The nucleoporin ELYS/Mel28 regulates nuclear envelope subdomain formation in HeLa cells

Nucleus

Volumn 3, Issue 2, 2012, Pages

  Clever, Michaela ^a   Funakoshi, Tomoko ^a   Mimura, Yasuhiro ^a   Takagi, Masatoshi ^a   Imamoto, Naoko ^a  

^a RIKEN   (Japan)

Author keywords

ELYS Mel28; Inner nuclear membrane; Lamin B receptor; Nuclear envelope; Nuclear envelope subdomains; Nuclear lamins; Nuclear pore complex

Indexed keywords

BARRIER TO AUTOINTEGRATION FACTOR; EMERIN; LAMIN B; NUCLEAR PROTEIN; NUCLEOPORIN; PROTEIN ELYS; PROTEIN LAP2 ALPHA; PROTEIN MEL28; PROTEIN NUP107; PROTEIN NUP160; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS MEMBRANE; CHROMOSOME; HELA CELL; HUMAN; HUMAN CELL; MITOSIS; NUCLEAR PORE COMPLEX; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

EID: 84859529827     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.3.2.19595     Document Type: Article

References (79)

1. Hetzer MW, Walther TC, Mattaj IW. Pushing the envelope: structure, function, and dynamics of the nuclear periphery. Annu Rev Cell Dev Biol 2005; 21:347-80; http://dx.doi.org/10.1146/annurev.cellbio.21.090704.151152
2. D'Angelo MA, Hetzer MW. The role of the nuclear envelope in cellular organization. Cell Mol Life Sci 2006; 63:316-32; http://dx.doi.org/10.1007/s00018-005-5361-3
3. Watson ML. The nuclear envelope; its structure and relation to cytoplasmic membranes. J Biophys Biochem Cytol 1955; 1:257-70; http://dx.doi.org/10.1083/jcb.1.3.257
4. Foisner R. Cell cycle dynamics of the nuclear envelope. ScientificWorldJournal 2003; 3:1-20; http://dx.doi.org/10.1100/tsw.2003.06
5. Hetzer MW. The nuclear envelope. Cold Spring Harb Perspect Biol 2010; 2:a000539; http://dx.doi.org/10.1101/cshperspect.a000539
6. Goldman RD, Gruenbaum Y, Moir RD, Shumaker DK, Spann TP. Nuclear lamins: building blocks of nuclear architecture. Genes Dev 2002; 16:533-47; http://dx.doi.org/10.1101/gad.960502
7. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, et al. The molecular architecture of the nuclear pore complex. Nature 2007; 450:695-701; http://dx.doi.org/10.1038/nature06405
8. Beck M, Lucić V, Förster F, Baumeister W, Medalia O. Snapshots of nuclear pore complexes in action captured by cryo-electron tomography. Nature 2007; 449:611-5; http://dx.doi.org/10.1038/nature06170
9. Hoelz A, Debler EW, Blobel G. The structure of the nuclear pore complex. Annu Rev Biochem 2011; 80:613-43; http://dx.doi.org/10.1146/annurev-biochem-060109-151030
10. Conti E, Izaurralde E. Nucleocytoplasmic transport enters the atomic age. Curr Opin Cell Biol 2001; 13: 310-9; http://dx.doi.org/10.1016/S0955-0674(00)00213-1
11. Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 2000; 148:635-51; http://dx.doi.org/10.1083/jcb.148.4.635
12. Madrid AS, Weis K. Nuclear transport is becoming crystal clear. Chromosoma 2006; 115:98-109; http://dx.doi.org/10.1007/s00412-005-0043-3
13. Mansfeld J, Güttinger S, Hawryluk-Gara LA, Panté N, Mall M, Galy V, et al. The conserved transmembrane nucleoporin NDC1 is required for nuclear pore complex assembly in vertebrate cells. Mol Cell 2006; 22:93-103; http://dx.doi.org/10.1016/j.molcel.2006.02.015
14. Hallberg E, Wozniak RW, Blobel G. An integral membrane protein of the pore membrane domain of the nuclear envelope contains a nucleoporin-like region. J Cell Biol 1993; 122:513-21; http://dx.doi.org/10.1083/jcb.122.3.513
