Brr6 drives the Schizosaccharomyces pombe spindle pole body nuclear envelope insertion/extrusion cycle

Journal of Cell Biology

Volumn 195, Issue 3, 2011, Pages 467-484

  Tamm, Tiina ^a,b   Grallert, Agnes ^a   Grossman, Emily P S ^a   Alvarez Tabares, Isabel ^a   Stevens, Frances E ^a,c   Hagan, Iain M ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF TARTU   (Estonia)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BRR6 PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN; STEROL; UNCLASSIFIED DRUG; BRR6 PROTEIN, S POMBE; MEMBRANE PROTEIN; NUCLEAR PROTEIN;

ANAPHASE; ARTICLE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; EUKARYOTE; GENE INSERTION; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SCHIZOSACCHAROMYCES POMBE; SPINDLE POLE BODY; CELL NUCLEUS; CYTOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; MITOSIS SPINDLE; SCHIZOSACCHAROMYCES; ULTRASTRUCTURE;

EUKARYOTA; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

CELL NUCLEUS; CYTOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; MEMBRANE PROTEINS; MITOSIS; MITOTIC SPINDLE APPARATUS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84855754191     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201106076     Document Type: Article

References (70)

1. Adams, I.R., and J.V. Kilmartin. 2000. Spindle pole body duplication: a model for centrosome duplication? Trends Cell Biol. 10:329-335. http://dx.doi.org/10.1016/S0962-8924(00)01798-0
2. Alber, F., S. Dokudovskaya, L.M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, R. Williams, B.T. Chait, et al. 2007. The molecular architecture of the nuclear pore complex. Nature. 450:695-701. http://dx.doi.org/10.1038/nature06405
3. Araki, Y., C.K. Lau, H. Maekawa, S.L. Jaspersen, T.H. Giddings Jr., E. Schiebel, and M. Winey. 2006. The Saccharomyces cerevisiae spindle pole body (SPB) component Nbp1p is required for SPB membrane insertion and interacts with the integral membrane proteins Ndc1p and Mps2p. Mol. Biol. Cell. 17:1959-1970. http://dx.doi.org/10.1091/mbc.E05-07-0668
4. Bähler, J., J.Q. Wu, M.S. Longtine, N.G. Shah, A. McKenzie III, A.B. Steever, A. Wach, P. Philippsen, and J.R. Pringle. 1998. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast. 14:943-951. http://dx.doi.org/10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y
5. Baï, S.W., J. Rouquette, M. Umeda, W. Faigle, D. Loew, S. Sazer, and V. Doye. 2004. The fission yeast Nup107-120 complex functionally interacts with the small GTPase Ran/Spi1 and is required for mRNA export, nuclear pore distribution, and proper cell division. Mol. Cell. Biol. 24:6379-6392. http://dx.doi.org/10.1128/MCB.24.14.6379-6392.2004
6. Barbet, N., W.J. Muriel, and A.M. Carr. 1992. Versatile shuttle vectors and genomic libraries for use with Schizosaccharomyces pombe. Gene. 114: 59-66. http://dx.doi.org/10.1016/0378-1119(92)90707-V
7. Bridge, A.J., M. Morphew, R. Bartlett, and I.M. Hagan. 1998. The fission yeast SPB component Cut12 links bipolar spindle formation to mitotic control. Genes Dev. 12:927-942. http://dx.doi.org/10.1101/gad.12.7.927
8. Broek, D., R. Bartlett, K. Crawford, and P. Nurse. 1991. Involvement of p34cdc2 in establishing the dependency of S phase on mitosis. Nature. 349:388-393. http://dx.doi.org/10.1038/349388a0
9. Broughton, J., D. Swennen, B.M. Wilkinson, P. Joyet, C. Gaillardin, and C.J. Stirling. 1997. Cloning of SEC61 homologues from Schizosaccharomyces pombe and Yarrowia lipolytica reveals the extent of functional conservation within this core component of the ER translocation machinery. J. Cell Sci. 110:2715-2727.
