Making the LINC: SUN and KASH protein interactions

Biological Chemistry

Volumn 396, Issue 4, 2015, Pages 295-310

  Kim, Dae In ^a   Kc, Birendra ^a,b   Roux, Kyle J ^a,b  

^a SANFORD RESEARCH   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

cytoskeleton; KASH; LINC complex; nuclear envelope; nucleus; SUN

Indexed keywords

ACTIN; BINDING PROTEIN; CYTOPLASM PROTEIN; CYTOSKELETON PROTEIN; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KASH PROTEIN; KU ANTIGEN; LINKER OF NUCLEOSKELETON AND CYTOSKELETON COMPLEX PROTEIN; MEMBRANE PROTEIN; PLECTIN; PROTEIN BQT1; PROTEIN BQT2; PROTEIN CSM4; PROTEIN HTZ1; PROTEIN KLAROID; PROTEIN KLARSICHT; PROTEIN KMS1; PROTEIN KMS2; PROTEIN KU80; PROTEIN MPS2; PROTEIN MPS3; PROTEIN MSP 300; PROTEIN NDJ1; PROTEIN SAD1; PROTEIN SPAG4; PROTEIN SUN1; REPLICATION FACTOR C; SUN PROTEIN; TELOMERASE; UNCLASSIFIED DRUG; NUCLEAR PROTEIN;

ARABIDOPSIS THALIANA; CAENORHABDITIS ELEGANS; CELL FUNCTION; CELL NUCLEUS MEMBRANE; DROSOPHILA MELANOGASTER; HUMAN; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; STOICHIOMETRY; VERTEBRATE; ZEBRA FISH; ANIMAL; CELL NUCLEUS MATRIX; CHEMISTRY; CYTOSKELETON; METABOLISM;

ANIMALS; CYTOSKELETON; HUMANS; NUCLEAR MATRIX; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPS;

EID: 84924912942     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0267     Document Type: Review

References (132)

1. Anno, T., Sakamoto, N., and Sato, M. (2012). Role of nesprin-1 in nuclear deformation in endothelial cells under static and uniaxial stretching conditions. Biochem. Biophys. Res. Commun. 424, 94-99.
2. Antoniacci, L.M., Kenna, M.A., Uetz, P., Fields, S., and Skibbens, R.V. (2004). The spindle pole body assembly component mps3p/ nep98p functions in sister chromatid cohesion. J. Biol. Chem. 279, 49542-49550.
3. Antoniacci, L.M., Kenna, M.A., and Skibbens, R.V. (2007). The nuclear envelope and spindle pole body-associated Mps3 protein bind telomere regulators and function in telomere clustering. Cell Cycle 6, 75-79.
4. Attali, R., Warwar, N., Israel, A., Gurt, I., McNally, E., Puckelwartz, M., Glick, B., Nevo, Y., Ben-Neriah, Z., and Melki, J. (2009). Mutation of SYNE-1, encoding an essential component of the nuclear lamina, is responsible for autosomal recessive arthrogryposis. Hum. Mol. Genet. 18, 3462-3469.
5. 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, e1004114.
6. Behrens, T.W., Kearns, G.M., Rivard, J.J., Bernstein, H.D., Yewdell, J.W., and Staudt, L.M. (1996). Carboxyl-terminal targeting and novel post-translational processing of JAW1, a lymphoid protein of the endoplasmic reticulum. J. Biol. Chem. 271, 23528-23534.
7. Borrego-Pinto, J., Jegou, T., Osorio, D.S., Aurade, F., Gorjanacz, M., Koch, B., Mattaj, I.W., and Gomes, E.R. (2012). Samp1 is a component of TAN lines and is required for nuclear movement. J. Cell Sci. 125, 1099-1105.
8. Bupp, J.M., Martin, A.E., Stensrud, E.S., and Jaspersen, S.L. (2007). Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3. J. Cell Biol. 179, 845-854.
9. Chan, J.N., Poon, B.P., Salvi, J., Olsen, J.B., Emili, A., and Mekhail, K. (2011). Perinuclear cohibin complexes maintain replicative life span via roles at distinct silent chromatin domains. Dev. Cell 20, 867-879.
