Genetic analysis of Mps3 SUN domain mutants in Saccharomyces cerevisiae reveals an interaction with the SUN-like protein Slp1

G3: Genes, Genomes, Genetics

Volumn 2, Issue 12, 2012, Pages 1703-1718

  Friederichs, Jennifer M ^a   Gardner, Jennifer M ^a   Smoyer, Christine J ^a   Whetstine, Christine R ^a   Gogol, Madelaine ^a   Slaughter, Brian D ^a   Jaspersen, Sue L ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Body; Duplication; Membrane; Mps3; Nuclear ER; SGA; Spindle pole; SUN protein

Indexed keywords

MEMBRANE PROTEIN; MPS3 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SUN PROTEIN; VESICULAR TRANSPORT PROTEIN; VPS33 PROTEIN, S CEREVISIAE;

ALLELE; ARTICLE; CELL CYCLE CHECKPOINT; CELL NUCLEUS MEMBRANE; CHEMISTRY; CHROMOSOME; ENDOPLASMIC RETICULUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOSIS SPINDLE; MPS3; MUTATION; NUCLEAR/ER MEMBRANE; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SGA; SPINDLE POLE BODY DUPLICATION;

MPS3; NUCLEAR/ER MEMBRANE; SGA; SPINDLE POLE BODY DUPLICATION; SUN PROTEIN;

ALLELES; CELL CYCLE CHECKPOINTS; CHROMOSOMES; ENDOPLASMIC RETICULUM; MEMBRANE PROTEINS; MITOTIC SPINDLE APPARATUS; MUTATION; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 84883182912     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.112.004614     Document Type: Article

References (85)

