Fission yeast Lem2 and Man1 perform fundamental functions of the animal cell nuclear lamina

Nucleus

Volumn 3, Issue 1, 2012, Pages 60-76

  Gonzalez, Yanira ^a   Saito, Akira ^a   Sazer, Shelley ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Chromosome organization; Fission yeast; HEH domain; LEM domain; Nuclear lamina; Nuclear periphery; Telomere anchoring

Indexed keywords

LEM2 PROTEIN; MAN1 PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS MEMBRANE; DNA BINDING; DNA HELIX; HETEROCHROMATIN; MEMBRANE PERMEABILITY; MEMBRANE STRUCTURE; NONHUMAN; NUCLEAR LAMINA; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SCHIZOSACCHAROMYCES POMBE; TELOMERE;

EID: 84860162529     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.18824     Document Type: Article

References (79)

1. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 2006; 124:573-586. PMID:16469703; http://dx.doi.org/10.1016/j.cell.2005.11.047
2. Hetzer MW, Walther TC, Mattaj IW. Pushing the envelope: structure, function, and dynamics of the nuclear periphery. Annu Rev Cell Dev Biol 2005; 21:347-380. PMID:16212499; http://dx.doi.org/10.1146/annurev.cellbio.21.090704.151152
3. Anderson DJ, Hetzer MW. Reshaping of the endoplasmic reticulum limits the rate for nuclear envelope formation. J Cell Biol 2008; 182:911-924. PMID:18779370; http://dx.doi.org/10.1083/jcb.200805140
4. D'Angelo MA, Hetzer MW. The role of the nuclear envelope in cellular organization. Cell Mol Life Sci 2006; 63:316-332. PMID:16389459; http://dx.doi.org/10.1007/s00018-005-5361-3
5. Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL. The nuclear lamina comes of age. Nat Rev Mol Cell Biol 2005; 6:21-31. PMID:15688064; http://dx.doi.org/10.1038/nrm1550
6. Sazer S. Nuclear envelope: nuclear pore complexity. Curr Biol 2005; 15:R23-R26. PMID:15649347; http://dx.doi.org/10.1016/j.cub.2004.12.015
7. 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; 8:1461-1479. PMID:9285819
8. McIntosh JR, O'Toole ET. Life cycles of yeast spindle pole bodies: getting microtubules into a closed nucleus. Biol Cell 1999; 91:305-312. PMID:10518997; http://dx.doi.org/10.1016/S0248-4900(99)80091-4
9. McCully EK, Robinow CF. Mitosis in the fission yeast Schizosaccharomyces pombe: a comparative study with light and electron microscopy. J Cell Sci 1971; 9:475-507. PMID:4108061
10. Cai M, Huang Y, Ghirlando R, Wilson KL, Craigie R, Clore GM. Solution structure of the constant region of nuclear envelope protein LAP2 reveals two LEM-domain structures: one binds BAF and the other binds DNA. EMBO J 2001; 20:4399-4407. PMID:11500367; http://dx.doi.org/10.1093/emboj/20.16.4399
11. Shumaker DK, Lee KK, Tanhehco YC, Craigie R, Wilson KL. LAP2 binds to BAF.DNA complexes: requirement for the LEM domain and modulation by variable regions. EMBO J 2001; 20:1754-1764. PMID:11285238; http://dx.doi.org/10.1093/emboj/20.7.1754
12. Lee KK, Haraguchi T, Lee RS, Koujin T, Hiraoka Y, Wilson KL. Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J Cell Sci 2001; 114:4567-4573. PMID:11792821
13. Wiesel N, Mattout A, Melcer S, Melamed-Book N, Herrmann H, Medalia O, et al. Laminopathic mutations interfere with the assembly, localization, and dynamics of nuclear lamins. Proc Natl Acad Sci USA 2008; 105:180-185. PMID:18162544; http://dx.doi.org/10.1073/pnas.0708974105
14. Worman HJ, Fong LG, Muchir A, Young SG. Laminopathies and the long strange trip from basic cell biology to therapy. J Clin Invest 2009; 119:1825-1836. PMID:19587457; http://dx.doi.org/10.1172/JCI37679