10. Byers, B., and L. Goetsch. 1975. Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae. J. Bacteriol. 124:511-523.
11. Chial, H.J., M.P. Rout, T.H. Giddings, and M. Winey. 1998. Saccharomyces cerevisiae Ndc1p is a shared component of nuclear pore complexes and spindle pole bodies. J. Cell Biol. 143:1789-1800. http://dx.doi.org/10.1083/jcb.143.7.1789
12. Craven, R.A., D.J. Griffiths, K.S. Sheldrick, R.E. Randall, I.M. Hagan, and A.M. Carr. 1998. Vectors for the expression of tagged proteins in Schizosaccharomyces pombe. Gene. 221:59-68. http://dx.doi.org/10.1016/S0378-1119(98)00434-X
13. de Bruyn Kops, A., and C. Guthrie. 2001. An essential nuclear envelope integral membrane protein, Brr6p, required for nuclear transport. EMBO J. 20:4183-4193. http://dx.doi.org/10.1093/emboj/20.15.4183
14. Decottignies, A., I. Sanchez-Perez, and P. Nurse. 2003. Schizosaccharomyces pombe essential genes: a pilot study. Genome Res. 13:399-406. http://dx.doi.org/10.1101/gr.636103
15. Ding, R., K.L. McDonald, and J.R. McIntosh. 1993. Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J. Cell Biol. 120:141-151. http://dx.doi.org/10.1083/jcb.120.1.141
16. Ding, R., R.R. West, D.M. Morphew, B.R. Oakley, and J.R. McIntosh. 1997. The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds. Mol. Biol. Cell. 8:1461-1479.
17. Finn, R.D., J. Tate, J. Mistry, P.C. Coggill, S.J. Sammut, H.R. Hotz, G. Ceric, K. Forslund, S.R. Eddy, E.L. Sonnhammer, and A. Bateman. 2008. The Pfam protein families database. Nucleic Acids Res. 36:D281-D288. http://dx.doi.org/10.1093/nar/gkm960
18. Fischer, T., S. Rodríguez-Navarro, G. Pereira, A. Rácz, E. Schiebel, and E. Hurt. 2004. Yeast centrin Cdc31 is linked to the nuclear mRNA export machinery. Nat. Cell Biol. 6:840-848. http://dx.doi.org/10.1038/ncb1163
19. Flory, M.R., M.M. Morphew, J.D. Joseph, A.R. Means, and T.N. Davis. 2002. Pcp1p, an Spc110p-related calmodulin target at the centrosome of the fission yeast Schizosaccharomyces pombe. Cell Growth Differ. 13:47-58.
20. Fujiu, K., and O. Numata. 1999. Localization of microtubules during macronuclear division in Tetrahymena and possible involvement of macronuclear microtubules in 'amitotic' chromatin distribution. Cell Struct. Funct. 24:401-404. http://dx.doi.org/10.1247/csf.24.401
21. Funabiki, H., I. Hagan, S. Uzawa, and M. Yanagida. 1993. Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J. Cell Biol. 121:961-976. http://dx.doi.org/10.1083/jcb.121.5.961
22. Gonzalez, Y., K. Meerbrey, J. Chong, Y. Torii, N.N. Padte, and S. Sazer. 2009. Nuclear shape, growth and integrity in the closed mitosis of fission yeast depend on the Ran-GTPase system, the spindle pole body and the endoplasmic reticulum. J. Cell Sci. 122:2464-2472. http://dx.doi.org/10.1242/jcs.049999
23. Goto, B., K. Okazaki, and O. Niwa. 2001. Cytoplasmic microtubular system implicated in de novo formation of a Rabl-like orientation of chromosomes in fission yeast. J. Cell Sci. 114:2427-2435.