1. Alber, F., S. Dokudovskaya, L. M. Veenhoff, W. Zhang, J. Kipper et al., 2007 The molecular architecture of the nuclear pore complex. Nature 450: 695-701.
2. Antoniacci, L. M., M. A. Kenna, P. Uetz, S. Fields, and R. V. Skibbens, 2004 The spindle pole body assembly component Mps3p/Nep98p functions in sister chromatid cohesion. J. Biol. Chem. 279: 49542-49550.
3. Antoniacci, L. M., M. A. Kenna, and R. V. Skibbens, 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. Baker, K. E., J. Coller, and R. Parker, 2004 The yeast Apq12 protein affects nucleocytoplasmic mRNA transport. RNA 10: 1352-1358.
5. Baldwin, B. R., C. O. Zhang, and S. Keay, 2000 Cloning and epitope mapping of a functional partial fusion receptor for human cytomegalovirus gH. J. Gen. Virol. 81: 27-35.
6. Bernsel, A., H. Viklund, A. Hennerdal, and A. Elofsson, 2009 TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res. 37: W465-W468.
7. Bupp, J. M., A. E. Martin, E. S. Stensrud, and S. L. Jaspersen, 2007 Telomere anchoring at the nuclear periphery requires the budding yeast Sad1- UNC-84 domain protein Mps3. J. Cell Biol. 179: 845-854.
8. Burke, B., 2012 It takes KASH to hitch to the SUN. Cell 149: 961-963. Burke, B., and K. J. Roux, 2009 Nuclei take a position: managing nuclear location. Dev. Cell 17: 587-597.
9. Burke, B., and K. J. Roux, 2009 Nuclei take a position: managing nuclear location. Dev. Cell 17: 587-597.
10. Burns, L. T., and S. R. Wente, 2012 Trafficking to uncharted territory of the nuclear envelope. Curr. Opin. Cell Biol. 24: 341-349.
11. Campbell, J. L., A. Lorenz, K. L. Witkin, T. Hays, J. Loidl et al., 2006 Yeast nuclear envelope subdomains with distinct abilities to resist membrane expansion. Mol. Biol. Cell 17: 1768-1778.
12. Casey, A. K., T. R. Dawson, J. Chen, J. M. Friederichs, S. L. Jaspersen et al., 2012 Integrity and function of the Saccharomyces cerevisiae spindle pole body depends on connections between the membrane proteins Ndc1, Rtn1, and Yop1. Genetics 192: 441-455.
13. Chadrin, A., B. Hess, M. San Roman, X. Gatti, B. Lombard et al., 2010 Pom33, a novel transmembrane nucleoporin required for proper nuclear pore complex distribution. J. Cell Biol. 189: 795-811.
14. Chan, J. N., B. P. Poon, J. Salvi, J. B. Olsen, A. Emili et al., 2011 Perinuclear cohibin complexes maintain replicative life span via roles at distinct silent chromatin domains. Dev. Cell 20: 867-879.
15. Chikashige, Y., C. Tsutsumi, M. Yamane, K. Okamasa, T. Haraguchi et al., 2006 Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125: 59-69.
16. Conrad, M. N., C. Y. Lee, J. L. Wilkerson, and M. E. Dresser, 2007 MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 104: 8863-8868.
17. Conrad, M. N., C. Y. Lee, G. Chao, M. Shinohara, H. Kosaka et al., 2008 Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133: 1175-1187.
18. Costanzo, M., A. Baryshnikova, J. Bellay, Y. Kim, E. D. Spear et al., 2010 The genetic landscape of a cell. Science 327: 425-431.
19. Crisp, M., Q. Liu, K. Roux, J. B. Rattner, C. Shanahan et al., 2006 Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172: 41-53.
20. Dawson, T. R., M. D. Lazarus, M. W. Hetzer, and S. R. Wente, 2009 ER membrane-bending proteins are necessary for de novo nuclear pore formation. J. Cell Biol. 184: 659-675.
21. Ding, X., R. Xu, J. Yu, T. Xu, Y. Zhuang et al., 2007 SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell 12: 863-872.
22. Friederichs, J. M., S. Ghosh, C. J. Smoyer, S. McCroskey, B. D. Miller et al., 2011 The SUN protein Mps3 is required for spindle pole body insertion into the nuclear membrane and nuclear envelope homeostasis. PLoS Genet. 7: e1002365.
23. Gardner, J. M., C. J. Smoyer, E. S. Stensrud, R. Alexander, M. Gogol et al., 2011 Targeting of the SUN protein Mps3 to the inner nuclear membrane by the histone variant H2A. Z. J Cell Biol 193: 489-507.
24. Ghosh, S., J. M. Gardner, C. J. Smoyer, J. M. Friederichs, J. Unruh et al., 2012 Acetylation of the SUN protein Mps3 by Eco1 regulates its function in nuclear organization. Mol. Biol. Cell 23: 2546-2559.
25. Greenland, K. B., H. Ding, M. Costanzo, C. Boone, and T. N. Davis, 2010 Identification of Saccharomyces cerevisiae spindle pole body remodeling factors. PLoS ONE 5: e15426.
26. Hetzer, M. W., and S. R. Wente, 2009 Border control at the nucleus: biogenesis and organization of the nuclear membrane and pore complexes. Dev. Cell 17: 606-616.
27. Hiraga, S., S. Botsios, D. Donze, and A. D. Donaldson, 2012 TFIIIC localizes budding yeast ETC sites to the nuclear periphery. Mol. Biol. Cell 23: 2741-2754.