10. Chen, C.Y., Chi, Y.H., Mutalif, R.A., Starost, M.F., Myers, T.G., Anderson, S.A., Stewart, C.L., and Jeang, K.T. (2012). Accumulation of the inner nuclear envelope protein Sun1 is pathogenic in progeric and dystrophic laminopathies. Cell 149, 565-577.
11. Chi, Y.H., Haller, K., Peloponese, J.M., Jr., and Jeang, K.T. (2007). Histone acetyltransferase hALP and nuclear membrane protein hsSUN1 function in de-condensation of mitotic chromosomes. J. Biol. Chem. 282, 27447-27458.
12. Chikashige, Y., Tsutsumi, C., Yamane, M., Okamasa, K., Haraguchi, T., and Hiraoka, Y. (2006). Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125, 59-69.
13. Conrad, M.N., Lee, C.Y., Wilkerson, J.L., and Dresser, M.E. (2007). MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 104, 8863-8868.
14. Conrad, M.N., Lee, C.Y., Chao, G., Shinohara, M., Kosaka, H., Shinohara, A., Conchello, J.A., and Dresser, M.E. (2008). Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133, 1175-1187.
15. 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.
16. Ding, X., Xu, R., Yu, J., Xu, T., Zhuang, Y., and Han, M. (2007). SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell 12, 863-872.
17. Elhanany-Tamir, H., Yu, Y.V., Shnayder, M., Jain, A., Welte, M., and Volk, T. (2012). Organelle positioning in muscles requires cooperation between two KASH proteins and microtubules. J. Cell Biol. 198, 833-846.
18. Fischer-Vize, J.A. and Mosley, K.L. (1994). Marbles mutants: uncoupling cell determination and nuclear migration in the developing Drosophila eye. Development 120, 2609-2618.
19. Fischer, J.A., Acosta, S., Kenny, A., Cater, C., Robinson, C., and Hook, J. (2004). Drosophila klarsicht has distinct subcellular localization domains for nuclear envelope and microtubule localization in the eye. Genetics 168, 1385-1393.
20. Fridolfsson, H.N., Ly, N., Meyerzon, M., and Starr, D.A. (2010). UNC-83 coordinates kinesin-1 and dynein activities at the nuclear envelope during nuclear migration. Dev. Biol. 338, 237-250.
21. Friederichs, J.M., Ghosh, S., Smoyer, C.J., McCroskey, S., Miller, B.D., Weaver, K.J., Delventhal, K.M., Unruh, J., Slaughter, B.D., and Jaspersen, S.L. (2011). The SUN protein Mps3 is required for spindle pole body insertion into the nuclear membrane and nuclear envelope homeostasis. PLoS Genet. 7, e1002365.
22. Geerts, D., Fontao, L., Nievers, M.G., Schaapveld, R.Q., Purkis, P.E., Wheeler, G.N., Lane, E.B., Leigh, I.M., and Sonnenberg, A. (1999). Binding of integrin-6-4 to plectin prevents plectin association with F-actin but does not interfere with intermediate filament binding. J. Cell Biol. 147, 417-434.
23. Ghosh, S., Gardner, J.M., Smoyer, C.J., Friederichs, J.M., Unruh, J.R., Slaughter, B.D., Alexander, R., Chisholm, R.D., Lee, K.K., Workman, J.L., et al. (2012). Acetylation of the SUN protein Mps3 by Eco1 regulates its function in nuclear organization. Mol. Biol. Cell 23, 2546-2559.
24. Gob, E., Schmitt, J., Benavente, R., and Alsheimer, M. (2010). Mammalian sperm head formation involves different polarization of two novel LINC complexes. PLoS One 5, e12072.
25. Gomes, E.R., Jani, S., and Gundersen, G.G. (2005). Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121, 451-463.
26. Gough, L.L., Fan, J., Chu, S., Winnick, S., and Beck, K.A. (2003). Golgi localization of Syne-1. Mol. Biol. Cell 14, 2410-2424.
27. Graumann, K. (2014). Evidence for LINC1-SUN associations at the plant nuclear periphery. PLoS One 9, e93406.
28. Graumann, K., Runions, J., and Evans, D.E. (2010). Characterization of SUN-domain proteins at the higher plant nuclear envelope. Plant J. 61, 134-144.
