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J Cell Biol. 1993 July 2; 122(2): 295–306.
PMCID: PMC2119651

Stepwise reassembly of the nuclear envelope at the end of mitosis


The nuclear envelope consists of three distinct membrane domains: the outer membrane with the bound ribosomes, the inner membrane with the bound lamina, and the pore membrane with the bound pore complexes. Using biochemical and morphological methods, we observed that the nuclear membranes of HeLa cells undergoing mitosis are disassembled in a domain-specific manner, i.e., integral membrane proteins representing the inner nuclear membrane (the lamin B receptor) and the nuclear pore membrane (gp210) are segregated into different populations of mitotic vesicles. At the completion of mitosis, the inner nuclear membrane- derived vesicles associate with chromatin first, beginning in anaphase, whereas the pore membranes and the lamina assemble later, during telophase and cytokinesis. Our data suggest that the ordered reassembly of the nuclear envelope is triggered by the early attachment of inner nuclear membrane-derived vesicles to the chromatin.

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Selected References

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  • Aaronson RP, Blobel G. On the attachment of the nuclear pore complex. J Cell Biol. 1974 Sep;62(3):746–754. [PMC free article] [PubMed]
  • Aris JP, Blobel G. Yeast nuclear envelope proteins cross react with an antibody against mammalian pore complex proteins. J Cell Biol. 1989 Jun;108(6):2059–2067. [PMC free article] [PubMed]
  • Bailer SM, Eppenberger HM, Griffiths G, Nigg EA. Characterization of A 54-kD protein of the inner nuclear membrane: evidence for cell cycle-dependent interaction with the nuclear lamina. J Cell Biol. 1991 Aug;114(3):389–400. [PMC free article] [PubMed]
  • Benavente R, Scheer U, Chaly N. Nucleocytoplasmic sorting of macromolecules following mitosis: fate of nuclear constituents after inhibition of pore complex function. Eur J Cell Biol. 1989 Oct;50(1):209–219. [PubMed]
  • Beck LA, Hosick TJ, Sinensky M. Incorporation of a product of mevalonic acid metabolism into proteins of Chinese hamster ovary cell nuclei. J Cell Biol. 1988 Oct;107(4):1307–1316. [PMC free article] [PubMed]
  • Burke B. On the cell-free association of lamins A and C with metaphase chromosomes. Exp Cell Res. 1990 Jan;186(1):169–176. [PubMed]
  • Burke B, Gerace L. A cell free system to study reassembly of the nuclear envelope at the end of mitosis. Cell. 1986 Feb 28;44(4):639–652. [PubMed]
  • Chaudhary N, McMahon C, Blobel G. Primary structure of a human arginine-rich nuclear protein that colocalizes with spliceosome components. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8189–8193. [PubMed]
  • Chen TY, Merisko EM. Annulate lamellae: comparison of antigenic epitopes of annulate lamellae membranes with the nuclear envelope. J Cell Biol. 1988 Oct;107(4):1299–1306. [PMC free article] [PubMed]
  • Conner GE, Noonan NE, Noonan KD. Nuclear envelope of Chinese hamster ovary cells. Re-formation of the nuclear envelope following mitosis. Biochemistry. 1980 Jan 22;19(2):277–289. [PubMed]
  • Courvalin JC, Chaudhary N, Danon F, Brouet JC, Lassoued K. Characterization of human autoantibodies specific for lamin A. Biol Cell. 1990;69(2):93–97. [PubMed]
  • Courvalin JC, Lassoued K, Bartnik E, Blobel G, Wozniak RW. The 210-kD nuclear envelope polypeptide recognized by human autoantibodies in primary biliary cirrhosis is the major glycoprotein of the nuclear pore. J Clin Invest. 1990 Jul;86(1):279–285. [PMC free article] [PubMed]