28. Hiraoka, Y., and A. F. Dernburg, 2009 The SUN rises on meiotic chromosome dynamics. Dev. Cell 17: 598-605.
29. Horigome, C., T. Okada, K. Shimazu, S. M. Gasser, and K. Mizuta, 2011 Ribosome biogenesis factors bind a nuclear envelope SUN domain protein to cluster yeast telomeres. EMBO J. 30: 3799-3811.
30. Howell, G. R., M. Shindo, S. Murray, T. Gridley, L. A. Wilson et al., 2007 Mutation of a ubiquitously expressed mouse transmembrane protein (Tapt1) causes specific skeletal homeotic transformations. Genetics 175: 699-707.
31. Jaspersen, S. L., and S. Ghosh, 2012 Nuclear envelope insertion of spindle pole bodies and nuclear pore complexes. Nucleus 3: 226-236.
32. Jaspersen, S. L., and R. S. Hawley, 2011 Meiotic pairing as a polo match. Dev. Cell 21: 805-806.
33. Jaspersen, S. L., T. H. Giddings Jr, and M. Winey, 2002 Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J. Cell Biol. 159: 945-956.
34. Jaspersen, S. L., A. E. Martin, G. Glazko, T. H. Giddings Jr, G. Morgan et al., 2006 The Sad1-UNC-84 homology domain in Mps3 interacts with Mps2 to connect the spindle pole body with the nuclear envelope. J. Cell Biol. 174: 665-675.
35. Jaspersen, S. L., and M. Winey, 2004 The budding yeast spindle pole body: structure, duplication, and function. Annu. Rev. Cell Dev. Biol. 20: 1-28.
36. Jay, J. J., J. D. Eblen, Y. Zhang, M. Benson, A. D. Perkins et al., 2012 A systematic comparison of genome-scale clustering algorithms. BMC Bioinformatics 13(Suppl. 10): S7.
37. Jonikas, M. C., S. R. Collins, V. Denic, E. Oh, E. M. Quan et al., 2009 Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323: 1693-1697.
38. Kupke, T., L. Di Cecco, H. M. Muller, A. Neuner, F. Adolf et al., 2011 Targeting of Nbp1 to the inner nuclear membrane is essential for spindle pole body duplication. EMBO J. 30: 3337-3352.
39. Lee, C. Y., M. N. Conrad, and M. E. Dresser, 2012 Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet. 8: e1002730.
40. Lei, K., X. Zhu, R. Xu, C. Shao, T. Xu et al., 2012 Inner nuclear envelope proteins SUN1 and SUN2 play a prominent role in the DNA damage response. Curr. Biol. 22: 1609-1615.
41. Liu, Q., N. Pante, T. Misteli, M. Elsagga, M. Crisp et al., 2007 Functional association of Sun1 with nuclear pore complexes. J. Cell Biol. 178: 785-798.
42. Longtine, M. S., A. McKenzie 3rd, D. J. Demarini, N. G. Shah, A. Wach et al., 1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
43. Makio, T., L. H. Stanton, C. C. Lin, D. S. Goldfarb, K. Weis et al., 2009 The nucleoporins Nup170p and Nup157p are essential for nuclear pore complex assembly. J. Cell Biol. 185: 459-473.
44. Malone, C. J., W. D. Fixsen, H. R. Horvitz, and M. Han, 1999 UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development 126: 3171-3181.
45. Mayer, M. L., S. P. Gygi, R. Aebersold, and P. Hieter, 2001 Identification of RFC(Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae. Mol. Cell 7: 959-970.
46. Mettenleiter, T. C., B. G. Klupp, and H. Granzow, 2006 Herpesvirus assembly: a tale of two membranes. Curr. Opin. Microbiol. 9: 423-429.
47. Miki, F., A. Kurabayashi, Y. Tange, K. Okazaki, M. Shimanuki et al., 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.
48. Morimoto, A., H. Shibuya, X. Zhu, J. Kim, K. Ishiguro et al., 2012 A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J. Cell Biol. 198: 165-172.
49. Nishikawa, S., Y. Terazawa, T. Nakayama, A. Hirata, T. Makio et al., 2003 Nep98p is a component of the yeast spindle pole body and essential for nuclear division and fusion. J. Biol. Chem. 278: 9938-9943.
50. Onischenko, E., L. H. Stanton, A. S. Madrid, T. Kieselbach, and K. Weis, 2009 Role of the Ndc1 interaction network in yeast nuclear pore complex assembly and maintenance. J. Cell Biol. 185: 475-491.
51. Ostlund, C., E. S. Folker, J. C. Choi, E. R. Gomes, G. G. Gundersen et al., 2009 Dynamics and molecular interactions of linker of nucleoskeleton and cytoskeleton (LINC) complex proteins. J. Cell Sci. 122: 4099-4108.
52. Oza, P., and C. L. Peterson, 2010 Opening the DNA repair toolbox: localization of DNA double strand breaks to the nuclear periphery. Cell Cycle 9: 43-49.
53. Oza, P., S. L. Jaspersen, A. Miele, J. Dekker, and C. L. Peterson, 2009 Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev. 23: 912-927.
54. Penkner, A. M., A. Fridkin, J. Gloggnitzer, A. Baudrimont, T. Machacek et al., 2009 Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139: 920-933.
55. Rao, H. B., M. Shinohara, and A. Shinohara, 2011 Mps3 SUN domain is important for chromosome motion and juxtaposition of homologous chromosomes during meiosis. Genes Cells 16: 1081-1096.