29. Gros-Louis, F., Dupre, N., Dion, P., Fox, M.A., Laurent, S., Verreault, S., Sanes, J.R., Bouchard, J.P., and Rouleau, G.A. (2007). Mutations in SYNE1 lead to a newly discovered form of autosomal recessive cerebellar ataxia. Nat. Genet. 39, 80-85.
30. Guilluy, C., Osborne, L.D., Van Landeghem, L., Sharek, L., Superfine, R., Garcia-Mata, R., and Burridge, K. (2014). Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat. Cell Biol. 16, 376-381.
31. Haas, J., Lemoncelli, A., Morozov, C., Franke, K., Dominder, J., and Antoniacci, L.M. (2012). Physical links between the nuclear envelope protein Mps3, three alternate replication factor C complexes, and a variant histone in Saccharomyces cerevisiae. DNA Cell Biol. 31, 917-924.
32. 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.
33. Haque, F., Mazzeo, D., Patel, J.T., Smallwood, D.T., Ellis, J.A., Shanahan, C.M., and Shackleton, S. (2010). Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes. J. Biol. Chem. 285, 3487-3498.
34. Hiraoka, Y., Maekawa, H., Asakawa, H., Chikashige, Y., Kojidani, T., Osakada, H., Matsuda, A., and Haraguchi, T. (2011). Inner nuclear membrane protein Ima1 is dispensable for intranuclear positioning of centromeres. Genes Cells 16, 1000-1011.
35. Hodzic, D.M., Yeater, D.B., Bengtsson, L., Otto, H., and Stahl, P.D. (2004). Sun2 is a novel mammalian inner nuclear membrane protein. J. Biol. Chem. 279, 25805-25812.
36. Horigome, C., Okada, T., Shimazu, K., Gasser, S.M., and Mizuta, K. (2011). Ribosome biogenesis factors bind a nuclear envelope SUN domain protein to cluster yeast telomeres. EMBO J. 30, 3799-3811.
37. 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. (2013a). The LINC complex is essential for hearing. J. Clin. Invest. 123, 740-750.
38. Horn, H.F., Kim, D.I., Wright, G.D., Wong, E.S., Stewart, C.L., Burke, B., and Roux, K.J. (2013b). A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J. Cell Biol. 202, 1023-1039.
39. Hou, H., Zhou, Z., Wang, Y., Wang, J., Kallgren, S.P., Kurchuk, T., Miller, E.A., Chang, F., and Jia, S. (2012). Csi1 links centromeres to the nuclear envelope for centromere clustering. J. Cell Biol. 199, 735-744.
40. Jafferali, M.H., Vijayaraghavan, B., Figueroa, R.A., Crafoord, E., Gudise, S., Larsson, V.J., and Hallberg, E. (2014). MCLIP, an effective method to detect interactions of transmembrane proteins of the nuclear envelope in live cells. Biochim. Biophys. Acta 1838, 2399-2403.
41. Jungwirth, M.T., Kumar, D., Jeong, D.Y., and Goodchild, R.E. (2011). The nuclear envelope localization of DYT1 dystonia torsin A-E requires the SUN1 LINC complex component. BMC Cell Biol. 12, 24.
42. Kennedy, C., Sebire, K., de Kretser, D.M., and O'Bryan, M.K. (2004). Human sperm associated antigen 4 (SPAG4) is a potential cancer marker. Cell Tissue Res. 315, 279-283.
43. 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.
44. Ketema, M., Kreft, M., Secades, P., Janssen, H., and Sonnenberg, A. (2013). Nesprin-3 connects plectin and vimentin to the nuclear envelope of Sertoli cells but is not required for Sertoli cell function in spermatogenesis. Mol. Biol. Cell 24, 2454-2466.
45. King, M.C., Drivas, T.G., and Blobel, G. (2008). A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 134, 427-438.
46. Kosaka, H., Shinohara, M., and Shinohara, A. (2008). Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination. PLoS Genet. 4, e1000196.
47. Koszul, R., Kim, K.P., Prentiss, M., Kleckner, N., and Kameoka, S. (2008). Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133, 1188-1201.
48. Kracklauer, M.P., Banks, S.M., Xie, X., Wu, Y., and Fischer, J.A. (2007). 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.
