Recruitment of functionally distinct membrane proteins to chromatin mediates nuclear envelope formation in vivo

Formation of the nuclear envelope (NE) around segregated chromosomes occurs by the reshaping of the endoplasmic reticulum (ER), a reservoir for disassembled nuclear membrane components during mitosis. In this study, we show that inner nuclear membrane proteins such as lamin B receptor (LBR), MAN1, Lap2β, and the trans-membrane nucleoporins Ndc1 and POM121 drive the spreading of ER membranes into the emerging NE via their capacity to bind chromatin in a collaborative manner. Despite their redundant functions, decreasing the levels of any of these trans-membrane proteins by RNAi-mediated knockdown delayed NE formation, whereas increasing the levels of any of them had the opposite effect. Furthermore, acceleration of NE formation interferes with chromosome separation during mitosis, indicating that the time frame over which chromatin becomes membrane enclosed is physiologically relevant and regulated. These data suggest that functionally distinct classes of chromatin-interacting membrane proteins, which are present at nonsaturating levels, collaborate to rapidly reestablish the nuclear compartment at the end of mitosis.

• Publication year

  2009

• Venue

  Journal of Cell Biology

• Publication date

  2009-07-27

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1083/jcb.200901106PMID 19620630PMCID 2717638
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Cisternal organization of the endoplasmic reticulum during mitosis.

  2009cited by this paper
• Shaping the endoplasmic reticulum into the nuclear envelope

  2008cited by this paper
• Systematic kinetic analysis of mitotic dis- and reassembly of the nuclear pore in living cells

  2008influential reference
• Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly

  2008cited by this paper
• Reshaping of the endoplasmic reticulum limits the rate for nuclear envelope formation

  2008influential reference
• Nuclear pore complex assembly through the cell cycle: Regulation and membrane organization

  2008cited by this paper
• Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin

  2007cited by this paper
• Enhanced expression of the nuclear envelope LAP2 transcriptional repressors in normal and malignant activated lymphocytes

  2007cited by this paper
• Nuclear envelope formation by chromatin-mediated reorganization of the endoplasmic reticulum

  2007influential reference
• Endoplasmic reticulum remains continuous and undergoes sheet-to-tubule transformation during cell division in mammalian cells

  2007cited by this paper
• Caenorhabditis elegans BAF‐1 and its kinase VRK‐1 participate directly in post‐mitotic nuclear envelope assembly

  2007cited by this paper
• Rough sheets and smooth tubules.

  2006cited by this paper
• A class of membrane proteins shaping the tubular endoplasmic reticulum.

  2006influential reference
• Direct membrane protein–DNA interactions required early in nuclear envelope assembly

  2006cited by this paper
• The conserved transmembrane nucleoporin NDC1 is required for nuclear pore complex assembly in vertebrate cells.

  2006cited by this paper
• The role of the nuclear envelope in cellular organization

  2006cited by this paper
• NDC1: a crucial membrane-integral nucleoporin of metazoan nuclear pore complexes

  2006cited by this paper
• Pushing the envelope: structure, function, and dynamics of the nuclear periphery.

  2005cited by this paper
• The conserved Nup107-160 complex is critical for nuclear pore complex assembly.

  2003cited by this paper
• MAN1 and emerin have overlapping function(s) essential for chromosome segregation and cell division in Caenorhabditis elegans

  2003cited by this paper
• Cell Cycle Dynamics of the Nuclear Envelope

  2003cited by this paper
• Structural organization of the endoplasmic reticulum

  2002influential reference
• Barrier-to-autointegration factor

  2002cited by this paper
• Remodelling the walls of the nucleus

  2002cited by this paper
• Inner nuclear membrane proteins: functions and targeting

  2001cited by this paper
• Live fluorescence imaging reveals early recruitment of emerin, LBR, RanBP2, and Nup153 to reforming functional nuclear envelopes.

  2000influential reference
• Dynamics and mobility of nuclear envelope proteins in interphase and mitotic cells revealed by green fluorescent protein chimeras.

  1999cited by this paper
• Roles of LAP2 Proteins in Nuclear Assembly and DNA Replication: Truncated LAP2β Proteins Alter Lamina Assembly, Envelope Formation, Nuclear Size, and DNA Replication Efficiency in Xenopus laevis Extracts

  1999cited by this paper
• The Major Nuclear Envelope Targeting Domain of LAP2 Coincides with Its Lamin Binding Region but Is Distinct from Its Chromatin Interaction Domain*

  1998cited by this paper
• Nuclear Membrane Dynamics and Reassembly in Living Cells: Targeting of an Inner Nuclear Membrane Protein in Interphase and Mitosis

  1997cited by this paper
• The lamin B receptor (LBR) provides essential chromatin docking sites at the nuclear envelope.

