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PMID: 10982402 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

C. elegans nuclear envelope proteins emerin, MAN1, lamin, and nucleoporins reveal unique timing of nuclear envelope breakdown during mitosis.

Molecular biology of the cell ·Vol. 11 ·No. 9 ·2000-09-00 ·Pages 3089-99

Lee KK, Gruenbaum Y, Spann P, Liu J, Wilson KL

Abstract

Emerin, MAN1, and LAP2 are integral membrane proteins of the vertebrate nuclear envelope. They share a 43-residue N-terminal motif termed the LEM domain. We found three putative LEM domain genes in Caenorhabditis elegans, designated emr-1, lem-2, and lem-3. We analyzed emr-l, which encodes Ce-emerin, and lem-2, which encodes Ce-MAN1. Ce-emerin and Ce-MAN1 migrate on SDS-PAGE as 17- and 52-kDa proteins, respectively. Based on their biochemical extraction properties and immunolocalization, both Ce-emerin and Ce-MAN1 are integral membrane proteins localized at the nuclear envelope. We used antibodies against Ce-MAN1, Ce-emerin, nucleoporins, and Ce-lamin to determine the timing of nuclear envelope breakdown during mitosis in C. elegans. The C. elegans nuclear envelope disassembles very late compared with vertebrates and Drosophila. The nuclear membranes remained intact everywhere except near spindle poles during metaphase and early anaphase, fully disassembling only during mid-late anaphase. Disassembly of pore complexes, and to a lesser extent the lamina, depended on embryo age: pore complexes were absent during metaphase in >30-cell embryos but existed until anaphase in 2- to 24-cell embryos. Intranuclear mRNA splicing factors disassembled after prophase. The timing of nuclear disassembly in C. elegans is novel and may reflect its evolutionary position between unicellular and more complex eukaryotes.