49. Kracklauer, M.P., Wiora, H.M., Deery, W.J., Chen, X., Bolival, B., Jr., Romanowicz, D., Simonette, R.A., Fuller, M.T., Fischer, J.A., and Beckingham, K.M. (2010). The Drosophila SUN protein Spag4 cooperates with the coiled-coil protein Yuri Gagarin to maintain association of the basal body and spermatid nucleus. J. Cell Sci. 123, 2763-2772.
50. Le Masson, I., Saveanu, C., Chevalier, A., Namane, A., Gobin, R., Fromont-Racine, M., Jacquier, A., and Mann, C. (2002). Spc24 interacts with Mps2 and is required for chromosome segregation, but is not implicated in spindle pole body duplication. Mol. Microbiol. 43, 1431-1443.
51. Lee, K.K., Starr, D., Cohen, M., Liu, J., Han, M., Wilson, K.L., and Gruenbaum, Y. (2002). Lamin-dependent localization of UNC-84, a protein required for nuclear migration in Caenorhabditis elegans. Mol. Biol. Cell. 13, 892-901.
52. 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. USA 106, 10207-10212.
53. Lei, K., Zhu, X., Xu, R., Shao, C., Xu, T., Zhuang, Y., and Han, M. (2012). Inner nuclear envelope proteins SUN1 and SUN2 play a prominent role in the DNA damage response. Curr. Biol. 22, 1609-1615.
54. Libotte, T., Zaim, H., Abraham, S., Padmakumar, V.C., Schneider, M., Lu, W., Munck, M., Hutchison, C., Wehnert, M., Fahrenkrog, B., et al. (2005). Lamin A/C-dependent localization of Nesprin-2, a giant scaffolder at the nuclear envelope. Mol. Biol. Cell. 16, 3411-3424.
55. Lindeman, R.E. and Pelegri, F. (2012). Localized products of futile cycle/lrmp promote centrosome-nucleus attachment in the zebrafish zygote. Curr. Biol. 22, 843-851.
56. Link, J., Leubner, M., Schmitt, J., Gob, E., Benavente, R., Jeang, K.T., Xu, R., and Alsheimer, M. (2014). Analysis of meiosis in SUN1 deficient mice reveals a distinct role of SUN2 in mammalian meiotic LINC complex formation and function. PLoS Genet. 10, e1004099.
57. Liu, Q., Pante, N., Misteli, T., Elsagga, M., Crisp, M., Hodzic, D., Burke, B., and Roux, K.J. (2007). Functional association of Sun1 with nuclear pore complexes. J. Cell Biol. 178, 785-798.
58. Lombardi, M.L. and Lammerding, J. (2010). Altered mechanical properties of the nucleus in disease. Methods Cell Biol. 98, 121-141.
59. 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.
60. MacQueen, A.J., Phillips, C.M., Bhalla, N., Weiser, P., Villeneuve, A.M., and Dernburg, A.F. (2005). Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123, 1037-1050.
61. 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.
62. Malone, C.J., Misner, L., Le Bot, N., Tsai, M.C., Campbell, J.M., Ahringer, J., and White, J.G. (2003). The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115, 825-836.
63. 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. USA 94, 849-854.
64. McGee, M.D., Stagljar, I., and Starr, D.A. (2009). KDP-1 is a nuclear envelope KASH protein required for cell-cycle progression. J. Cell Sci. 122, 2895-2905.
65. Meier, I., Zhou, X., Brkljacic, J., Rose, A., Zhao, Q., and Xu, X.M. (2010). Targeting proteins to the plant nuclear envelope. Biochem. Soc. Trans. 38, 733-740.
66. Meinke, P., Mattioli, E., Haque, F., Antoku, S., Columbaro, M., Straatman, K.R., Worman, H.J., Gundersen, G.G., Lattanzi, G., Wehnert, M., et al. (2014). Muscular dystrophy-associated SUN1 and SUN2 variants disrupt nuclear-cytoskeletal connections and myonuclear organization. PLoS Genet. 10, e1004605.
67. 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.
68. Miki, F., Kurabayashi, A., Tange, Y., Okazaki, K., Shimanuki, M., and Niwa, O. (2004). Two-hybrid search for proteins that interact with Sad1 and Kms1, two membrane-bound components of the spindle pole body in fission yeast. Mol. Genet. Genomics 270, 449-461.