56. Razafsky, D., and D. Hodzic, 2009 Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J. Cell Biol. 186: 461-472.
57. Reinders, J., R. P. Zahedi, N. Pfanner, C. Meisinger, and A. Sickmann, 2006 Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J Prot Res 5: 1543-1554.
58. Reynolds, S. M., L. Kall, M. E. Riffle, J. A. Bilmes, and W. S. Noble, 2008 Transmembrane topology and signal peptide prediction using dynamic bayesian networks. PLOS Comput. Biol. 4: e1000213.
59. Santos-Rosa, H., J. Leung, N. Grimsey, S. Peak-Chew, and S. Siniossoglou, 2005 The yeast lipin Smp2 couples phospholipid biosynthesis to nuclear membrane growth. EMBO J. 24: 1931-1941.
60. Sato, A., B. Isaac, C. M. Phillips, R. Rillo, P. M. Carlton et al., 2009 Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139: 907-919.
61. Scarcelli, J. J., C. A. Hodge, and C. N. Cole, 2007 The yeast integral membrane protein Apq12 potentially links membrane dynamics to assembly of nuclear pore complexes. J. Cell Biol. 178: 799-812.
62. Schirmer, E. C., and L. Gerace, 2005 The nuclear membrane proteome: extending the envelope. Trends Biochem. Sci. 30: 551-558.
63. Schober, H., H. Ferreira, V. Kalck, L. R. Gehlen, and S. M. Gasser, 2009 Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev. 23: 928-938.
64. Sheff, M. A., and K. S. Thorn, 2004 Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21: 661-670.
65. Sickmann, A., J. Reinders, Y. Wagner, C. Joppich, R. Zahedi et al., 2003 The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. USA 100: 13207-13212.
66. Siniossoglou, S., H. Santos-Rosa, J. Rappsilber, M. Mann, and E. Hurt, 1998 A novel complex of membrane proteins required for formation of a spherical nucleus. EMBO J. 17: 6449-6464.
67. Sosa, B. A., A. Rothballer, U. Kutay, and T. U. Schwartz, 2012 LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins. Cell 149: 1035-1047.
68. Speese, S. D., J. Ashley, V. Jokhi, J. Nunnari, R. Barria et al., 2012 Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 149: 832-846.
69. Starr, D. A., and H. N. Fridolfsson, 2010 Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu. Rev. Cell Dev. Biol. 26: 421-444.
70. Starr, D. A., and M. Han, 2002 Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 298: 406-409.
71. Talamas, J. A., and M. W. Hetzer, 2011 POM121 and Sun1 play a role in early steps of interphase NPC assembly. J. Cell Biol. 194: 27-37.
72. Tamm, T., A. Grallert, E. P. Grossman, I. Alvarez-Tabares, F. E. Stevens et al., 2011 Brr6 drives the Schizosaccharomyces pombe spindle pole body nuclear envelope insertion/extrusion cycle. J. Cell Biol. 195: 467-484.
73. Tang, X., Y. Jin, and W. Z. Cande, 2006 Bqt2p is essential for initiating telomere clustering upon pheromone sensing in fission yeast. J. Cell Biol. 173: 845-851.
74. Terry, L. J., E. B. Shows, and S. R. Wente, 2007 Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport. Science 318: 1412-1416.
75. Tong, A. H., and C. Boone, 2006 Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 313: 171-192.
76. Tong, A. H., M. Evangelista, A. B. Parsons, H. Xu, G. D. Bader et al., 2001 Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
77. Tong, A. H., G. Lesage, G. D. Bader, H. Ding, H. Xu et al., 2004 Global mapping of the yeast genetic interaction network. Science 303: 808-813.
78. Wang, Q., X. Du, Z. Cai, and M. I. Greene, 2006 Characterization of the structures involved in localization of the SUN proteins to the nuclear envelope and the centrosome. DNA Cell Biol. 25: 554-562.
79. Wang, W., Z. Shi, S. Jiao, C. Chen, H. Wang et al., 2012 Structural insights into SUN-KASH complexes across the nuclear envelope. Cell Res. 22: 1440-1452.
80. Weis, K., 2003 Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 112: 441-451.
81. Wilson, K. L., and S. C. Dawson, 2011 Functional evolution of nuclear structure. J. Cell Biol. 195: 171-181.
82. Winey, M., and K. Bloom, 2012 Mitotic spindle form and function. Genetics 190: 1197-1224.
83. Winzeler, E. A., D. D. Shoemaker, A. Astromoff, H. Liang, K. Anderson et al., 1999 Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
84. Witkin, K. L., J. M. Friederichs, O. Cohen-Fix, and S. L. Jaspersen, 2010 Changes in the nuclear envelope environment affect spindle pole body duplication in Saccharomyces cerevisiae. Genetics 186: 867-883.
85. Zhou, Z., X. Du, Z. Cai, X. Song, H. Zhang et al., 2012 Structure of Sad1- UNC84 homology (SUN) domain defines features of molecular bridge in nuclear envelope. J. Biol. Chem. 287: 5317-5326.