LINCing complex functions at the nuclear envelope what the molecular architecture of the LINC complex can reveal about its function

Nucleus (United States)

Volumn 4, Issue 1, 2013, Pages 29-36

  Rothballer, Andrea ^a   Schwartz, Thomas U ^b   Kutay, Ulrike ^a  

^a ETH ZURICH   (Switzerland)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

KASH domain; LINC complex; Mechanotransduction; Membrane fusion; Nuclear envelope; Nuclear membrane spacing; Nuclear pore complex; Spermatogenesis; Spindle pole body; SUN domain

Indexed keywords

KASH PROTEIN; LINKER OF NUCLEOSKELETON AND CYTOSKELETON COMPLEX; MEMBRANE PROTEIN; NUCLEAR PROTEIN; NUCLEOPORIN; SUN PROTEIN; UNCLASSIFIED DRUG; BRSK1 PROTEIN, HUMAN; LINC COMPLEX; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; SUN1 PROTEIN, HUMAN;

ARTICLE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; COMPLEX FORMATION; CYTOARCHITECTURE; CYTOSKELETON; HUMAN; MECHANOTRANSDUCTION; MEMBRANE FUSION; NONHUMAN; NUCLEAR PORE COMPLEX; NUCLEAR SHAPE; SPINDLE POLE BODY; CELL NUCLEUS MATRIX; KASH DOMAIN; METABOLISM; NUCLEAR MEMBRANE SPACING; PROTEIN TERTIARY STRUCTURE; SPERMATOGENESIS; SUN DOMAIN;

KASH DOMAIN; LINC COMPLEX; MECHANOTRANSDUCTION; MEMBRANE FUSION; NUCLEAR ENVELOPE; NUCLEAR MEMBRANE SPACING; NUCLEAR PORE COMPLEX; SPERMATOGENESIS; SPINDLE POLE BODY; SUN DOMAIN;

CYTOSKELETON; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; NUCLEAR ENVELOPE; NUCLEAR MATRIX; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES;

EID: 84873539589     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.23387     Document Type: Article

References (60)