69. Mislow, J.M., Holaska, J.M., Kim, M.S., Lee, K.K., Segura-Totten, M., Wilson, K.L., and McNally, E.M. (2002). Nesprin-1-self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett. 525, 135-140.
70. Morimoto, A., Shibuya, H., Zhu, X., Kim, J., Ishiguro, K., Han, M., and Watanabe, Y. (2012). A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J. Cell Biol. 198, 165-172.
71. Mosley-Bishop, K.L., Li, Q., Patterson, L., and Fischer, J.A. (1999). Molecular analysis of the klarsicht gene and its role in nuclear migration within differentiating cells of the Drosophila eye. Curr. Biol. 9, 1211-1220.
72. Murphy, S.P., Simmons, C.R., and Bass, H.W. (2010). Structure and expression of the maize (Zea mays L.) SUN-domain protein gene family: evidence for the existence of two divergent classes of SUN proteins in plants. BMC Plant Biol. 10, 269.
73. Nery, F.C., Zeng, J., Niland, B.P., Hewett, J., Farley, J., Irimia, D., Li, Y., Wiche, G., Sonnenberg, A., and Breakefield, X.O. (2008). TorsinA binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton. J. Cell Sci. 121, 3476-3486.
74. Nikolova-Krstevski, V., Leimena, C., Xiao, X.H., Kesteven, S., Tan, J.C., Yeo, L.S., Yu, Z.Y., Zhang, Q., Carlton, A., Head, S., et al. (2011). Nesprin-1 and actin contribute to nuclear and cytoskeletal defects in lamin A/C-deficient cardiomyopathy. J Mol. Cell Cardiol. 50, 479-486.
75. Niwa, O., Shimanuki, M., and Miki, F. (2000). Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis. EMBO J. 19, 3831-3840.
76. Oza, P., Jaspersen, S.L., Miele, A., Dekker, J., and Peterson, C.L. (2009). Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev. 23, 912-927.
77. 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.
78. Patterson, K., Molofsky, A.B., Robinson, C., Acosta, S., Cater, C., and Fischer, J.A. (2004). The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye. Mol. Biol. Cell 15, 600-610.
79. Phillips, C.M. and Dernburg, A.F. (2006). A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev. Cell 11, 817-829.
80. Postel, R., Ketema, M., Kuikman, I., de Pereda, J.M., and Sonnenberg, A. (2011). Nesprin-3 augments peripheral nuclear localization of intermediate filaments in zebrafish. J. Cell Sci. 124, 755-764.
81. Rajgor, D., Mellad, J.A., Autore, F., Zhang, Q., and Shanahan, C.M. (2012). Multiple novel nesprin-1 and nesprin-2 variants act as versatile tissue-specific intracellular scaffolds. PLoS One 7, e40098.
82. Rosenberg-Hasson, Y., Renert-Pasca, M., and Volk, T. (1996). A Drosophila dystrophin-related protein, MSP-300, is required for embryonic muscle morphogenesis. Mech. Dev. 60, 83-94.
83. 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. USA 106, 2194-2199.
84. Sato, A., Isaac, B., Phillips, C.M., Rillo, R., Carlton, P.M., Wynne, D.J., Kasad, R.A., and Dernburg, A.F. (2009). Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139, 907-919.
85. Scherthan, H., Wang, H., Adelfalk, C., White, E.J., Cowan, C., Cande, W.Z., and Kaback, D.B. (2007). Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 104, 16934-16939.
86. 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.
87. Schober, H., Ferreira, H., Kalck, V., Gehlen, L.R., and Gasser, S.M. (2009). Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev. 23, 928-938.
88. Schramm, C., Elliott, S., Shevchenko, A., and Schiebel, E. (2000). The Bbp1p-Mps2p complex connects the SPB to the nuclear envelope and is essential for SPB duplication. EMBO J. 19, 421-433.
89. Shao, X., Tarnasky, H.A., Lee, J.P., Oko, R., and van der Hoorn, F.A. (1999). Spag4, a novel sperm protein, binds outer dense-fiber protein Odf1 and localizes to microtubules of manchette and axoneme. Dev. Biol. 211, 109-123.
