Orchestrating nuclear envelope disassembly and reassembly during mitosis

Key Points The nucleus is surrounded by the nuclear envelope (NE), which is formed by two juxtaposed membranes, termed the inner and outer nuclear membranes. A protein meshwork of intermediate filament proteins — the nuclear lamina — is attached to the inner face of the NE. The NE is perforated by h...

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Published inNature reviews. Molecular cell biology Vol. 10; no. 3; pp. 178 - 191
Main Authors Güttinger, Stephan, Laurell, Eva, Kutay, Ulrike
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.03.2009
Nature Publishing Group
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Online AccessGet full text
ISSN1471-0072
1471-0080
DOI10.1038/nrm2641

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Abstract Key Points The nucleus is surrounded by the nuclear envelope (NE), which is formed by two juxtaposed membranes, termed the inner and outer nuclear membranes. A protein meshwork of intermediate filament proteins — the nuclear lamina — is attached to the inner face of the NE. The NE is perforated by holes that are occupied by nuclear pore complexes (NPCs), which serve the selective transport of macromolecules between nucleus and cytoplasm. The NE is a highly dynamic structure that is completely disassembled and reassembled during open mitosis in higher eukaryotes. These mitotic changes are subject to both spatial and temporal control mechanisms that are embedded in the more general network that controls cell division. NE breakdown (NEBD) involves the disassembly of NPCs, the disintegration of the nuclear lamina and the retraction of NE membranes into the membrane system of the endoplasmic reticulum. NEBD is triggered by the concerted action of mitotic kinases, some of which are known to directly contribute to NEBD. Some of the protein constituents of NPCs, termed nucleoporins, have prominent roles during specific steps of mitotic progression, such as spindle assembly and sister chromatid separation. NE reformation occurs around a compacted mass of segregated chromatin in each daughter cell. NPC assembly is initiated in anaphase by the deposition of prepores on chromatin. Nuclear membrane reformation commences with the attraction of ER tubules to the surface of chromatin, which then flatten to form membrane sheets. DNA-binding inner nuclear membrane proteins have a pivotal role in establishing chromatin–membrane contacts. Subsequent events in nuclear reformation include the formation of a closed NE that contains fully assembled, transport-competent NPCs, and the reformation of the nuclear lamina. The nuclear envelope is a dynamic structure that is disassembled and reassembled during 'open' mitosis in higher eukaryotes. These mitotic changes are subject to both spatial and temporal control mechanisms that are embedded in the more general regulatory network that directs cell division. Cell division in eukaryotes requires extensive architectural changes of the nuclear envelope (NE) to ensure that segregated DNA is finally enclosed in a single cell nucleus in each daughter cell. Higher eukaryotic cells have evolved 'open' mitosis, the most extreme mechanism to solve the problem of nuclear division, in which the NE is initially completely disassembled and then reassembled in coordination with DNA segregation. Recent progress in the field has now started to uncover mechanistic and molecular details that underlie the changes in NE reorganization during open mitosis. These studies reveal a tight interplay between NE components and the mitotic machinery.
AbstractList Cell division in eukaryotes requires extensive architectural changes of the nuclear envelope (NE) to ensure that segregated DNA is finally enclosed in a single cell nucleus in each daughter cell. Higher eukaryotic cells have evolved 'open' mitosis, the most extreme mechanism to solve the problem of nuclear division, in which the NE is initially completely disassembled and then reassembled in coordination with DNA segregation. Recent progress in the field has now started to uncover mechanistic and molecular details that underlie the changes in NE reorganization during open mitosis. These studies reveal a tight interplay between NE components and the mitotic machinery.