  • Courvalin JC, Lassoued K, Worman HJ, Blobel G. Identification and characterization of autoantibodies against the nuclear envelope lamin B receptor from patients with primary biliary cirrhosis. J Exp Med. 1990 Sep 1;172(3):961–967. [PMC free article] [PubMed]
  • 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 Sep 25;267(27):19035–19038. [PubMed]
  • Dabauvalle MC, Scheer U. Assembly of nuclear pore complexes in Xenopus egg extract. Biol Cell. 1991;72(1-2):25–29. [PubMed]
  • Dabauvalle MC, Loos K, Merkert H, Scheer U. Spontaneous assembly of pore complex-containing membranes ("annulate lamellae") in Xenopus egg extract in the absence of chromatin. J Cell Biol. 1991 Mar;112(6):1073–1082. [PMC free article] [PubMed]
  • Davis LI, Blobel G. Identification and characterization of a nuclear pore complex protein. Cell. 1986 Jun 6;45(5):699–709. [PubMed]
  • Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. [PMC free article] [PubMed]
  • Dwyer N, Blobel G. A modified procedure for the isolation of a pore complex-lamina fraction from rat liver nuclei. J Cell Biol. 1976 Sep;70(3):581–591. [PMC free article] [PubMed]
  • Fisher DZ, Chaudhary N, Blobel G. cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6450–6454. [PubMed]
  • Gerace L, Blum A, Blobel G. Immunocytochemical localization of the major polypeptides of the nuclear pore complex-lamina fraction. Interphase and mitotic distribution. J Cell Biol. 1978 Nov;79(2 Pt 1):546–566. [PMC free article] [PubMed]
  • Gerace L, Blobel G. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell. 1980 Jan;19(1):277–287. [PubMed]
  • Gerace L, Blobel G. Nuclear lamina and the structural organization of the nuclear envelope. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 2):967–978. [PubMed]
  • Gerace L, Ottaviano Y, Kondor-Koch C. Identification of a major polypeptide of the nuclear pore complex. J Cell Biol. 1982 Dec;95(3):826–837. [PMC free article] [PubMed]
  • Glass JR, Gerace L. Lamins A and C bind and assemble at the surface of mitotic chromosomes. J Cell Biol. 1990 Sep;111(3):1047–1057. [PMC free article] [PubMed]
  • Goldman AE, Moir RD, Montag-Lowy M, Stewart M, Goldman RD. Pathway of incorporation of microinjected lamin A into the nuclear envelope. J Cell Biol. 1992 Nov;119(4):725–735. [PMC free article] [PubMed]
  • Greber UF, Senior A, Gerace L. A major glycoprotein of the nuclear pore complex is a membrane-spanning polypeptide with a large lumenal domain and a small cytoplasmic tail. EMBO J. 1990 May;9(5):1495–1502. [PubMed]
  • Guilly MN, Bensussan A, Bourge JF, Bornens M, Courvalin JC. A human T lymphoblastic cell line lacks lamins A and C. EMBO J. 1987 Dec 1;6(12):3795–3799. [PubMed]
  • Harel A, Zlotkin E, Nainudel-Epszteyn S, Feinstein N, Fisher PA, Gruenbaum Y. Persistence of major nuclear envelope antigens in an envelope-like structure during mitosis in Drosophila melanogaster embryos. J Cell Sci. 1989 Nov;94(Pt 3):463–470. [PubMed]
  • Heald R, McKeon F. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell. 1990 May 18;61(4):579–589. [PubMed]
  • Höger TH, Krohne G, Franke WW. Amino acid sequence and molecular characterization of murine lamin B as deduced from cDNA clones. Eur J Cell Biol. 1988 Dec;47(2):283–290. [PubMed]
  • Höger TH, Krohne G, Kleinschmidt JA. Interaction of Xenopus lamins A and LII with chromatin in vitro mediated by a sequence element in the carboxyterminal domain. Exp Cell Res. 1991 Dec;197(2):280–289. [PubMed]