24. Grallert, A., A. Krapp, S. Bagley, V. Simanis, and I.M. Hagan. 2004. Recruitment of NIMA kinase shows that maturation of the S. pombe spindle-pole body occurs over consecutive cell cycles and reveals a role for NIMA in modulating SIN activity. Genes Dev. 18:1007-1021. http://dx.doi.org/10.1101/gad.296204
25. + associates with the fission yeast spindle pole body and is essential for viability. J. Cell Biol. 129:1033-1047. http://dx.doi.org/10.1083/jcb.129.4.1033
26. Hagan, I.M., P.N. Riddle, and J.S. Hyams. 1990. Intramitotic controls in the fission yeast Schizosaccharomyces pombe: the effect of cell size on spindle length and the timing of mitotic events. J. Cell Biol. 110:1617-1621. http://dx.doi.org/10.1083/jcb.110.5.1617
27. Heath, I.B. 1980. Variant mitoses in lower eukaryotes: indicators of the evolution of mitosis. Int. Rev. Cytol. 64:1-80. http://dx.doi.org/10.1016/S0074-7696(08)60235-1
28. Hodge, C.A., V. Choudhary, M.J. Wolyniak, J.J. Scarcelli, R. Schneiter, and C.N. Cole. 2010. Integral membrane proteins Brr6 and Apq12 link assembly of the nuclear pore complex to lipid homeostasis in the endoplasmic reticulum. J. Cell Sci. 123:141-151. http://dx.doi.org/10.1242/jcs.055046
29. Ito, T., T. Chiba, R. Ozawa, M. Yoshida, M. Hattori, and Y. Sakaki. 2001. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA. 98:4569-4574. http://dx.doi.org/10.1073/pnas.061034498
30. 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. http://dx.doi.org/10.1083/jcb.200208169
31. Jaspersen, S.L., A.E. Martin, G. Glazko, T.H. Giddings Jr., G. Morgan, A. Mushegian, and M. Winey. 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. http://dx.doi.org/10.1083/jcb.200601062
32. Kanbe, T., Y. Hiraoka, K. Tanaka, and M. Yanagida. 1990. The transition of cells of the fission yeast beta-tubulin mutant nda3-311 as seen by freezesubstitution electron microscopy. Requirement of functional tubulin for spindle pole body duplication. J. Cell Sci. 96:275-282.
33. Kilmartin, J.V. 2003. Sfi1p has conserved centrin-binding sites and an essential function in budding yeast spindle pole body duplication. J. Cell Biol. 162:1211-1221. http://dx.doi.org/10.1083/jcb.200307064
34. King, M.C., T.G. Drivas, and G. Blobel. 2008. A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell. 134:427-438. http://dx.doi.org/10.1016/j.cell.2008.06.022
35. Kniola, B., E. O'Toole, J.R. McIntosh, B. Mellone, R. Allshire, S. Mengarelli, K. Hultenby, and K. Ekwall. 2001. The domain structure of centromeres is conserved from fission yeast to humans. Mol. Biol. Cell. 12:2767-2775.
36. Kohli, J., H. Hottinger, P. Munz, A. Strauss, and P. Thuriaux. 1977. Genetic mapping in Schizosaccharomyces pombe by mitotic and meiotic analysis and induced haploidization. Genetics. 87:471-489.
37. Kubai, D.F. 1976. The evolution of the mitotic spindle. Int. Rev. Cytol. 43:167-227. http://dx.doi.org/10.1016/S0074-7696(08)60069-8
38. Lo Presti, L., M. Cockell, L. Cerutti, V. Simanis, and P.M. Hauser. 2007. Functional characterization of Pneumocystis carinii brl1 by transspecies complementation analysis. Eukaryot. Cell. 6:2448-2452. http://dx.doi.org/10.1128/EC.00321-07
39. MacIver, F.H., D.M. Glover, and I.M. Hagan. 2003. A 'marker switch' approach for targeted mutagenesis of genes in Schizosaccharomyces pombe. Yeast. 20:587-594. http://dx.doi.org/10.1002/yea.983
40. McCully, E.K., and C.F. Robinow. 1971. Mitosis in the fission yeast Schizosaccharomyces pombe: a comparative study with light and electron microscopy. J. Cell Sci. 9:475-507.