90. Shimanuki, M., Miki, F., Ding, D.Q., Chikashige, Y., Hiraoka, Y., Horio, T., and Niwa, O. (1997). A novel fission yeast gene, kms1+, is required for the formation of meiotic prophase-specific nuclear architecture. Mol. Gen. Genet. 254, 238-249.
91. Shindo, Y., Kim, M.R., Miura, H., Yuuki, T., Kanda, T., Hino, A., and Kusakabe, Y. (2010). Lrmp/Jaw1 is expressed in sweet, bitter, and umami receptor-expressing cells. Chem. Senses 35, 171-177.
92. Sohaskey, M.L., Jiang, Y., Zhao, J.J., Mohr, A., Roemer, F., and Harland, R.M. (2010). Osteopotentia regulates osteoblast maturation, bone formation, and skeletal integrity in mice. J. Cell Biol. 189, 511-525.
93. Sosa, B.A., Rothballer, A., Kutay, U., and Schwartz, T.U. (2012). LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins. Cell 149, 1035-1047.
94. Starr, D.A. and Han, M. (2002). Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 298, 406-409.
95. Starr, D.A., Hermann, G.J., Malone, C.J., Fixsen, W., Priess, J.R., Horvitz, H.R., and Han, M. (2001). unc-83 encodes a novel component of the nuclear envelope and is essential for proper nuclear migration. Development 128, 5039-5050.
96. 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.
97. Swan, A., Nguyen, T., and Suter, B. (1999). Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning. Nat. Cell Biol. 1, 444-449.
98. Tamura, K., Iwabuchi, K., Fukao, Y., Kondo, M., Okamoto, K., Ueda, H., Nishimura, M., and Hara-Nishimura, I. (2013). Myosin XI-i links the nuclear membrane to the cytoskeleton to control nuclear movement and shape in Arabidopsis. Curr. Biol. 23, 1776-1781.
99. Taranum, S., Sur, I., Muller, R., Lu, W., Rashmi, R.N., Munck, M., Neumann, S., Karakesisoglou, I., and Noegel, A.A. (2012). Cytoskeletal interactions at the nuclear envelope mediated by nesprins. Int. J. Cell Biol. 2012, 736524.
100. Technau, M. and Roth, S. (2008). The Drosophila KASH domain proteins Msp-300 and Klarsicht and the SUN domain protein Klaroid have no essential function during oogenesis. Fly (Austin) 2, 82-91.
101. Trelles-Sticken, E., Adelfalk, C., Loidl, J., and Scherthan, H. (2005). Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J. Cell Biol. 170, 213-223.
102. Tulgren, E.D., Turgeon, S.M., Opperman, K.J., and Grill, B. (2014). The Nesprin family member ANC-1 regulates synapse formation and axon termination by functioning in a pathway with RPM-1 and - catenin. PLoS Genet. 10, e1004481.
103. Tzur, Y.B., Margalit, A., Melamed-Book, N., and Gruenbaum, Y. (2006a). Matefin/SUN-1 is a nuclear envelope receptor for CED-4 during Caenorhabditis elegans apoptosis. Proc. Natl. Acad. Sci. USA 103, 13397-13402.
104. Tzur, Y.B., Wilson, K.L., and Gruenbaum, Y. (2006b). SUN-domain proteins: 'Velcro' that links the nucleoskeleton to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 7, 782-788.
105. Volk, T. (1992). A new member of the spectrin superfamily may participate in the formation of embryonic muscle attachments in Drosophila. Development 116, 721-730.
106. Volk, T. (2013). Positioning nuclei within the cytoplasm of striated muscle fiber: cooperation between microtubules and KASH proteins. Nucleus 4, 18-22.
107. Walde, S. and King, M.C. (2014). The KASH protein Kms2 coordinates mitotic remodeling of the spindle pole body. J. Cell Sci. 127, 3625-3640.
108. Wanat, J.J., Kim, K.P., Koszul, R., Zanders, S., Weiner, B., Kleckner, N., and Alani, E. (2008). Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis. PLoS Genet. 4, e1000188.
