborn, S. K. et al. (2009). Disruption of nesprin-1 produces an Emery Dreifuss muscular dystrophy-like phenotype in mice. Hum. Mol. Genet. 18, 607-620.
32. Rajgor, D. and Shanahan, C. M. (2013). Nesprins: from the nuclear envelope and beyond. Expert Rev. Mol. Med. 15, e5.
33. Randles, K. N., Lam, L. T., Sewry, C. A., Puckelwartz, M., Furling, D., Wehnert, M., McNally, E. M. and Morris, G. E. (2010). Nesprins, but not sun proteins, switch isoforms at the nuclear envelope during muscle development. Dev. Dyn. 239, 998-1009.
34. Razafsky, D. S., Ward, C. L., Kolb, T. and Hodzic, D. (2013). Developmental regulation of linkers of the nucleoskeleton to the cytoskeleton during mouse postnatal retinogenesis. Nucleus 4, 399-409.
35. Romero, N. B. (2010). Centronuclear myopathies: a widening concept. Neuromuscul. Disord. 20, 223-228.
36. 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 kinesinmediated cell polarization. Proc. Natl. Acad. Sci. USA 106, 2194-2199.
37. Schmidt, M. R., Maritzen, T., Kukhtina, V., Higman, V. A., Doglio, L., Barak, N. N., Strauss, H., Oschkinat, H., Dotti, C. G. and Haucke, V. (2009). Regulation of endosomal membrane traffic by a Gadkin/AP-1/kinesin KIF5 complex. Proc. Natl. Acad. Sci. USA 106, 15344-15349.
38. 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.
39. Shubeita, G. T., Tran, S. L., Xu, J., Vershinin, M., Cermelli, S., Cotton, S. L., Welte, M. A. and Gross, S. P. (2008). Consequences of motor copy number on the intracellular transport of kinesin-1-driven lipid droplets. Cell 135, 1098-1107.
40. Simpson, J. G. and Roberts, R. G. (2008). Patterns of evolutionary conservation in the nesprin genes highlight probable functionally important protein domains and isoforms. Biochem. Soc. Trans. 36, 1359-1367.
41. Spencer, D. M., Wandless, T. J., Schreiber, S. L. and Crabtree, G. R. (1993). Controlling signal transduction with synthetic ligands. Science 262, 1019-1024.
42. Splinter, D., Tanenbaum, M. E., Lindqvist, A., Jaarsma, D., Flotho, A., Yu, K. L., Grigoriev, I., Engelsma, D., Haasdijk, E. D., Keijzer, N. et al. (2010). Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol. 8, e1000350.
43. 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.
44. Verhey, K. J. and Hammond, J. W. (2009). Traffic control: regulation of kinesin motors. Nat. Rev. Mol. Cell Biol. 10, 765-777.
45. Verhey, K. J., Lizotte, D. L., Abramson, T., Barenboim, L., Schnapp, B. J. and Rapoport, T. A. (1998). Light chain-dependent regulation of Kinesin’s interaction with microtubules. J. Cell Biol. 143, 1053-1066.
46. Wang, Z., Cui, J., Wong, W. M., Li, X., Xue, W., Lin, R., Wang, J., Wang, P., Tanner, J. A., Cheah, K. S. E. et al. (2013a). Kif5b controls the localization of myofibril components for their assembly and linkage to the myotendinous junctions. Development 140, 617-626.
47. Wang, Z., Xue, W., Li, X., Lin, R., Cui, J. and Huang, J.-D. (2013b). Dissect Kif5b in nuclear positioning during myogenesis: the light chain binding domain and the autoinhibitory peptide are both indispensable. Biochem. Biophys. Res. Commun. 432, 242-247.
48. Wheeler, M. A., Davies, J. D., Zhang, Q., Emerson, L. J., Hunt, J., Shanahan, C. M. and Ellis, J. A. (2007). Distinct functional domains in nesprin-1alpha and nesprin-2beta bind directly to emerin and both interactions are disrupted in X-linked Emery-Dreifuss muscular dystrophy. Exp. Cell Res. 313, 2845-2857.
49. Wilson, M. H. and Holzbaur, E. L. F. (2012). Opposing microtubule motors drive robust nuclear dynamics in developing muscle cells. J. Cell Sci. 125, 4158-4169.
50. 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. (2007a). 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.
51. Zhang, X., Xu, R., Zhu, B., Yang, X., Ding, X., Duan, S., Xu, T., Zhuang, Y. and Han, M. (2007b). Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 134, 901-908.
52. Zhang, J., Felder, A., Liu, Y., Guo, L. T., Lange, S., Dalton, N. D., Gu, Y., Peterson, K. L., Mizisin, A. P., Shelton, G. D. et al. (2010). Nesprin 1 is critical for nuclear positioning and anchorage. Hum. Mol. Genet. 19, 329-341.
53. Zhong, Z., Chang, S. A., Kalinowski, A., Wilson, K. L. and Dahl, K. N. (2010). Stabilization of the spectrin-like domains of nesprin-1alpha by the evolutionarily conserved “adaptive” domain. Cell. Mol. Bioeng. 3, 139-150.