15. Gerace L, Ottaviano Y, Kondor-Koch C. Identification of a major polypeptide of the nuclear pore complex. J Cell Biol 1982; 95:826-37; http://dx.doi.org/10.1083/jcb.95.3.826
16. Wilson KL, Berk JM. The nuclear envelope at a glance. J Cell Sci 2010; 123:1973-8; http://dx.doi.org/10.1242/jcs.019042
17. Schirmer EC, Foisner R. Proteins that associate with lamins: many faces, many functions. Exp Cell Res 2007; 313:2167-79; http://dx.doi.org/10.1016/j.yexcr.2007.03.012
18. Worman HJ, Bonne G. "Laminopathies": a wide spectrum of human diseases. Exp Cell Res 2007; 313:2121-33; http://dx.doi.org/10.1016/j.yexcr.2007.03.028
19. Maeshima K, Yahata K, Sasaki Y, Nakatomi R, Tachibana T, Hashikawa T, et al. Cell-cycle-dependent dynamics of nuclear pores: pore-free islands and lamins. J Cell Sci 2006; 119:4442-51; http://dx.doi.org/10.1242/jcs.03207
20. Goldberg MW, Fiserova J, Huttenlauch I, Stick R. A new model for nuclear lamina organization. Biochem Soc Trans 2008; 36:1339-43; http://dx.doi.org/10.1042/BST0361339
21. Shimi T, Pfleghaar K, Kojima S, Pack CG, Solovei I, Goldman AE, et al. The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev 2008; 22:3409-21; http://dx.doi.org/10.1101/gad.1735208
22. Furukawa K, Ishida K, Tsunoyama TA, Toda S, Osoda S, Horigome T, et al. A-type and B-type lamins initiate layer assembly at distinct areas of the nuclear envelope in living cells. Exp Cell Res 2009; 315:1181-9; http://dx.doi.org/10.1016/j.yexcr.2008.12.024
23. Kutay U, Hetzer MW. Reorganization of the nuclear envelope during open mitosis. Curr Opin Cell Biol 2008; 20:669-77; http://dx.doi.org/10.1016/j.ceb.2008.09.010
24. Haraguchi T, Koujin T, Hayakawa T, Kaneda T, Tsutsumi C, Imamoto N, et al. Live fluorescence imaging reveals early recruitment of emerin, LBR, RanBP2, and Nup153 to reforming functional nuclear envelopes. J Cell Sci 2000; 113:779-94
25. Haraguchi T, Kojidani T, Koujin T, Shimi T, Osakada H, Mori C, et al. Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly. J Cell Sci 2008; 121:2540-54; http://dx.doi.org/10.1242/jcs.033597
26. Wagner N, Krohne G. LEM-Domain proteins: new insights into lamin-interacting proteins. Int Rev Cytol 2007; 261:1-46; http://dx.doi.org/10.1016/S0074-7696(07)61001-8
27. Duband-Goulet I, Courvalin JC. Inner nuclear membrane protein LBR preferentially interacts with DNA secondary structures and nucleosomal linker. Biochemistry 2000; 39:6483-8; http://dx.doi.org/10.1021/bi992908b
28. Ye Q, Worman HJ. Primary structure analysis and lamin B and DNA binding of human LBR, an integral protein of the nuclear envelope inner membrane. J Biol Chem 1994; 269:11306-11
29. Lechner MS, Schultz DC, Negorev D, Maul GG, Rauscher FJ, 3rd. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem Biophys Res Commun 2005; 331:929-37; http://dx.doi.org/10.1016/j.bbrc.2005.04.016
30. Martins SB, Eide T, Steen RL, Jahnsen T, Skålhegg B S, Collas P. HA95 is a protein of the chromatin and nuclear matrix regulating nuclear envelope dynamics. J Cell Sci 2000; 113:3703-13
31. Guarda A, Bolognese F, Bonapace IM, Badaracco G. Interaction between the inner nuclear membrane lamin B receptor and the heterochromatic methyl binding protein, MeCP2. Exp Cell Res 2009; 315:1895-903; http://dx.doi.org/10.1016/j.yexcr.2009.01.019
32. 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; 120:520-30; http://dx.doi.org/10.1242/jcs.03355
