The missing LINC: A mammalian KASH-domain protein coupling meiotic chromosomes to the cytoskeleton

Nucleus (United States)

Volumn 5, Issue 1, 2014, Pages 3-10

  Stewart, Colin L ^a   Burke, Brian ^a  

^a INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

Dynein; LINC complex; Meiosis; Nuclear envelope; Nuclear membrane; Spermatocyte

Indexed keywords

CYTOPLASMIC DYNEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; PROTEIN; PROTEIN KASH5; PROTEIN SUN1; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS MEMBRANE; CHROMOSOME; CHROMOSOME PAIRING; COMPLEX FORMATION; CYTOSKELETON; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; KASH DOMAIN; MEIOTIC PROPHASE I; NONHUMAN; PROTEIN DOMAIN; SPERMATOCYTE; SUN DOMAIN; TELOMERE;

EID: 84897511498     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.27819     Document Type: Article

References (67)

1. Wilkins A S, Holliday R. The evolution of meiosis from mitosis. Genetics 2009; 181:3-12; PMID:19139151; http://dx.doi.org/10.1534/genetics.108.099762
2. Fraune J, Schramm S, Alsheimer M, Benavente R. The mammalian synaptonemal complex: protein components, assembly and role in meiotic recombination. Exp Cell Res 2012; 318:1340-6; PMID:22394509; http://dx.doi.org/10.1016/j.yexcr.2012.02.018
3. Revenkova E, Jessberger R. Shaping meiotic prophase chromosomes: cohesins and synaptonemal complex proteins. Chromosoma 2006; 115:235-40; PMID:16518630; http://dx.doi.org/10.1007/s00412-006-0060-x
4. Vallente RU, Cheng EY, Hassold TJ. The synaptonemal complex and meiotic recombination in humans: new approaches to old questions. Chromosoma 2006; 115:241-9; PMID:16547726; http://dx.doi.org/10.1007/s00412-006-0058-4
5. Zickler D. From early homologue recognition to synaptonemal complex formation. Chromosoma 2006; 115:158-74; PMID:16570189; http://dx.doi.org/10.1007/s00412-006-0048-6
6. Scherthan H. A bouquet makes ends meet. Nat Rev Mol Cell Biol 2001; 2:621-7;PMID:11483995; http://dx.doi.org/10.1038/35085086
7. Lee CY, Conrad MN, Dresser ME. Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet 2012; 8:e1002730; PMID:22654677; http://dx.doi.org/10.1371/journal.pgen.1002730
8. Trelles-Sticken E, Adelfalk C, Loidl J, Scherthan H. Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J Cell Biol 2005; 170:213-23; PMID:16027219; http://dx.doi.org/10.1083/jcb.200501042
9. Conrad MN, Lee CY, Chao G, Shinohara M, Kosaka H, Shinohara A, Conchello JA, Dresser ME. Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 2008; 133:1175-87; PMID:18585352; http://dx.doi.org/10.1016/j.cell.2008.04.047
10. Koszul R, Kim KP, Prentiss M, Kleckner N, Kameoka S. Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 2008; 133:1188-201; PMID:18585353; http://dx.doi.org/10.1016/j.cell.2008.04.050
11. Wilson KL, Dawson SC. Evolution: functional evolution of nuclear structure. J Cell Biol 2011; 195:171-81; PMID:22006947; http://dx.doi.org/10.1083/jcb.201103171
12. 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
13. Schirmer EC, Florens L, Guan T, Yates JR III, Gerace L. Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 2003; 301:1380-2; PMID:12958361; http://dx.doi.org/10.1126/science.1088176
14. Burke B, Stewart CL. The nuclear lamins: flexibility in function. Nat Rev Mol Cell Biol 2013; 14:13-24; PMID:23212477; http://dx.doi.org/10.1038/nrm3488
15. 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
16. Starr DA, Han M. ANChors away: an actin based mechanism of nuclear positioning. J Cell Sci 2003; 116:211-6; PMID:12482907; http://dx.doi.org/10.1242/jcs.00248
17. Starr DA. A nuclear-envelope bridge positions nuclei and moves chromosomes. J Cell Sci 2009; 122:577-86; PMI D:19225124; http://dx.doi.org/10.1242/jcs.037622
18. Zhang Q, Ragnauth C, Greener MJ, Shanahan CM, Roberts RG. The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300. Genomics 2002; 80:473-81; PMID:12408964; http://dx.doi.org/10.1006/geno.2002.6859
19. Zhang X, Xu R, Zhu B, Yang X, Ding X, Duan S, Xu T, Zhuang Y, Han M. Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 2007; 134:901-8; PMID:172674 47; http://dx.doi.org/10.1242/dev.02783
20. 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
21. Padmakumar VC, Abraham S, Braune S, Noegel AA, Tunggal B, Karakesisoglou I, Korenbaum E. 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
22. Starr DA, Han M. Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 2002; 298:406-9; PMID:12169658; http://dx.doi.org/10.1126/science.1075119