1. Shimi T, Butin-Israeli V, Goldman RD. The functions of the nuclear envelope in mediating the molecular crosstalk between the nucleus and the cytoplasm. Curr Opin Cell Biol 2012; 24:71-8. PMID:22192274; http://dx.doi.org/10.1016/j.ceb.2011.11.007.
2. Stewart CL, Roux KJ, Burke B. Blurring the boundary: the nuclear envelope extends its reach. Science 2007; 318:1408-12. PMID:18048680; http://dx.doi.org/10.1126/science.1142034.
3. Worman HJ, Ostlund C, Wang Y. Diseases of the nuclear envelope. Cold Spring Harb Perspect Biol 2010; 2:a000760. PMID:20182615; http://dx.doi.org/10.1101/cshperspect.a000760.
4. Grossman E, Medalia O, Zwerger M. Functional architecture of the nuclear pore complex. Annu Rev Biophys 2012; 41:557-84. PMID:22577827; http//dx.doi.org/10.1146/a nnurev-bio-phys-050511-102328.
5. Burke B, Roux KJ. Nuclei take a position: managing nuclear location. Dev Cell 2009; 17:587-97. PMID:19922864; http://dx.doi.org/10.1016/j.devcel.2009.10.018.
6. Fridkin A, Penkner A, Jantsch V, Gruenbaum Y. SUN-domain and KASH-domain proteins during development, meiosis and disease. Cell Mol Life Sci 2009; 66:1518-33. PMID:19125221; http://dx.doi.org/10.1007/s00018-008-8713-y.
7. Starr DA, Fridolfsson HN. Interactions between nuclei and the cytoskeleton are mediated by SUNKASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 2010; 26:421-44. PMID:20507227; http://dx.doi.org/10.1146/annurev-cellbio-100109-104037.
8. Sosa BA, Rothballer A, Kutay U, Schwartz TU. LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins. Cell 2012; 149:1035-47. PMID:22632968; http://dx.doi.org/10.1016/j.cell.2012.03.046.
9. Zhou Z, Du X, Cai Z, Song X, Zhang H, Mizuno T, et al. Structure of Sad1-UNC84 homology (SUN) domain defines features of molecular bridge in nuclear envelope. J Biol Chem 2012; 287:5317-26. PMID:22170055; http://dx.doi.org/10.1074/jbc.M111.304543.
10. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, et al. Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 2006; 172:41-53. PMID:16380439; http://dx.doi.org/10.1083/jcb.200509124.
11. Padmakumar VC, Libotte T, Lu W, Zaim H, Abraham S, Noegel AA, et al. The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J Cell Sci 2005; 118:3419-30. PMID:16079285; http://dx.doi.org/10.1242/jcs.02471.
12. Wang W, Shi Z, Jiao S, Chen C, Wang H, Liu G, et al. Structural insights into SUN-KASH complexes across the nuclear envelope. Cell Res 2012; 22:1440-52. PMID:22945352; http://dx.doi.org/10.1038/cr.2012.126.
13. Hodzic DM, Yeater DB, Bengtsson L, Otto H, Stahl PD. Sun2 is a novel mammalian inner nuclear membrane protein. J Biol Chem 2004; 279:25805-12. PMID:15082709; http://dx.doi.org/10.1074/jbc.M313157200.
14. Luxton GW, Gomes ER, Folker ES, Vintinner E, Gundersen GG. Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science 2010; 329:956-9. PMID:20724637; http://dx.doi.org/10.1126/science.1189072.
15. Ding X, Xu R, Yu J, Xu T, Zhuang Y, Han M. SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 2007; 12:863-72. PMID:17543860; http://dx.doi.org/10.1016/j.devcel.2007.03.018.
16. Morimoto A, Shibuya H, Zhu X, Kim J, Ishiguro K, Han M, et al. A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J Cell Biol 2012; 198:165-72. PMID:22826121; http://dx.doi.org/10.1083/jcb.201204085.
17. Schmitt J, Benavente R, Hodzic D, Höög C, Stewart CL, Alsheimer M. Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope. Proc Natl Acad Sci U S A 2007; 104:7426-31. PMID:17452644; http://dx.doi.org/10.1073/pnas.0609198104.
18. Mislow JM, Holaska JM, Kim MS, Lee KK, Segura-Totten M, Wilson KL, et al. Nesprin-1alpha self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett 2002; 525:135-40. PMID:12163176; http://dx.doi.org/10.1016/S0014-5793(02)03105-8.
19. Padmakumar VC, Abraham S, Braune S, Noegel AA, Tunggal B, Karakesisoglou I, et al. Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp Cell Res 2004; 295:330-9. PMID:15093733; http://dx.doi.org/10.1016/j.yexcr.2004.01.014.
20. Zhang Q, Skepper JN, Yang F, Davies JD, Hegyi L, Roberts RG, et al. Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J Cell Sci 2001; 114:4485-98. PMID:11792814.