33. Lu X, Shi Y, Lu Q, Ma Y, Luo J, Wang Q, et al. Requirement for lamin B receptor and its regulation by importin beta and phosphorylation in nuclear envelope assembly during mitotic exit. J Biol Chem 2010; 285:33281-93; http://dx.doi.org/10.1074/jbc.M110.102368
34. Silve S, Dupuy PH, Ferrara P, Loison G. Human lamin B receptor exhibits sterol C14-reductase activity in Saccharomyces cerevisiae. Biochim Biophys Acta 1998; 1392:233-44
35. Collas P, Courvalin JC, Poccia D. Targeting of membranes to sea urchin sperm chromatin is mediated by a lamin B receptor-like integral membrane protein. J Cell Biol 1996; 135:1715-25; http://dx.doi.org/10.1083/jcb.135.6.1715
36. Pyrpasopoulou A, Meier J, Maison C, Simos G, Georgatos SD. The lamin B receptor (LBR) provides essential chromatin docking sites at the nuclear envelope. EMBO J 1996; 15:7108-19
37. 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; 186:183-91; http://dx.doi.org/10.1083/jcb.200901106
38. Hoffmann K, Sperling K, Olins AL, Olins DE. The granulocyte nucleus and lamin B receptor: avoiding the ovoid. Chromosoma 2007; 116:227-35; http://dx.doi.org/10.1007/s00412-007-0094-8
39. Kimura N, Takizawa M, Okita K, Natori O, Igarashi K, Ueno M, et al. Identification of a novel transcription factor, ELYS, expressed predominantly in mouse foetal haematopoietic tissues. Genes Cells 2002; 7:435-46; http://dx.doi.org/10.1046/j.1365-2443.2002.00529.x
40. Fernandez AG, Piano F. MEL-28 is downstream of the Ran cycle and is required for nuclear-envelope function and chromatin maintenance. Curr Biol 2006; 16:1757-63; http://dx.doi.org/10.1016/j.cub.2006.07.071
41. Galy V, Askjaer P, Franz C, López-Iglesias C, Mattaj IW. MEL-28, a novel nuclear-envelope and kinetochore protein essential for zygotic nuclear-envelope assembly in C. elegans. Curr Biol 2006; 16:1748-56; http://dx.doi.org/10.1016/j.cub.2006.06.067
42. Rasala BA, Orjalo AV, Shen Z, Briggs S, Forbes DJ. ELYS is a dual nucleoporin/kinetochore protein required for nuclear pore assembly and proper cell division. Proc Natl Acad Sci U S A 2006; 103:17801-6; http://dx.doi.org/10.1073/pnas.0608484103
43. Gillespie PJ, Khoudoli GA, Stewart G, Swedlow JR, Blow JJ. ELYS/MEL-28 chromatin association coordinates nuclear pore complex assembly and replication licensing. Curr Biol 2007; 17:1657-62; http://dx.doi.org/10.1016/j.cub.2007.08.041
44. Rasala BA, Ramos C, Harel A, Forbes DJ. Capture of AT-rich chromatin by ELYS recruits POM121 and NDC1 to initiate nuclear pore assembly. Mol Biol Cell 2008; 19:3982-96; http://dx.doi.org/10.1091/mbc.E08-01-0012
45. Walther TC, Alves A, Pickersgill H, Loïodice I, Hetzer M, Galy V, et al. The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 2003; 113:195-206; http://dx.doi.org/10.1016/S0092-8674(03)00235-6
46. Dultz E, Zanin E, Wurzenberger C, Braun M, Rabut G, Sironi L, et al. Systematic kinetic analysis of mitotic dis- and reassembly of the nuclear pore in living cells. J Cell Biol 2008; 180:857-65; http://dx.doi.org/10.1083/jcb.200707026
47. Fernandez-Martinez J, Rout MP. Nuclear pore complex biogenesis. Curr Opin Cell Biol 2009; 21:603-12; http://dx.doi.org/10.1016/j.ceb.2009.05.001
48. Orjalo AV, Arnaoutov A, Shen Z, Boyarchuk Y, Zeitlin SG, Fontoura B, et al. The Nup107-160 nucleoporin complex is required for correct bipolar spindle assembly. Mol Biol Cell 2006; 17:3806-18; http://dx.doi.org/10.1091/mbc.E05-11-1061