41. Miao, M., K.J. Ryan, and S.R. Wente. 2006. The integral membrane protein Pom34p functionally links nucleoporin subcomplexes. Genetics. 172:1441-1457. http://dx.doi.org/10.1534/genetics.105.052068
42. Miki, F., A. Kurabayashi, Y. Tange, K. Okazaki, M. Shimanuki, and O. Niwa. 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. http://dx.doi.org/10.1007/s00438-003-0938-8
43. Mitchison, J.M., and B.L.A. Carter. 1975. Cell cycle analysis. In Methods in Cell Biology. Vol. 11. D.M. Prescott, editor. Academic Press, New York. 201-219.
44. Moens, P.B. 1976. Spindle and kinetochore morphology of Dictyostelium discoideum. J. Cell Biol. 68:113-122. http://dx.doi.org/10.1083/jcb.68.1.113
45. Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795-823. http://dx.doi.org/10.1016/0076-6879(91)94059-L
46. Morgan, B.A., F.L. Conlon, M. Manzanares, J.B.A. Millar, N. Kanuga, J. Sharpe, R. Krumlauf, J.C. Smith, and S.G. Sedgwick. 1996. Transposon tools for recombinant DNA manipulation: characterization of transcriptional regulators from yeast, Xenopus, and mouse. Proc. Natl. Acad. Sci. USA. 93:2801-2806. http://dx.doi.org/10.1073/pnas.93.7.2801
47. Muñoz-Centeno, M.C., S. McBratney, A. Monterrosa, B. Byers, C. Mann, and M. Winey. 1999. Saccharomyces cerevisiae MPS2 encodes a membrane protein localized at the spindle pole body and the nuclear envelope. Mol. Biol. Cell. 10:2393-2406.
48. Murray, S. 2008. High pressure freezing and freeze substitution of Schizosaccharomyces pombe and Saccharomyces cerevisiae for TEM. Methods Cell Biol. 88:3-17. http://dx.doi.org/10.1016/S0091-679X(08)00401-9
49. Niepel, M., C. Strambio-de-Castillia, J. Fasolo, B.T. Chait, and M.P. Rout. 2005. The nuclear pore complex-associated protein, Mlp2p, binds to the yeast spindle pole body and promotes its efficient assembly. J. Cell Biol. 170:225-235. http://dx.doi.org/10.1083/jcb.200504140
50. Nurse, P. 1975. Genetic control of cell size at cell division in yeast. Nature. 256:547-551. http://dx.doi.org/10.1038/256547a0
51. Ogbadoyi, E., K. Ersfeld, D. Robinson, T. Sherwin, and K. Gull. 2000. Architecture of the Trypanosoma brucei nucleus during interphase and mitosis. Chromosoma. 108:501-513. http://dx.doi.org/10.1007/s004120050402
52. 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. http://dx.doi.org/10.1083/jcb.200810030
53. Paoletti, A., N. Bordes, R. Haddad, C.L. Schwartz, F. Chang, and M. Bornens. 2003. Fission yeast cdc31p is a component of the half-bridge and controls SPB duplication. Mol. Biol. Cell. 14:2793-2808. http://dx.doi.org/10.1091/mbc.E02-10-0661
54. Petersen, J., J. Paris, M. Willer, M. Philippe, and I.M. Hagan. 2001. The S. pombe aurora-related kinase Ark1 associates with mitotic structures in a stage dependent manner and is required for chromosome segregation. J. Cell Sci. 114:4371-4384.