23. Mosley-Bishop KL, Li Q, Patterson L, Fischer JA. Molecular analysis of the klarsicht gene and its role in nuclear migration within differentiating cells of the Drosophila eye. Curr Biol 1999; 9:1211-20; PMID:10556085; http://dx.doi.org/10.1016/S0960-9822(99)80501-6
24. Malone CJ, Misner L, Le Bot N, Tsai MC, Campbell JM, Ahringer J, White JG. The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 2003; 115: 825-36; PMID:14697201; http://dx.doi.org/10.1016/S0092-8674(03)00985-1
25. Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, Stewart CL, Burke B. Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci U S A 2009; 106:2194-9; PMID:19164528; http://dx.doi.org/10.1073/pnas.0808602106
26. Horn HF, Brownstein Z, Lenz DR, Shivatzki S, Dror AA, Dagan-Rosenfeld O, Friedman LM, Roux KJ, Kozlov S, Jeang KT, et al. The LINC complex is essential for hearing. J Clin Invest 2013; 123:740-50; PMID:23348741
27. Ketema M, Kreft M, Secades P, Janssen H, Sonnenberg A. 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 2013; 24:2454-66; PMID:23761073; http://dx.doi.org/10.1091/mbc.E13-02-0100
28. Ketema M, Wilhelmsen K, Kuikman I, Janssen H, Hodzic D, Sonnenberg A. Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin. J Cell Sci 2007; 120:3384-94; PMID: 17881500; http://dx.doi.org/10.1242/jcs.014191
29. Wilhelmsen K, Litjens SH, Kuikman I, Tshimbalanga N, Janssen H, van den Bout I, Raymond K, Sonnenberg A. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J Cell Biol 2005; 171:799-810; PMID:16330710; http://dx.doi.org/10.1083/jcb.200506083
30. Liu Q, Pante N, Misteli T, Elsagga M, Crisp M, Hodzic D, Burke B, Roux KJ. 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
31. Sohaskey ML, Jiang Y, Zhao JJ, Mohr A, Roemer F, Harland RM. Osteopotentia regulates osteoblast maturation, bone formation, and skeletal integrity in mice. J Cell Biol 2010; 189:511-25; PMID: 20440000; http://dx.doi.org/10.1083/jcb.201003006
32. 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
33. Hasan S, Güttinger S, Mühlhäusser P, Anderegg F, Bürgler S, Kutay U. Nuclear envelope localization of human UNC84A does not require nuclear lamins. FEBS Lett 2006; 580:1263-8; PMID:16445915; http://dx.doi.org/10.1016/j.febslet.2006.01.039
34. Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM, Fry AM, Trembath RC, Shackleton S. SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 2006; 26:3738-51; PMID:16648470; http://dx.doi.org/10.1128/MCB.26.10.3738-3751.2006
35. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D. 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
36. Padmakumar VC, Libotte T, Lu W, Zaim H, Abraham S, Noegel AA, Gotzmann J, Foisner R, Karakesisoglou I. 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
37. McGee MD, Rillo R, Anderson AS, Starr DA. 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 2006; 17:1790-801; PMID:16481402; http://dx.doi.org/10.1091/mbc.E05-09-0894
38. 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
39. Zhou Z, Du X, Cai Z, Song X, Zhang H, Mizuno T, Suzuki E, Yee MR, Berezov A, Murali R, 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
40. 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
41. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, Xu R, Han M. SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 2009; 64:173-87; PMID:19874786; http://dx.doi.org/10.1016/j.neuron.2009.08.018
42. Lindeman RE, Pelegri F. Localized products of futile cycle/lrmp promote centrosome-nucleus attachment in the zebrafish zygote. Curr Biol 2012; 22:843-51; PMID:22542100; http://dx.doi.org/10.1016/j.cub.2012.03.058
43. Chikashige Y, Tsutsumi C, Yamane M, Okamasa K, Haraguchi T, Hiraoka Y. Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 2006; 125:59-69; PMID: 16615890; http://dx.doi.org/10.1016/j.cell.2006.01.048
44. 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
45. Chi YH, Cheng LI, Myers T, Ward JM, Williams E, Su Q, Faucette L, Wang J Y, Jeang KT. Requirement for Sun1 in the expression of meiotic reproductive genes and piRNA. Development 2009; 136:965-73; PMID:19211677; http://dx.doi.org/10.1242/dev.029868
46. Sato A, Isaac B, Phillips CM, Rillo R, Carlton PM, Wynne DJ, Kasad RA, Dernburg A F. Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 2009; 139:907-19; PMID:19913287; http://dx.doi.org/10.1016/j.cell.2009.10.039