15. Burke B, Stewart CL. The laminopathies: the functional architecture of the nucleus and its contribution to disease. Annu Rev Genomics Hum Genet 2006; 7:369-405. PMID:16824021; http://dx.doi.org/10.1146/annurev.genom.7.080505.115732
16. Kim Y, Sharov AA, McDole K, Cheng M, Hao H, Fan CM, et al. Mouse B-Type Lamins Are Required for Proper Organogenesis But Not by Embryonic Stem Cells. Science 2011;. PMID:22116031; http://dx.doi.org/10.1126/science.1211222
17. Hirano Y, Iwase Y, Ishii K, Kumeta M, Horigome T, Takeyasu K. Cell cycle-dependent phosphorylation of MAN1. Biochemistry 2009; 48:1636-1643. PMID:19166343; http://dx.doi.org/10.1021/bi802060v
18. Hirano Y, Segawa M, Ouchi FS, Yamakawa Y, Furukawa K, Takeyasu K, et al. Dissociation of emerin from barrierto-autointegration factor is regulated through mitotic phosphorylation of emerin in a xenopus egg cell-free system. J Biol Chem 2005; 280:39925-39933. PMID:16204256; http://dx.doi.org/10.1074/jbc.M503214200
19. Mans BJ, Anantharaman V, Aravind L, Koonin E. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 2004; 3:1612-1637. PMID:15611647; http://dx.doi.org/10.4161/cc.3.12.1316
20. Meier I, Zhou X, Brkljacic J, Rose A, Zhao Q, Xu XM. Targeting proteins to the plant nuclear envelope. Biochem Soc Trans 2010; 38:733-740. PMID:20491658; http://dx.doi.org/10.1042/BST0380733
21. Mattaj IW. Sorting out the nuclear envelope from the endoplasmic reticulum. Nat Rev Mol Cell Biol 2004; 5:65-69. PMID:14663490; http://dx.doi.org/10.1038/nrm1263
22. Shibata Y, Voeltz GK, Rapoport TA. Rough sheets and smooth tubules. Cell 2006; 126:435-439. PMID:16901774; http://dx.doi.org/10.1016/j.cell.2006.07.019
23. Anderson DJ, Hetzer MW. Nuclear envelope formation by chromatin-mediated reorganization of the endoplasmic reticulum. Nat Cell Biol 2007; 9:1160-1166. PMID:17828249; http://dx.doi.org/10.1038/ncb1636
24. Anderson DJ, Vargas JD, Hsiao JP, Hetzer MW. Recruitment of functionally distinct membrane proteins to chromatin mediates nuclear envelope formation in vivo. J Cell Biol 2009; 186:183-191. PMID:19620630; http://dx.doi.org/10.1083/jcb.200901106
25. Lim HWG, Huber G, Torii Y, Hirata A, Miller J, Sazer S. Vesicle-like biomechanics governs important aspects of nuclear geometry in fission yeast. PLoS ONE 2007; 2:e948. PMID:17895989; http://dx.doi.org/10.1371/journal.pone.0000948
26. Gonzalez Y, Meerbrey K, Chong J, Torii Y, Padte NN, Sazer S. 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 2009; 122:2464-2472. PMID:19571115; http://dx.doi.org/10.1242/jcs.049999
27. Demeter J, Morphew M, Sazer S. A mutation in the RCC1-related protein pim1 results in nuclear envelope fragmentation in fission yeast. Proc Natl Acad Sci USA 1995; 92:1436-1440. PMID:7877997; http://dx.doi.org/10.1073/pnas.92.5.1436
28. King MC, Lusk CP, Blobel G. Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 2006; 442:1003-1007. PMID:16929305; http://dx.doi.org/10.1038/nature05075
29. Ohba T, Schirmer EC, Nishimoto T, Gerace L. Energy- and temperature-dependent transport of integral proteins to the inner nuclear membrane via the nuclear pore. J Cell Biol 2004; 167:1051-1062. PMID:15611332; http://dx.doi.org/10.1083/jcb.200409149
30. Misteli T. Beyond the sequence: cellular organization of genome function. Cell 2007; 128:787-800. PMID:17320514; http://dx.doi.org/10.1016/j.cell.2007.01.028