21. Zhen YY, Libotte T, Munck M, Noegel AA, Korenbaum E. NUANCE, a giant protein connecting the nucleus and actin cytoskeleton. J Cell Sci 2002; 115:3207-22. PMID:12118075.
22. Haque F, Mazzeo D, Patel JT, Smallwood DT, Ellis JA, Shanahan CM, et al. Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes. J Biol Chem 2010; 285:3487-98. PMID:19933576; http://dx.doi.org/10.1074/jbc.M109.071910.
23. Roca-Cusachs P, Iskratsch T, Sheetz MP. Finding the weakest link: exploring integrin-mediated mechanical molecular pathways. J Cell Sci 2012; 125:3025-38. PMID:22797926; http://dx.doi.org/10.1242/ jcs.095794.
24. Lombardi ML, Zwerger M, Lammerding J. Biophysical assays to probe the mechanical properties of the interphase cell nucleus: substrate strain application and microneedle manipulation. J Vis Exp 2011; 55:e3087. PMID:21946671; http://dx.doi.org/10.3791/3087.
25. Anno T, Sakamoto N, Sato M. Role of nesprin-1 in nuclear deformation in endothelial cells under static and uniaxial stretching conditions. Biochem Biophys Res Commun 2012; 424:94-9. PMID:22728879; http://dx.doi.org/10.1016/j.bbrc.2012.06.073.
26. Lombardi ML, Jaalouk DE, Shanahan CM, Burke B, Roux KJ, Lammerding J. The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J Biol Chem 2011; 286:26743-53. PMID:21652697; http://dx.doi.org/10.1074/jbc.M111.233700.
27. Testa OD, Moutevelis E, Woolfson DN. CC+: a relational database of coiled-coil structures. Nucleic Acids Res 2009; 37(Database issue):D315-22. PMID:18842638; http://dx.doi.org/10.1093/nar/gkn675.
28. Voeltz GK, Prinz WA. Sheets, ribbons and tubules - how organelles get their shape. Nat Rev Mol Cell Biol 2007; 8:258-64. PMID:17287811; http://dx.doi.org/10.1038/nrm2119.
29. Göb E, Schmitt J, Benavente R, Alsheimer M. Mammalian sperm head formation involves different polarization of two novel LINC complexes. PLoS One 2010; 5:e12072. PMID:20711465; http://dx.doi.org/10.1371/journal.pone.0012072.
30. Tarnasky H, Gill D, Murthy S, Shao X, Demetrick DJ, van der Hoorn FA. A novel testis-specific gene, SPAG4, whose product interacts specifically with outer dense fiber protein ODF27, maps to human chromosome 20q11.2. Cytogenet Cell Genet 1998; 81:65-7. PMID:9691178; http://dx.doi.org/10.1159/000014990.
31. Xing XW, Li LY, Liu G, Fu JJ, Tan XJ, Lu GX. Identification of a novel gene SRG4 expressed at specific stages of mouse spermatogenesis. Acta Biochim Biophys Sin (Shanghai) 2004; 36:351-9. PMID:15156277; http://dx.doi.org/10.1093/abbs/36.5.351.
32. Kierszenbaum AL, Rivkin E, Tres LL. Molecular biology of sperm head shaping. Soc Reprod Fertil Suppl 2007; 65:33-43. PMID:17644953.
33. Shao X, Tarnasky HA, Lee JP, Oko R, van der Hoorn FA. Spag4, a novel sperm protein, binds outer densefiber protein Odf1 and localizes to microtubules of manchette and axoneme. Dev Biol 1999; 211:109-23. PMID:10373309; http://dx.doi.org/10.1006/dbio.1999.9297.
34. Kracklauer MP, Wiora HM, Deery WJ, Chen X, Bolival B Jr., Romanowicz D, et al. 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 2010; 123:2763-72. PMID:20647369; http://dx.doi.org/10.1242/jcs.066589.
35. Russell LD, Russell JA, MacGregor GR, Meistrich ML. Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents. Am J Anat 1991; 192:97-120. PMID:1759685; http://dx.doi.org/10.1002/aja.1001920202.
36. Tokuyasu KT. Dynamics of spermiogenesis in Drosophila melanogaster. IV. Nuclear transformation. J Ultrastruct Res 1974; 48:284-303. PMID:4210599; http://dx.doi.org/10.1016/S0022-5320(74)80083-3.
37. Kracklauer MP, Banks SM, Xie X, Wu Y, Fischer JA. Drosophila klaroid encodes a SUN domain protein required for Klarsicht localization to the nuclear envelope and nuclear migration in the eye. Fly (Austin) 2007; 1:75-85. PMID:18820457.
38. Tapley EC, Ly N, Starr DA. Multiple mechanisms actively target the SUN protein UNC-84 to the inner nuclear membrane. Mol Biol Cell 2011; 22:1739-52. PMID:21411627; http://dx.doi.org/10.1091/mbc.E10-08-0733.
39. Miki F, Kurabayashi A, Tange Y, Okazaki K, Shimanuki M, Niwa O. 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 2004; 270:449-61. PMID:14655046; http://dx.doi.org/10.1007/s00438-003-0938-8.