47. Hiraoka Y, Dernburg A F. The SUN rises on meiotic chromosome dynamics. Dev Cell 2009; 17:598-605; PMID:19922865; http://dx.doi.org/10.1016/j.devcel.2009.10.014
48. 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: 4 49-61; PMID:14655046; http://dx.doi.org/10.1007/s00438-003-0938-8
49. Miki F, Okazaki K, Shimanuki M, Yamamoto A, Hiraoka Y, Niwa O. The 14-kDa dynein light chain-family protein Dlc1 is required for regular oscillatory nuclear movement and efficient recombination during meiotic prophase in fission yeast. Mol Biol Cell 2002; 13:930-46; PMID:11907273; http://dx.doi.org/10.1091/mbc.01-11-0543
50. Chikashige Y, Yamane M, Okamasa K, Tsutsumi C, Kojidani T, Sato M, Haraguchi T, Hiraoka Y. Membrane proteins Bqt3 and -4 anchor telomeres to the nuclear envelope to ensure chromosomal bouquet formation. J Cell Biol 2009; 187:413-27; PMID:19948484; http://dx.doi.org/10.1083/jcb.200902122
51. 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
52. Conrad MN, Lee CY, Wilkerson JL, Dresser ME. MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2007; 104:8863-8; PMID:17495028; http://dx.doi.org/10.1073/pnas.0606165104
53. Penkner A, Tang L, Novatchkova M, Ladurner M, Fridkin A, Gruenbaum Y, Schweizer D, Loidl J, Jantsch V. The nuclear envelope protein Matefin/ SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell 2007; 12:873-85; PMID:17543861; http://dx.doi.org/10.1016/j.devcel.2007.05.004
54. Penkner AM, Fridkin A, Gloggnitzer J, Baudrimont A, Machacek T, Woglar A, Csaszar E, Pasierbek P, Ammerer G, Gruenbaum Y, et al. Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 2009; 139:920-33; PMID:19913286; http://dx.doi.org/10.1016/j.cell.2009.10.045
55. Phillips CM, Dernburg AF. A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell 2 0 0 6; 11: 817-29; PMID: 17141157; http://dx.doi.org/10.1016/j.devcel.2006.09.020
56. Phillips CM, Wong C, Bhalla N, Carlton PM, Weiser P, Meneely PM, Dernburg AF. HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 2005; 123:1051-63; PMID:16360035; http://dx.doi.org/10.1016/j.cell.2005.09.035
57. Baudrimont A, Penkner A, Woglar A, Machacek T, Wegrostek C, Gloggnitzer J, Fridkin A, Klein F, Gruenbaum Y, Pasierbek P, et al. Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans. PLoS Genet 2010; 6:e1001219; PMID:21124819; http://dx.doi.org/10.1371/journal.pgen.1001219
58. Harper L, Golubovskaya I, Cande WZ. A bouquet of chromosomes. J Cell Sci 2004; 117:4025-32; PMID:15316078; http://dx.doi.org/10.1242/jcs.01363
59. Morimoto A, Shibuya H, Zhu X, Kim J, Ishiguro K, Han M, Watanabe Y. 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
60. Horn HF, Kim DI, Wright GD, Wong ES, Stewart CL, Burke B, Roux KJ. A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J Cell Biol 2013; 202:1023-39; PMID:24062341; http://dx.doi.org/10.1083/jcb.201304004
61. Dekens MP, Pelegri FJ, Maischein HM, Nüsslein-Volhard C. The maternal-effect gene futile cycle is essential for pronuclear congression and mitotic spindle assembly in the zebraf ish zygote. Development 2003; 130:3907-16; PMID: 12874114; http://dx.doi.org/10.1242/dev.00606
62. Kretsinger RH, Barry CD. The predicted structure of the calcium-binding component of troponin. Biochim Biophys Acta 1975; 405:40-52; PMID:1174567; http://dx.doi.org/10.1016/0005-2795(75)90312-8
63. Schermelleh L, Carlton PM, Haase S, Shao L, Winoto L, Kner P, Burke B, Cardoso MC, Agard DA, Gustafsson MG, et al. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 2008; 320:1332-6; PMID:18535242; http://dx.doi.org/10.1126/science.1156947
64. Zhang Q, Skepper JN, Yang F, Davies JD, Hegyi L, Roberts RG, Weissberg PL, Ellis JA, Shanahan CM. 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
65. Behrens TW, Jagadeesh J, Scherle P, Kearns G, Yewdell J, Staudt LM. Jaw1, A lymphoid-restricted membrane protein localized to the endoplasmic reticulum. J Immunol 1994; 153:682-90; PMID:8021504
66. Schneider M, Lu W, Neumann S, Brachner A, Gotzmann J, Noegel AA, Karakesisoglou I. Molecular mechanisms of centrosome and cytoskeleton anchorage at the nuclear envelope. Cell Mol Life Sci 2011; 6 8: 1593-610; PMID:20922455; http://dx.doi.org/10.1007/s00018-010-0535-z
67. Shindo Y, Kim MR, Miura H, Yuuki T, Kanda T, Hino A, Kusakabe Y. Lrmp/Jaw1 is expressed in sweet, bitter, and umami receptor-expressing cells. Chem Senses 2010; 35:171-7; PMID:20071408; http://dx.doi.org/10.1093/chemse/bjp097