31. Cremer T, Cremer M. Chromosome territories. Cold Spring Harb Perspect Biol 2010; 2:a003889. PMID:20300217; http://dx.doi.org/10.1101/cshperspect.a003889
32. Taddei A, Hediger F, Neumann FR, Gasser SM. The function of nuclear architecture: a genetic approach. Annu Rev Genet 2004; 38:305-345. PMID:15568979; http://dx.doi.org/10.1146/annurev.genet.37.110801.142705
33. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, et al. Life with 6000 genes. Science 1996; 274:546-547. PMID:8849441; http://dx.doi.org/10.1126/science.274.5287.546
34. Eisen JA, Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, et al. The genome sequence of Schizosaccharomyces pombe. Nature 2002; 415:845-848. PMID:11859347; http://dx.doi.org/10.1038/nature725
35. Lusk CP, Blobel G, King MC. Highway to the inner nuclear membrane: rules for the road. Nat Rev Mol Cell Biol 2007; 8:414-420. PMID:17440484; http://dx.doi.org/10.1038/nrm2165
36. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, et al. Global analysis of protein localization in budding yeast. Nature 2003; 425: 686-691. PMID:14562095; http://dx.doi.org/10.1038/nature02026
37. Matsuyama A, Arai R, Yashiroda Y, Shirai A, Kamata A, Sekido S, et al. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 2006; 24:841-847. PMID:16823372; http://dx.doi.org/10.1038/nbt1222
38. Cam HP, Sugiyama T, Chen ES, Chen X, FitzGerald PC, Grewal SI. Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet 2005; 37:809-819. PMID:15976807; http://dx.doi.org/10.1038/ng1602
39. Grund SE, Fischer T, Cabal GG, Antunez O, Perez-Ortin JE, Hurt E. The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. J Cell Biol 2008; 182:897-910. PMID:18762579; http://dx.doi.org/10.1083/jcb.200803098
40. Mekhail K, Seebacher J, Gygi SP, Moazed D. Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 2008; 456:667-670. PMID:18997772; http://dx.doi.org/10.1038/nature07460
41. Goto B, Okazaki K, Niwa O. Cytoplasmic microtubular system implicated in de novo formation of a Rabl-like orientation of chromosomes in fission yeast. J Cell Sci 2001; 114:2427-2435. PMID:11559751
42. Funabiki H, Hagan I, Uzawa S, Yanagida M. Cell cycle-dependent specific positioning and clustering of certromeres and telomeres in fission yeast. J Cell Biol 1993; 121:961-976. PMID:8388878; http://dx.doi.org/10.1083/jcb.121.5.961
43. Chikashige Y, Yamane M, Okamasa K, Tsutsumi C, Kojidani T, Sato M, et al. Membrane proteins Bqt3 and -4 anchor telomeres to the nuclear envelope to ensure chromosomal bouquet formation. J Cell Biol 2009; 187:413-427. PMID:19948484; http://dx.doi.org/10.1083/jcb.200902122
44. Hayashi A, Da-Qiao D, Tsutsumi C, Chikashige Y, Masuda H, Haraguchi T, et al. Localization of gene products using a chromosomally tagged GFP-fusion library in the fission yeast Schizosaccharomyces pombe. Genes Cells 2009; 14:217-225. PMID:19170768; http://dx.doi.org/10.1111/j.1365-2443.2008.01264.x
45. King MC, Drivas TG, Blobel G. A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 2008; 134:427-438. PMID:18692466; http://dx.doi.org/10.1016/j.cell.2008.06.022
46. Prüfert K, Vogel A, Krohne G. The lamin CxxM motif promotes nuclear membrane growth. J Cell Sci 2004; 117:6105-6116. PMID:15546914; http://dx.doi.org/10.1242/jcs.01532
47. Ralle T, Grund C, Franke WW, Stick R. Intranuclear membrane structure formations by CaaX-containing nuclear proteins. J Cell Sci 2004; 117:6095-6104. PMID:15546917; http://dx.doi.org/10.1242/jcs.01528
48. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, et al. The Pfam protein families database. Nucleic Acids Res 2010; 38:D211-D222. PMID:19920124; http://dx.doi.org/10.1093/nar/gkp985
49. Caputo S, Couprie J, Duband-Goulet I, Konde E, Lin F, Braud S, et al. The carboxyl-terminal nucleoplasmic region of MAN1 exhibits a DNA binding winged helix domain. J Biol Chem 2006; 281:18208-18215. PMID: 16648637; http://dx.doi.org/10.1074/jbc.M601980200
50. Yoshida M, Sazer S. Nucleocytoplasmic transport and nuclear envelope integrity in the fission yeast Schizosaccharomyces pombe. Methods 2004; 33:226-238. PMID:15157890; http://dx.doi.org/10.1016/j.ymeth.2003.11.018
51. Grallert A, Krapp A, Bagley S, Simanis V, Hagan IM. 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 2004; 18:1007-1021. PMID:15132994; http://dx.doi.org/10.1101/gad.296204
52. Miki F, Kurabayashi A, Tange Y, Okazaki K, Shimanuki M, Niwa O. Two-hybrid search for proteins that interact with Sad1 and Kms1, two membranebound components of the spindle pole body in fission yeast. Mol Genet Genomics 2004; 270:449-461. PMID:14655046; http://dx.doi.org/10.1007/s00438-003-0938-8
53. Nabeshima K, Nakagawa T, Straight AF, Murray A, Chikashige Y, Yamashita YM, et al. Dynamics of centromeres during metaphase-anaphase transition in fission yeast: Dis1 is implicated in force balance in metaphase bipolar spindle. Mol Biol Cell 1998; 9: 3211-3225. PMID:9802907
54. Wright R, Basson M, D'Ari L, Rine J. Increased amounts of HMG-CoA reductase induce "karmellae": a proliferation of stacked membrane pairs surrounding the yeast nucleus. J Cell Biol 1988; 107:101-114. PMID:3292536; http://dx.doi.org/10.1083/jcb.107.1.101
55. Pidoux AL, Armstrong J. The BiP protein and the endoplasmic reticulum of Schizosaccharomyces pombe: fate of the nuclear envelope during cell division. J Cell Sci 1993; 105:1115-1120. PMID:8227200
56. Tomlin GC, Morrell JL, Gould KL. The spindle pole body protein Cdc11p links Sid4p to the fission yeast septation initiation network. Mol Biol Cell 2002; 13:1203-1214. PMID:11950932; http://dx.doi.org/10.1091/mbc.01-09-0455
57. Jin Y, Uzawa S, Cande WZ. Fission yeast mutants affecting telomere clustering and meiosis-specific spindle pole body integrity. Genetics 2002; 160:861-876. PMID:11901107
58. Hediger F, Taddei A, Neumann FR, Gasser SM. Methods for visualizing chromatin dynamics in living yeast. Methods Enzymol 2004; 375:345-365. PMID: 14870677; http://dx.doi.org/10.1016/S0076-6879(03)75022-8
59. Ma Y, Cai S, Lv Q, Jiang Q, Zhang Q, Sodmergen, et al. Lamin B receptor plays a role in stimulating nuclear envelope production and targeting membrane vesicles to chromatin during nuclear envelope assembly through direct interaction with importin beta. J Cell Sci 2007; 120:520-530. PMID:17251381; http://dx.doi.org/10.1242/jcs.03355
60. Smith S, Blobel G. Colocalization of vertebrate lamin B and lamin B receptor (LBR) in nuclear envelopes and in LBR-induced membrane stacks of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1994; 91:10124-10128. PMID:7937849; http://dx.doi.org/10.1073/pnas.91.21.10124
61. Hattier T, Andrulis ED, Tartakoff AM. Immobility, inheritance and plasticity of shape of the yeast nucleus. BMC Cell Biol 2007; 8:47. PMID:17996101; http://dx.doi.org/10.1186/1471-2121-8-47
62. Schirmer EC, Guan T, Gerace L. Involvement of the lamin rod domain in heterotypic lamin interactions important for nuclear organization. J Cell Biol 2001; 153:479-489. PMID:11331300; http://dx.doi.org/10.1083/jcb.153.3.479
63. Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, Gordon LB, et al. Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 2004; 101:8963-8968. PMID:15184648; http://dx.doi.org/10.1073/pnas.0402943101
64. Campbell JL, Lorenz A, Witkin KL, Hays T, Loidl J, Cohen-Fix O. Yeast nuclear envelope subdomains with distinct abilities to resist membrane expansion. Mol Biol Cell 2006; 17:1768-1778. PMID:16467382; http://dx.doi.org/10.1091/mbc.E05-09-0839
65. Yewdell WT, Colombi P, Makhnevych T, Lusk CP. Lumenal interactions in nuclear pore complex assembly and stability. Mol Biol Cell 2011; 22:1375-1388. PMID:21346187; http://dx.doi.org/10.1091/mbc.E10-06-0554
66. Tallada VA, Tanaka K, Yanagida M, Hagan IM. The S. pombe mitotic regulator Cut12 promotes spindle pole body activation and integration into the nuclear envelope. J Cell Biol 2009; 185:875-888. PMID:19487457; http://dx.doi.org/10.1083/jcb.200812108
67. Sazer S, Nurse P. A fission yeast RCC1-related protein is required for the mitosis to interphase transition. EMBO J 1994; 13:606-615. PMID:8313905
68. Hiraoka Y, Maekawa H, Asakawa H, Chikashige Y, Kojidani T, Osakada H, et al. Inner Nuclear Membrane Protein Ima1 is Dispensable for Intranuclear Positioning of Centromeres. Genes Cells 2011; 16:1000-1011. PMID: 21880100; http://dx.doi.org/10.1111/j.1365-2443.2011.01544.x
69. Steglich B, Filion G, van Steensel B, Ekwall K. The inner nuclear membrane proteins Man1 and Ima1 link to two different types of chromatin at the nuclear periphery in S. pombe. Nucleus 2012; 3:78-88. PMID:22156748; http://dx.doi.org/10.4161/nucl.3.1.18825
70. Wilson KL, Dawson SC. Evolution: functional evolution of nuclear structure. J Cell Biol 2011; 195:171-181. PMID:22006947; http://dx.doi.org/10.1083/jcb.201103171
71. Moreno S, Klar A, Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 1991; 194:795-823. PMID:2005825; http://dx.doi.org/10.1016/0076-6879(91)94059-L
72. Suga M, Hatakeyama T. A rapid and simple procedure for high-efficiency lithium acetate transformation of cryopreserved Schizosaccharomyces pombe cells. Yeast 2005; 22:799-804 PMID:16088874; http://dx.doi.org/10.1002/yea.1247
73. Maundrell K. Nmt1 of fission yeast. J Biol Chem 1990; 265:10857-10864. PMID:2358444
74. Forsburg SL. Comparison of Schizosaccharomyces pombe expression systems. Nucleic Acids Res 1993; 21: 2955-2956. PMID:8332516; http://dx.doi.org/10.1093/nar/21.12.2955
75. Matsuyama A, Shirai A, Yashiroda Y, Kamata A, Horinouchi S, Yoshida M. PDUAL, a multipurpose, multicopy vector capable of chromosomal integration in fission yeast. Yeast 2004; 21:1289-1305. PMID: 15546162; http://dx.doi.org/10.1002/yea.1181
76. Forsburg SL, Sherman DA. General purpose tagging vectors for fission yeast. Gene 1997; 191:191-195. PMID: 9218719; http://dx.doi.org/10.1016/S0378-1119(97)00058-9
77. Xu Y, Gong Z. Adaptation of inverse PCR to generate an internal deletion. Biotechniques 1999; 26:639-641. PMID:10343901
78. Bähler J, Wu JQ, Longtine MS, Shah NG, McKenzie A, 3rd, Steever AB, et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 1998; 14:943-951. PMID:9717240; http://dx.doi.org/10.1002/(SICI)1097-0061(199807)14:10,943::AID-YEA292.3 .0.CO;2-Y
79. Giddings TH, Jr., O'Toole ET, Morphew M, Mastronarde DN, McIntosh JR, Winey M. Using rapid freeze and freeze-substitution for the preparation of yeast cells for electron microscopy and three-dimensional analysis. Methods Cell Biol 2001; 67:27-42. PMID:11550475; http://dx.doi.org/10.1016/S0091-679X(01)67003-1