40. Jaspersen SL, Martin AE, Glazko G, Giddings TH Jr., Morgan G, Mushegian A, et al. The Sad1-UNC-84 homology domain in Mps3 interacts with Mps2 to connect the spindle pole body with the nuclear envelope. J Cell Biol 2006; 174:665-75. PMID:16923827; http://dx.doi.org/10.1083/jcb.200601062.
41. Hagan I, Yanagida M. The product of the spindle formation gene sad1+ associates with the fission yeast spindle pole body and is essential for viability. J Cell Biol 1995; 129:1033-47. PMID:7744953; http://dx.doi.org/10.1083/jcb.129.4.1033.
42. Jaspersen SL, Giddings TH Jr., Winey M. Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J Cell Biol 2002; 159:945-56. PMID:12486115; http://dx.doi.org/10.1083/jcb.200208169.
43. Muñoz-Centeno MC, McBratney S, Monterrosa A, Byers B, Mann C, Winey M. Saccharomyces cerevisiae MPS2 encodes a membrane protein localized at the spindle pole body and the nuclear envelope. Mol Biol Cell 1999; 10:2393-406. PMID:10397772.
44. Bupp JM, Martin AE, Stensrud ES, Jaspersen SL. Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3. J Cell Biol 2007; 179:845-54. PMID:18039933; http://dx.doi.org/10.1083/jcb.200706040.
45. King MC, Drivas TG, Blobel G. A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 2008; 134:427-38. PMID:18692466; http://dx.doi.org/10.1016/j.cell.2008.06.022.
46. Horigome C, Okada T, Shimazu K, Gasser SM, Mizuta K. Ribosome biogenesis factors bind a nuclear envelope SUN domain protein to cluster yeast telomeres. EMBO J 2011; 30:3799-811. PMID:21822217; http://dx.doi.org/10.1038/emboj.2011.267.
47. Murray S. High pressure freezing and freeze substitution of Schizosaccharomyces pombe and Saccharomyces cerevisiae for TEM. Methods Cell Biol 2008; 88:3-17. PMID:18617025; http://dx.doi.org/10.1016/S0091-679X(08)00401-9.
48. McDonald K. Cryopreparation methods for electron microscopy of selected model systems. Methods Cell Biol 2007; 79:23-56. PMID:17327151; http://dx.doi.org/10.1016/S0091-679X(06)79002-1.
49. Güttinger S, Laurell E, Kutay U. Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol 2009; 10:178-91. PMID:19234477; http://dx.doi.org/10.1038/nrm2641.
50. Doucet CM, Hetzer MW. Nuclear pore biogenesis into an intact nuclear envelope. Chromosoma 2010; 119:469-77. PMID:20721671; http://dx.doi.org/10.1007/s00412-010-0289-2.
51. Risselada HJ, Grubmüller H. How SNARE molecules mediate membrane fusion: recent insights from molecular simulations. Curr Opin Struct Biol 2012; 22:187-96. PMID:22365575; http://dx.doi.org/10.1016/j.sbi.2012.01.007.
52. Liu Q, Pante N, Misteli T, Elsagga M, Crisp M, Hodzic D, et al. Functional association of Sun1 with nuclear pore complexes. J Cell Biol 2007; 178:785-98. PMID:17724119; http://dx.doi.org/10.1083/jcb.200704108.
53. Talamas JA, Hetzer MW. POM121 and Sun1 play a role in early steps of interphase NPC assembly. J Cell Biol 2011; 194:27-37. PMID:21727197; http://dx.doi.org/10.1083/jcb.201012154.
54. Jaspersen SL, Ghosh S. Nuclear envelope insertion of spindle pole bodies and nuclear pore complexes. Nucleus 2012; 3:226-36. PMID:22572959; http://dx.doi.org/10.4161/nucl.20148.
55. Jaspersen SL, Winey M. The budding yeast spindle pole body: structure, duplication, and function. Annu Rev Cell Dev Biol 2004; 20:1-28. PMID:15473833; http://dx.doi.org/10.1146/annurev.cellbio.20.022003.114106.
56. Ding R, West RR, Morphew DM, Oakley BR, McIntosh JR. The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds. Mol Biol Cell 1997; 8:1461-79. PMID:9285819.
57. Friederichs JM, Ghosh S, Smoyer CJ, McCroskey S, Miller BD, Weaver KJ, et al. The SUN protein Mps3 is required for spindle pole body insertion into the nuclear membrane and nuclear envelope homeostasis. PLoS Genet 2011; 7:e1002365. PMID:22125491; http://dx.doi.org/10.1371/journal.pgen.1002365.
58. Winey M, Goetsch L, Baum P, Byers B. MPS1 and MPS2: novel yeast genes defining distinct steps of spindle pole body duplication. J Cell Biol 1991; 114:745-54. PMID:1869587; http://dx.doi.org/10.1083/jcb.114.4.745.
59. Harrison SC. Viral membrane fusion. Nat Struct Mol Biol 2008; 15:690-8. PMID:18596815; http://dx.doi.org/10.1038/nsmb.1456.
60. Murphy SP, Simmons CR, Bass HW. 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 2010; 10:269. PMID:21143845; http://dx.doi.org/10.1186/1471-2229-10-269.