49. Zuccolo M, Alves A, Galy V, Bolhy S, Formstecher E, Racine V, et al. The human Nup107-160 nuclear pore subcomplex contributes to proper kinetochore functions. EMBO J 2007; 26:1853-64; http://dx.doi.org/10.1038/sj.emboj.7601642
50. Mishra RK, Chakraborty P, Arnaoutov A, Fontoura BM, Dasso M. The Nup107-160 complex and gamma- TuRC regulate microtubule polymerization at kinetochores. Nat Cell Biol 2010; 12:164-9; http://dx.doi.org/10.1038/ncb2016
51. Platani M, Santarella-Mellwig R, Posch M, Walczak R, Swedlow JR, Mattaj IW. The Nup107-160 nucleoporin complex promotes mitotic events via control of the localization state of the chromosome passenger complex. Mol Biol Cell 2009; 20:5260-75; http://dx.doi.org/10.1091/mbc.E09-05-0377
52. Ruchaud S, Carmena M, Earnshaw WC. Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 2007; 8:798-812; http://dx.doi.org/10.1038/nrm2257
53. Meyer H, Drozdowska A, Dobrynin G. A role for Cdc48/p97 and Aurora B in controlling chromatin condensation during exit from mitosis. Biochem Cell Biol 2010; 88:23-8; http://dx.doi.org/10.1139/O09-119
54. Smythe C, Jenkins HE, Hutchison CJ. Incorporation of the nuclear pore basket protein nup153 into nuclear pore structures is dependent upon lamina assembly: evidence from cell-free extracts of Xenopus eggs. EMBO J 2000; 19:3918-31; http://dx.doi.org/10.1093/emboj/19.15.3918
55. Hawryluk-Gara LA, Shibuya EK, Wozniak RW. Vertebrate Nup53 interacts with the nuclear lamina and is required for the assembly of a Nup93-containing complex. Mol Biol Cell 2005; 16:2382-94; http://dx.doi.org/10.1091/mbc.E04-10-0857
56. 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; http://dx.doi.org/10.1083/jcb.200704108
57. Funakoshi T, Clever M, Watanabe A, Imamoto N. Localization of Pom121 to the inner nuclear membrane is required for an early step of interphase nuclear pore complex assembly. Mol Biol Cell 2011; 22:1058-69; http://dx.doi.org/10.1091/mbc.E10-07-0641
58. Lussi YC, Hügi I, Laurell E, Kutay U, Fahrenkrog B. The nucleoporin Nup88 is interacting with nuclear lamin A. Mol Biol Cell 2011; 22:1080-90; http://dx.doi.org/10.1091/mbc.E10-05-0463
59. Talamas JA, Hetzer MW. POM121 and Sun1 play a role in early steps of interphase NPC assembly. J Cell Biol 2011; 194:27-37; http://dx.doi.org/10.1083/jcb.201012154
60. Yewdell WT, Colombi P, Makhnevych T, Lusk CP. Lumenal interactions in nuclear pore complex assembly and stability. Mol Biol Cell 2011; 22:1375-88; http://dx.doi.org/10.1091/mbc.E10-06-0554
61. Adam SA, Marr RS, Gerace L. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J Cell Biol 1990; 111:807-16; http://dx.doi.org/10.1083/jcb.111.3.807
62. Chaudhary N, Courvalin JC. Stepwise reassembly of the nuclear envelope at the end of mitosis. J Cell Biol 1993; 122:295-306; http://dx.doi.org/10.1083/jcb.122.2.295
63. Moir RD, Spann TP, Herrmann H, Goldman RD. Disruption of nuclear lamin organization blocks the elongation phase of DNA replication. J Cell Biol 2000; 149:1179-92; http://dx.doi.org/10.1083/jcb.149.6.1179
64. Courvalin JC, Segil N, Blobel G, Worman HJ. The lamin B receptor of the inner nuclear membrane undergoes mitosis-specific phosphorylation and is a substrate for p34cdc2-type protein kinase. J Biol Chem 1992; 267:19035-8