MeSH Terms
Amino Acid Sequence Animals Caenorhabditis elegans/cytology,genetics,physiology Caenorhabditis elegans Proteins Cell Cycle/physiology DNA-Binding Proteins Embryo, Nonmammalian/physiology Humans Lamins Membrane Proteins/chemistry,genetics,metabolism Metaphase Mitosis/physiology Molecular Sequence Data Nuclear Envelope/ultrastructure Nuclear Pore/physiology,ultrastructure Nuclear Proteins/chemistry,genetics,metabolism Sequence Alignment Sequence Homology, Amino Acid Thymopoietins/chemistry,genetics,metabolism
Chemicals
Caenorhabditis elegans Proteins DNA-Binding Proteins LEMD3 protein, human Lamins Membrane Proteins Nuclear Proteins Thymopoietins emerin lem-2 protein, C elegans
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lee K K
Department of Cell Biology and Anatomy, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.
Gruenbaum Y
Spann P
Liu J
Wilson K L
References (61)
61 references, click to expand
  1. Functional diversity of LAP2alpha and LAP2beta in postmitotic chromosome association is caused by an alpha-specific nuclear targeting domain.
    EMBO J. 1999 Nov 15;18(22):6370-84 PMID: 10562549
  2. The nuclear envelope, muscular dystrophy and gene expression.
    Trends Cell Biol. 2000 Apr;10(4):125-9 PMID: 10740265
  3. Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease.
    N Engl J Med. 1999 Dec 2;341(23):1715-24 PMID: 10580070
  4. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy.
    J Cell Biol. 1999 Nov 29;147(5):913-20 PMID: 10579712
  5. Nuclear lamin A/C R482Q mutation in canadian kindreds with Dunnigan-type familial partial lipodystrophy.
    Hum Mol Genet. 2000 Jan 1;9(1):109-12 PMID: 10587585
  6. Lamins and lamin-binding proteins in functional chromatin organization.
    Crit Rev Eukaryot Gene Expr. 1999;9(3-4):257-65 PMID: 10651242
  7. The nuclear lamina: molecular organization and interaction with chromatin.
    Crit Rev Eukaryot Gene Expr. 1999;9(3-4):285-93 PMID: 10651245
  8. LMNA, encoding lamin A/C, is mutated in partial lipodystrophy.
    Nat Genet. 2000 Feb;24(2):153-6 PMID: 10655060
  9. MAN1, an inner nuclear membrane protein that shares the LEM domain with lamina-associated polypeptide 2 and emerin.
    J Biol Chem. 2000 Feb 18;275(7):4840-7 PMID: 10671519
  10. Live fluorescence imaging reveals early recruitment of emerin, LBR, RanBP2, and Nup153 to reforming functional nuclear envelopes.
    J Cell Sci. 2000 Mar;113 ( Pt 5):779-94 PMID: 10671368
  11. Direct interaction between emerin and lamin A.
    Biochem Biophys Res Commun. 2000 Jan 27;267(3):709-14 PMID: 10673356
  12. Translocation of C. elegans CED-4 to nuclear membranes during programmed cell death.
    Science. 2000 Feb 25;287(5457):1485-9 PMID: 10688797
  13. P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA.
    Dev Biol. 2000 Mar 15;219(2):315-33 PMID: 10694425
  14. Review: nuclear lamins--structural proteins with fundamental functions.
    J Struct Biol. 2000 Apr;129(2-3):313-23 PMID: 10806082
  15. MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos.
    Mol Cell. 2000 Apr;5(4):671-82 PMID: 10882103
  16. The molecular organization of membranes.
    Annu Rev Biochem. 1974;43(0):805-33 PMID: 4277710
  17. 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):546-66 PMID: 102651
  18. Identification of a major polypeptide of the nuclear pore complex.
    J Cell Biol. 1982 Dec;95(3):826-37 PMID: 7153248
  19. Dynamics of the nuclear envelope and of nuclear pore complexes during mitosis in the Drosophila embryo.
    Eur J Cell Biol. 1984 May;34(1):179-89 PMID: 6428889
  20. Identification and characterization of a nuclear pore complex protein.
    Cell. 1986 Jun 6;45(5):699-709 PMID: 3518946
  21. Monoclonal antibodies identify a group of nuclear pore complex glycoproteins.
    J Cell Biol. 1987 May;104(5):1143-56 PMID: 2437126
  22. Functional organization of the nuclear envelope.
    Annu Rev Cell Biol. 1988;4:335-74 PMID: 2461721
  23. 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):463-70 PMID: 2517292
  24. A monoclonal antibody that recognizes a phosphorylated epitope stains lampbrush chromosome loops and small granules in the amphibian germinal vesicle.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2217-23 PMID: 1703534
  25. GST-lamin fusion proteins act as dominant negative mutants in Xenopus egg extract and reveal the function of the lamina in DNA replication.
    J Cell Sci. 1997 Oct;110 ( Pt 20):2507-18 PMID: 9372440
  26. Nuclear assembly.
    Annu Rev Cell Dev Biol. 1997;13:669-95 PMID: 9442884
  27. A previously unidentified host protein protects retroviral DNA from autointegration.
    Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1528-33 PMID: 9465049
  28. Major binding sites for the nuclear import receptor are the internal nucleoporin Nup153 and the adjacent nuclear filament protein Tpr.
    J Cell Biol. 1998 Apr 6;141(1):31-49 PMID: 9531546
  29. Nuclear envelope disassembly in mitotic extract requires functional nuclear pores and a nuclear lamina.
    J Cell Sci. 1998 May;111 ( Pt 9):1293-303 PMID: 9547309
  30. Immunocytochemical detection of emerin within the nuclear matrix.