  • Höger TH, Zatloukal K, Waizenegger I, Krohne G. Characterization of a second highly conserved B-type lamin present in cells previously thought to contain only a single B-type lamin. Chromosoma. 1990 Dec;100(1):67–69. [PubMed]
  • Kessel RG. The annulate lamellae--from obscurity to spotlight. Electron Microsc Rev. 1989;2(2):257–348. [PubMed]
  • Kitten GT, Nigg EA. The CaaX motif is required for isoprenylation, carboxyl methylation, and nuclear membrane association of lamin B2. J Cell Biol. 1991 Apr;113(1):13–23. [PMC free article] [PubMed]
  • Lohka MJ. The reconstitution of nuclear envelopes in cell-free extracts. Cell Biol Int Rep. 1988 Sep;12(9):833–848. [PubMed]
  • Matsuura S, Masuda R, Omori K, Negishi M, Tashiro Y. Distribution and induction of cytochrome P-450 in rat liver nuclear envelope. J Cell Biol. 1981 Oct;91(1):212–220. [PMC free article] [PubMed]
  • Maul GG. The nuclear and the cytoplasmic pore complex: structure, dynamics, distribution, and evolution. Int Rev Cytol Suppl. 1977;(6):75–186. [PubMed]
  • McKeon FD, Kirschner MW, Caput D. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature. 1986 Feb 6;319(6053):463–468. [PubMed]
  • Migliaccio G, Nicchitta CV, Blobel G. The signal sequence receptor, unlike the signal recognition particle receptor, is not essential for protein translocation. J Cell Biol. 1992 Apr;117(1):15–25. [PMC free article] [PubMed]
  • Miller M, Park MK, Hanover JA. Nuclear pore complex: structure, function, and regulation. Physiol Rev. 1991 Jul;71(3):909–949. [PubMed]
  • Newport J. Nuclear reconstitution in vitro: stages of assembly around protein-free DNA. Cell. 1987 Jan 30;48(2):205–217. [PubMed]
  • Newport JW, Wilson KL, Dunphy WG. A lamin-independent pathway for nuclear envelope assembly. J Cell Biol. 1990 Dec;111(6 Pt 1):2247–2259. [PMC free article] [PubMed]
  • Nigg EA. The nuclear envelope. Curr Opin Cell Biol. 1989 Jun;1(3):435–440. [PubMed]
  • Padan R, Nainudel-Epszteyn S, Goitein R, Fainsod A, Gruenbaum Y. Isolation and characterization of the Drosophila nuclear envelope otefin cDNA. J Biol Chem. 1990 May 15;265(14):7808–7813. [PubMed]
  • Peter M, Nakagawa J, Dorée M, Labbé JC, Nigg EA. In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell. 1990 May 18;61(4):591–602. [PubMed]
  • Pfaller R, Smythe C, Newport JW. Assembly/disassembly of the nuclear envelope membrane: cell cycle-dependent binding of nuclear membrane vesicles to chromatin in vitro. Cell. 1991 Apr 19;65(2):209–217. [PubMed]
  • Pollard KM, Chan EK, Grant BJ, Sullivan KF, Tan EM, Glass CA. In vitro posttranslational modification of lamin B cloned from a human T-cell line. Mol Cell Biol. 1990 May;10(5):2164–2175. [PMC free article] [PubMed]
  • Reichelt R, Holzenburg A, Buhle EL, Jr, Jarnik M, Engel A, Aebi U. Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J Cell Biol. 1990 Apr;110(4):883–894. [PMC free article] [PubMed]
  • Richardson JC, Maddy AH. The polypeptides of rat liver nuclear envelope. II. Comparison of rat liver nuclear membrane polypeptides with those of the rough endoplasmic reticulum. J Cell Sci. 1980 Jun;43:269–277. [PubMed]
  • Roberts SB, Segil N, Heintz N. Differential phosphorylation of the transcription factor Oct1 during the cell cycle. Science. 1991 Aug 30;253(5023):1022–1026. [PubMed]
  • Senior A, Gerace L. Integral membrane proteins specific to the inner nuclear membrane and associated with the nuclear lamina. J Cell Biol. 1988 Dec;107(6 Pt 1):2029–2036. [PMC free article] [PubMed]