109. Wang, W., Shi, Z., Jiao, S., Chen, C., Wang, H., Liu, G., Wang, Q., Zhao, Y., Greene, M.I., and Zhou, Z. (2012). Structural insights into SUN-KASH complexes across the nuclear envelope. Cell Res. 22, 1440-1452.
110. Wang, Z., Xue, W., Li, X., Lin, R., Cui, J., and Huang, J.D. (2013). 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.
111. Warren, D.T., Tajsic, T., Mellad, J.A., Searles, R., Zhang, Q., and Shanahan, C.M. (2010). Novel nuclear nesprin-2 variants tether active extracellular signal-regulated MAPK1 and MAPK2 at promyelocytic leukemia protein nuclear bodies and act to regulate smooth muscle cell proliferation. J. Biol. Chem. 285, 1311-1320.
112. Welte, M.A. (2004). Bidirectional transport along microtubules. Curr. Biol. 14, R525-537.
113. 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-1-and nesprin-2-bind directly to emerin and both interactions are disrupted in X-linked Emery-Dreifuss muscular dystrophy. Exp. Cell Res. 313, 2845-2857.
114. 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.
115. Xie, X. and Fischer, J.A. (2008). On the roles of the Drosophila KASH domain proteins Msp-300 and Klarsicht. Fly (Austin) 2, 74-81.
116. Xu, X.M., Meulia, T., and Meier, I. (2007). Anchorage of plant RanGAP to the nuclear envelope involves novel nuclear-poreassociated proteins. Curr. Biol. 17, 1157-1163.
117. Yamamoto, A., West, R.R., McIntosh, J.R., and Hiraoka, Y. (1999). A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J. Cell Biol. 145, 1233-1249.
118. Yoshida, M., Katsuyama, S., Tateho, K., Nakamura, H., Miyoshi, J., Ohba, T., Matsuhara, H., Miki, F., Okazaki, K., Haraguchi, T., et al. (2013). Microtubule-organizing center formation at telomeres induces meiotic telomere clustering. J. Cell Biol. 200, 385-395.
119. Yu, J., Starr, D.A., Wu, X., Parkhurst, S.M., Zhuang, Y., Xu, T., Xu, R., and Han, M. (2006). The KASH domain protein MSP-300 plays an essential role in nuclear anchoring during Drosophila oogenesis. Dev. Biol. 289, 336-345.
120. 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.
121. Zhang, Q., Skepper, J.N., Yang, F., Davies, J.D., Hegyi, L., Roberts, R.G., Weissberg, P.L., Ellis, J.A., and Shanahan, C.M. (2001). Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J. Cell Sci. 114, 4485-4498.
122. Zhang, Q., Ragnauth, C., Greener, M.J., Shanahan, C.M., and Roberts, R.G. (2002). The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300. Genomics 80, 473-481.
123. 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.
124. 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.
125. 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.
126. Zhang, X., Lei, K., Yuan, X., Wu, X., Zhuang, Y., Xu, T., Xu, R., and Han, M. (2009). SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64, 173-187.
127. Zhao, Q., Brkljacic, J., and Meier, I. (2008). Two distinct interacting classes of nuclear envelope-associated coiled-coil proteins are required for the tissue-specific nuclear envelope targeting of Arabidopsis RanGAP. Plant Cell 20, 1639-1651.
128. 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.
129. Zhou, K., Rolls, M.M., Hall, D.H., Malone, C.J., and Hanna-Rose, W. (2009). A ZYG-12-dynein interaction at the nuclear envelope defines cytoskeletal architecture in the C. elegans gonad. J. Cell Biol. 186, 229-241.
130. Zhou, X., Graumann, K., Evans, D.E., and Meier, I. (2012a). Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination. J. Cell Biol. 196, 203-211.
131. Zhou, Z., Du, X., Cai, Z., Song, X., Zhang, H., Mizuno, T., Suzuki, E., Yee, M.R., Berezov, A., Murali, R., et al. (2012b). Structure of Sad1-UNC84 homology (SUN) domain defines features of molecular bridge in nuclear envelope. J. Biol. Chem. 287, 5317-5326.
132. Zhou, X., Graumann, K., Wirthmueller, L., Jones, J.D., and Meier, I. (2014). Identification of unique SUN-interacting nuclear envelope proteins with diverse functions in plants. J. Cell Biol. 205, 677-692.