65. Takano M, Koyama Y, Ito H, Hoshino S, Onogi H, Hagiwara M, et al. Regulation of binding of lamin B receptor to chromatin by SR protein kinase and cdc2 kinase in Xenopus egg extracts. J Biol Chem 2004; 279:13265-71; http://dx.doi.org/10.1074/jbc.M308854200
66. Smith S, Blobel G. The first membrane spanning region of the lamin B receptor is sufficient for sorting to the inner nuclear membrane. J Cell Biol 1993; 120: 631-7; http://dx.doi.org/10.1083/jcb.120.3.631
67. Uehara R, Goshima G. Functional central spindle assembly requires de novo microtubule generation in the interchromosomal region during anaphase. J Cell Biol 2010; 191:259-67; http://dx.doi.org/10.1083/jcb.201004150
68. Tseng LC, Chen RH. Temporal control of nuclear envelope assembly by phosphorylation of lamin B receptor. Mol Biol Cell 2011; 22:3306-17; http://dx.doi.org/10.1091/mbc.E11-03-0199
69. Nikolakaki E, Drosou V, Sanidas I, Peidis P, Papamarcaki T, Iakoucheva LM, et al. RNA association or phosphorylation of the RS domain prevents aggregation of RS domain-containing proteins. Biochim Biophys Acta 2008; 1780:214-25; http://dx.doi.org/10.1016/j.bbagen.2007.10.014
70. Rotem A, Gruber R, Shorer H, Shaulov L, Klein E, Harel A. Importin beta regulates the seeding of chromatin with initiation sites for nuclear pore assembly. Mol Biol Cell 2009; 20:4031-42; http://dx.doi.org/10.1091/mbc.E09-02-0150
71. Ródenas E, González-Aguilera C, Ayuso C, Askjaer P. Dissection of the NUP107 nuclear pore subcomplex reveals a novel interaction with spindle assembly checkpoint protein MAD1 in C. elegans. Mol Biol Cell 2012; http://dx.doi.org/10.1091/mbc.E11-11-0927
72. Dechat T, Gajewski A, Korbei B, Gerlich D, Daigle N, Haraguchi T, et al. LAP2alpha and BAF transiently localize to telomeres and specific regions on chromatin during nuclear assembly. J Cell Sci 2004; 117:6117-28; http://dx.doi.org/10.1242/jcs.01529
73. 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; 20:1754-64; http://dx.doi.org/10.1093/emboj/20.7.1754
74. Margalit A, Segura-Totten M, Gruenbaum Y, Wilson KL. Barrier-to-autointegration factor is required to segregate and enclose chromosomes within the nuclear envelope and assemble the nuclear lamina. Proc Natl Acad Sci U S A 2005; 102:3290-5; http://dx.doi.org/10.1073/pnas.0408364102
75. Guse A, Mishima M, Glotzer M. Phosphorylation of ZEN-4/MKLP1 by aurora B regulates completion of cytokinesis. Curr Biol 2005; 15:778-86; http://dx.doi.org/10.1016/j.cub.2005.03.041
76. Yahata K, Kishine H, Sone T, Sasaki Y, Hotta J, Chesnut JD, et al. Multi-gene gateway clone design for expression of multiple heterologous genes in living cells: conditional gene expression at near physiological levels. J Biotechnol 2005; 118:123-34; http://dx.doi.org/10.1016/j.jbiotec.2005.02.020
77. Boehmer T, Enninga J, Dales S, Blobel G, Zhong H. Depletion of a single nucleoporin, Nup107, prevents the assembly of a subset of nucleoporins into the nuclear pore complex. Proc Natl Acad Sci U S A 2003; 100:981-5; http://dx.doi.org/10.1073/pnas.252749899
78. Funakoshi T, Maeshima K, Yahata K, Sugano S, Imamoto F, Imamoto N. Two distinct human POM121 genes: requirement for the formation of nuclear pore complexes. FEBS Lett 2007; 581:4910-6; http://dx.doi.org/10.1016/j.febslet.2007.09.021
79. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001; 411:494-8; http://dx.doi.org/10.1038/35078107