  • Sheehan MA, Mills AD, Sleeman AM, Laskey RA, Blow JJ. Steps in the assembly of replication-competent nuclei in a cell-free system from Xenopus eggs. J Cell Biol. 1988 Jan;106(1):1–12. [PMC free article] [PubMed]
  • Smith DE, Fisher PA. Identification, developmental regulation, and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryos: application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots. J Cell Biol. 1984 Jul;99(1 Pt 1):20–28. [PMC free article] [PubMed]
  • Snow CM, Senior A, Gerace L. Monoclonal antibodies identify a group of nuclear pore complex glycoproteins. J Cell Biol. 1987 May;104(5):1143–1156. [PMC free article] [PubMed]
  • Soullam B, Worman HJ. The amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal. J Cell Biol. 1993 Mar;120(5):1093–1100. [PMC free article] [PubMed]
  • Stick R, Angres B, Lehner CF, Nigg EA. The fates of chicken nuclear lamin proteins during mitosis: evidence for a reversible redistribution of lamin B2 between inner nuclear membrane and elements of the endoplasmic reticulum. J Cell Biol. 1988 Aug;107(2):397–406. [PMC free article] [PubMed]
  • Ulitzur N, Harel A, Feinstein N, Gruenbaum Y. Lamin activity is essential for nuclear envelope assembly in a Drosophila embryo cell-free extract. J Cell Biol. 1992 Oct;119(1):17–25. [PMC free article] [PubMed]
  • Vigers GP, Lohka MJ. A distinct vesicle population targets membranes and pore complexes to the nuclear envelope in Xenopus eggs. J Cell Biol. 1991 Feb;112(4):545–556. [PMC free article] [PubMed]
  • Vigers GP, Lohka MJ. Regulation of nuclear envelope precursor functions during cell division. J Cell Sci. 1992 Jun;102(Pt 2):273–284. [PubMed]
  • Ward GE, Kirschner MW. Identification of cell cycle-regulated phosphorylation sites on nuclear lamin C. Cell. 1990 May 18;61(4):561–577. [PubMed]
  • White JM. Membrane fusion. Science. 1992 Nov 6;258(5084):917–924. [PubMed]
  • Wiedmann M, Kurzchalia TV, Hartmann E, Rapoport TA. A signal sequence receptor in the endoplasmic reticulum membrane. Nature. 328(6133):830–833. [PubMed]
  • Wilson KL, Newport J. A trypsin-sensitive receptor on membrane vesicles is required for nuclear envelope formation in vitro. J Cell Biol. 1988 Jul;107(1):57–68. [PMC free article] [PubMed]
  • Wolda SL, Glomset JA. Evidence for modification of lamin B by a product of mevalonic acid. J Biol Chem. 1988 May 5;263(13):5997–6000. [PubMed]
  • Worman HJ, Yuan J, Blobel G, Georgatos SD. A lamin B receptor in the nuclear envelope. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8531–8534. [PubMed]
  • Worman HJ, Evans CD, Blobel G. The lamin B receptor of the nuclear envelope inner membrane: a polytopic protein with eight potential transmembrane domains. J Cell Biol. 1990 Oct;111(4):1535–1542. [PMC free article] [PubMed]
  • Wozniak RW, Bartnik E, Blobel G. Primary structure analysis of an integral membrane glycoprotein of the nuclear pore. J Cell Biol. 1989 Jun;108(6):2083–2092. [PMC free article] [PubMed]
  • Yang CH, Lambie EJ, Snyder M. NuMA: an unusually long coiled-coil related protein in the mammalian nucleus. J Cell Biol. 1992 Mar;116(6):1303–1317. [PMC free article] [PubMed]
  • Zeligs JD, Wollman SH. Mitosis in rat thyroid epithelial cells in vivo. I. Ultrastructural changes in cytoplasmic organelles during the mitotic cycle. J Ultrastruct Res. 1979 Jan;66(1):53–77. [PubMed]
  • Zieve GW, Turnbull D, Mullins JM, McIntosh JR. Production of large numbers of mitotic mammalian cells by use of the reversible microtubule inhibitor nocodazole. Nocodazole accumulated mitotic cells. Exp Cell Res. 1980 Apr;126(2):397–405. [PubMed]

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