Key Points The nucleus is surrounded by the nuclear envelope (NE), which is formed by two juxtaposed membranes, termed the inner and outer nuclear membranes. A protein meshwork of intermediate filament proteins — the nuclear lamina — is attached to the inner face of the NE. The NE is perforated by holes that are occupied by nuclear pore complexes (NPCs), which serve the selective transport of macromolecules between nucleus and cytoplasm. The NE is a highly dynamic structure that is completely disassembled and reassembled during open mitosis in higher eukaryotes. These mitotic changes are subject to both spatial and temporal control mechanisms that are embedded in the more general network that controls cell division. NE breakdown (NEBD) involves the disassembly of NPCs, the disintegration of the nuclear lamina and the retraction of NE membranes into the membrane system of the endoplasmic reticulum. NEBD is triggered by the concerted action of mitotic kinases, some of which are known to directly contribute to NEBD. Some of the protein constituents of NPCs, termed nucleoporins, have prominent roles during specific steps of mitotic progression, such as spindle assembly and sister chromatid separation. NE reformation occurs around a compacted mass of segregated chromatin in each daughter cell. NPC assembly is initiated in anaphase by the deposition of prepores on chromatin. Nuclear membrane reformation commences with the attraction of ER tubules to the surface of chromatin, which then flatten to form membrane sheets. DNA-binding inner nuclear membrane proteins have a pivotal role in establishing chromatin–membrane contacts. Subsequent events in nuclear reformation include the formation of a closed NE that contains fully assembled, transport-competent NPCs, and the reformation of the nuclear lamina. The nuclear envelope is a dynamic structure that is disassembled and reassembled during 'open' mitosis in higher eukaryotes. These mitotic changes are subject to both spatial and temporal control mechanisms that are embedded in the more general regulatory network that directs cell division. Cell division in eukaryotes requires extensive architectural changes of the nuclear envelope (NE) to ensure that segregated DNA is finally enclosed in a single cell nucleus in each daughter cell. Higher eukaryotic cells have evolved 'open' mitosis, the most extreme mechanism to solve the problem of nuclear division, in which the NE is initially completely disassembled and then reassembled in coordination with DNA segregation. Recent progress in the field has now started to uncover mechanistic and molecular details that underlie the changes in NE reorganization during open mitosis. These studies reveal a tight interplay between NE components and the mitotic machinery.
Audience Academic
Author Laurell, Eva
Kutay, Ulrike
Güttinger, Stephan
Author_xml – sequence: 1
  givenname: Stephan
  surname: Güttinger
  fullname: Güttinger, Stephan
  organization: Institute of Biochemistry, Eidgenössische Technische Hochschule Zurich, HPM F11.1
– sequence: 2
  givenname: Eva
  surname: Laurell
  fullname: Laurell, Eva
  organization: Institute of Biochemistry, Eidgenössische Technische Hochschule Zurich, HPM F11.1
– sequence: 3
  givenname: Ulrike
  surname: Kutay
  fullname: Kutay, Ulrike
  email: ulrike.kutay@bc.biol.ethz.ch
  organization: Institute of Biochemistry, Eidgenössische Technische Hochschule Zurich, HPM F11.1
BackLink https://www.ncbi.nlm.nih.gov/pubmed/19234477$$D View this record in MEDLINE/PubMed
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Snippet Key Points The nucleus is surrounded by the nuclear envelope (NE), which is formed by two juxtaposed membranes, termed the inner and outer nuclear membranes. A...
Cell division in eukaryotes requires extensive architectural changes of the nuclear envelope (NE) to ensure that segregated DNA is finally enclosed in a single...
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SubjectTerms Animals
Biochemistry
Biomedical and Life Sciences
Cancer Research
Cell Biology
Cell division
Cell Nucleus - chemistry
Cell Nucleus - metabolism
Deoxyribonucleic acid
Developmental Biology
DNA
Forecasting
Humans
Life Sciences
Membranes
Mitosis
Models, Biological
Nuclear Envelope - chemistry
Nuclear Envelope - metabolism
Nuclear membranes
Physiological aspects
Proteins
review-article
Stem Cells
Title Orchestrating nuclear envelope disassembly and reassembly during mitosis
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