    Neuromuscul Disord. 1998 Jun;8(5):338-44 PMID: 9673989
  31. Nuclear lamins: their structure, assembly, and interactions.
    J Struct Biol. 1998;122(1-2):42-66 PMID: 9724605
  32. The maternal-to-zygotic transition in embryonic patterning of Caenorhabditis elegans.
    Curr Opin Genet Dev. 1998 Aug;8(4):472-80 PMID: 9729725
  33. Detergent-salt resistance of LAP2alpha in interphase nuclei and phosphorylation-dependent association with chromosomes early in nuclear assembly implies functions in nuclear structure dynamics.
    EMBO J. 1998 Aug 17;17(16):4887-902 PMID: 9707448
  34. 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. 1998 Oct;9(10):2839-55 PMID: 9763447
  35. Solution structure of the cellular factor BAF responsible for protecting retroviral DNA from autointegration.
    Nat Struct Biol. 1998 Oct;5(10):903-9 PMID: 9783751
  36. Sequential PKC- and Cdc2-mediated phosphorylation events elicit zebrafish nuclear envelope disassembly.
    J Cell Sci. 1999 Mar;112 ( Pt 6):977-87 PMID: 10036247
  37. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy.
    Nat Genet. 1999 Mar;21(3):285-8 PMID: 10080180
  38. The Caenorhabditis elegans gene ncc-1 encodes a cdc2-related kinase required for M phase in meiotic and mitotic cell divisions, but not for S phase.
    Development. 1999 May;126(10):2227-39 PMID: 10207147
  39. Intracellular trafficking of emerin, the Emery-Dreifuss muscular dystrophy protein.
    J Cell Sci. 1999 Jun;112 ( Pt 11):1709-19 PMID: 10318763
  40. LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction.
    J Cell Sci. 1999 Aug;112 ( Pt 15):2485-92 PMID: 10393804
  41. The Emery-Dreifuss muscular dystrophy phenotype arises from aberrant targeting and binding of emerin at the inner nuclear membrane.
    J Cell Sci. 1999 Aug;112 ( Pt 15):2571-82 PMID: 10393813
  42. Heart to heart: from nuclear proteins to Emery-Dreifuss muscular dystrophy.
    Hum Mol Genet. 1999;8(10):1847-51 PMID: 10469836
  43. Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins.
    J Cell Sci. 1999 Oct;112 ( Pt 20):3463-75 PMID: 10504295
  44. Variant mitoses in lower eukaryotes: indicators of the evolution of mitosis.
    Int Rev Cytol. 1980;64:1-80 PMID: 20815116
  45. Human SR proteins and isolation of a cDNA encoding SRp75.
    Mol Cell Biol. 1993 Jul;13(7):4023-8 PMID: 8321209
  46. A nuclear lamin of the nematode Caenorhabditis elegans with unusual structural features; cDNA cloning and gene organization.
    Eur J Cell Biol. 1993 Dec;62(2):214-23 PMID: 7925480
  47. Identification of a protein complex that is required for nuclear protein import and mediates docking of import substrate to distinct nucleoporins.
    Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1769-73 PMID: 7878057
  48. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy.
    Nat Genet. 1994 Dec;8(4):323-7 PMID: 7894480
  49. Soma-germline asymmetry in the distributions of embryonic RNAs in Caenorhabditis elegans.
    Development. 1994 Oct;120(10):2823-34 PMID: 7607073
  50. The dynamic properties and possible functions of nuclear lamins.
    Int Rev Cytol. 1995;162B:141-82 PMID: 8557486
  51. A sperm-supplied factor required for embryogenesis in C. elegans.
    Development. 1996 Jan;122(1):391-404 PMID: 8565851
  52. The characterization and localization of the mouse thymopoietin/lamina-associated polypeptide 2 gene and its alternatively spliced products.
    Genome Res. 1996 May;6(5):361-70 PMID: 8743987
  53. The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein.
    Hum Mol Genet. 1996 Jun;5(6):801-8 PMID: 8776595
  54. Time-resolved, in vivo studies of mitotic spindle formation and nuclear lamina breakdown in Drosophila early embryos.
    J Cell Sci. 1996 Mar;109 ( Pt 3):591-607 PMID: 8907705
  55. Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis.
    J Cell Biol. 1997 Mar 24;136(6):1201-12 PMID: 9087437
  56. Integral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis.
    J Cell Biol. 1997 Jun 16;137(6):1199-210 PMID: 9182656
  57. The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds.
    Mol Biol Cell. 1997 Aug;8(8):1461-79 PMID: 9285819
  58. Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis.
    J Cell Biol. 1997 Sep 22;138(6):1193-206 PMID: 9298976
  59. Nuclear envelope breakdown in mammalian cells involves stepwise lamina disassembly and microtubule-drive deformation of the nuclear membrane.
    J Cell Sci. 1997 Sep;110 ( Pt 17):2129-40 PMID: 9378763
  60. Dynamics of the endoplasmic reticulum and golgi apparatus during early sea urchin development.
    Mol Biol Cell. 2000 Mar;11(3):897-914 PMID: 10712508
  61. Distribution of emerin during the cell cycle.
    Eur J Cell Biol. 1999 Oct;78(10):749-56 PMID: 10569247
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2000-09-00
Pages
3089-99
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC14977
Subset
IM
Grants
NICHD NIH HHS · F32 HD008331 · United States
NIGMS NIH HHS · R01 GM048646 · United States
NIGMS NIH HHS · R01GM48646 · United States
NICHD NIH HHS · F32HD08331 · United States
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