55. Poloni, D., and V. Simanis. 2002. A DMSO-sensitive conditional mutant of the fission yeast orthologue of the Saccharomyces cerevisiae SEC13 gene is defective in septation. FEBS Lett. 511:85-89. http://dx.doi.org/10.1016/S0014-5793(01)03285-9
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. http://dx.doi.org/10.1083/jcb.200906068
57. Saitoh, Y.H., K. Ogawa, and T. Nishimoto. 2005. Brl1p - a novel nuclear envelope protein required for nuclear transport. Traffic. 6:502-517. http://dx.doi.org/10.1111/j.1600-0854.2005.00295.x
58. Schmidt, H. 1993. Effective long range mapping in Schizosaccharomyces pombe with the help of swi5. Curr. Genet. 24:271-273. http://dx.doi.org/10.1007/BF00351803
59. Schramm, C., S. Elliott, A. Shevchenko, and E. Schiebel. 2000. The Bbp1p-Mps2p complex connects the SPB to the nuclear envelope and is essential for SPB duplication. EMBO J. 19:421-433. http://dx.doi.org/10.1093/emboj/19.3.421
60. Sezen, B., M. Seedorf, and E. Schiebel. 2009. The SESA network links duplication of the yeast centrosome with the protein translation machinery. Genes Dev. 23:1559-1570. http://dx.doi.org/10.1101/gad.524209
61. Sohrmann, M., S. Schmidt, I. Hagan, and V. Simanis. 1998. Asymmetric segregation on spindle poles of the Schizosaccharomyces pombe septuminducing protein kinase Cdc7p. Genes Dev. 12:84-94. http://dx.doi.org/10.1101/gad.12.1.84
62. Tallada, V.A., K. Tanaka, M. Yanagida, and I.M. Hagan. 2009. The S. pombe mitotic regulator Cut12 promotes spindle pole body activation and integration into the nuclear envelope. J. Cell Biol. 185:875-888. http://dx.doi.org/10.1083/jcb.200812108
63. Tanaka, K., J. Petersen, F.H. MacIver, D.P. Mulvihill, D.M. Glover, and I.M. Hagan. 2001. The role of Plo1 kinase in mitotic commitment and septation in Schizosaccharomyces pombe. EMBO J. 20:1259-1270. http://dx.doi.org/10.1093/emboj/20.6.1259
64. Toda, T., K. Umesono, A. Hirata, and M. Yanagida. 1983. Cold-sensitive nuclear division arrest mutants of the fission yeast Schizosaccharomyces pombe. J. Mol. Biol. 168:251-270. http://dx.doi.org/10.1016/S0022-2836(83)80017-5
65. Uemura, T., H. Ohkura, Y. Adachi, K. Morino, K. Shiozaki, and M. Yanagida. 1987. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell. 50:917-925. http://dx.doi.org/10.1016/0092-8674(87)90518-6
66. Uzawa, S., F. Li, Y. Jin, K.L. McDonald, M.B. Braunfeld, D.A. Agard, and W.Z. Cande. 2004. Spindle pole body duplication in fission yeast occurs at the G1/S boundary but maturation is blocked until exit from S by an event downstream of cdc10+. Mol. Biol. Cell. 15:5219-5230. http://dx.doi.org/10.1091/mbc.E04-03-0255
67. West, R.R., E.V. Vaisberg, R. Ding, P. Nurse, and J.R. McIntosh. 1998. cut11(+): A gene required for cell cycle-dependent spindle pole body anchoring in the nuclear envelope and bipolar spindle formation in Schizosaccharomyces pombe. Mol. Biol. Cell. 9:2839-2855.
68. 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. http://dx.doi.org/10.1534/genetics.110.119149
69. Wozniak, R.W., G. Blobel, and M.P. Rout. 1994. POM152 is an integral protein of the pore membrane domain of the yeast nuclear envelope. J. Cell Biol. 125:31-42. http://dx.doi.org/10.1083/jcb.125.1.31
70. Yoshida, M., and S. Sazer. 2004. Nucleocytoplasmic transport and nuclear envelope integrity in the fission yeast Schizosaccharomyces pombe. Methods. 33:226-238. http://dx.doi.org/10.1016/j.ymeth.2003.11.018