  1996cited by this paper
• Interaction between an Integral Protein of the Nuclear Envelope Inner Membrane and Human Chromodomain Proteins Homologous to Drosophila HP1*

  1996cited by this paper
• The Salk Institute for Biological Studies(話題)

  1975cited by this paper

• Mitotic dynamics of the nuclear lamina behind the scenes of chromosome separation

  2025cites this paper
• An interkinetic envelope surrounds chromosomes between meiosis I and II in C. elegans oocytes

  2024cites this paper
• Phosphorylation of ELYS promotes its interaction with VAPB at decondensing chromosomes during mitosis

  2024cites this paper
• Non-random spatial organization of telomeres varies during the cell cycle and requires LAP2 and BAF

  2024cites this paper
• Sculpting nuclear envelope identity from the endoplasmic reticulum during the cell cycle

  2024cites this paper
• An interkinetic envelope surrounds chromosomes between meiosis I and II in C. elegans oocytes

  2024cites this paper
• Phosphorylation-dependent interactions of VAPB and ELYS contribute to the temporal progression of mitosis

  2023cites this paper
• Ndc1 drives nuclear pore complex assembly independent of membrane biogenesis to promote nuclear formation and growth

  2022cites this paper
• A role for Nup153 in nuclear assembly reveals differential requirements for targeting of nuclear envelope constituents

  2022cites this paper
• Spatial modeling of telomere intra-nuclear distribution reveals non-random organization that varies during cell cycle and depends on LAP2 and BAF

  2022cites this paper
• Chromosome length and gene density contribute to micronuclear membrane stability

  2021influential citation
• Inherited nuclear pore substructures template post-mitotic pore assembly.

  2021cites this paper
• Mitotic disassembly and reassembly of nuclear pore complexes.

  2021cites this paper
• The Diverse Cellular Functions of Inner Nuclear Membrane Proteins.

  2021cites this paper
• Reticulon-like REEP4 at the inner nuclear membrane promotes nuclear pore complex formation

  2021cites this paper
• Lamin B receptor-mediated chromatin tethering to the nuclear envelope is detrimental to the xenopus blastula.

  2020cites this paper
• Mitotic checkpoint protein Mad1 is required for early Nup153 recruitment to chromatin and nuclear envelope integrity

  2020cites this paper
• Nuclear Membrane Rupture and Its Consequences.

  2020cites this paper
• Interplay of the nuclear envelope with chromatin in physiology and pathology

  2020cites this paper
• The Cell Nucleus and Its Compartments

  2020cites this paper
• Diverse cellular functions of barrier-to-autointegration factor and its roles in disease

  2020cites this paper
• A Cell Cycle Checkpoint for the Endoplasmic Reticulum.

  2020cites this paper
• REEP4 is recruited to the inner nuclear membrane by ELYS and promotes nuclear pore complex formation

  2020cites this paper
• ESCRT-III–mediated membrane fusion drives chromosome fragments through nuclear envelope channels

  2020cites this paper
• Clinical Significance of POM121 Expression in Lung Cancer

  2020cites this paper
• Roles of Nup133, Nup153 and membrane fenestrations in assembly of the nuclear pore complex at the end of mitosis

  2019cites this paper
• ESCRT-III/Vps4 Controls Heterochromatin-Nuclear Envelope Attachments

  2019cites this paper
• Comparative genomics of nuclear envelope proteins

  2018cites this paper
• Precise and economic FIB/SEM for CLEM: with 2 nm voxels through mitosis

  2018cites this paper
• Coaching from the sidelines: the nuclear periphery in genome regulation

  2018cites this paper
• ROLE OF NUCLEAR ENVELOPE PROTEIN MAN1 IN NUCLEAR ORGANISATION AND MAINTENANCE OF GENOME STABILITY

  2018cites this paper
• Dynein pulling forces counteract lamin-mediated nuclear stability during nuclear envelope repair

  2018cites this paper
• Lamin A/C might be involved in the EMT signalling pathway.

  2018cites this paper
• DNA Cross-Bridging Shapes a Single Nucleus from a Set of Mitotic Chromosomes

  2017cites this paper
• Chromosomes Orchestrate Their Own Liberation: Nuclear Envelope Disassembly.

  2017cites this paper
• The gamma-tubulin meshwork as a therapeutic target

  2017cites this paper
• The GTPase DRG1 controls microtubule dynamics and is involved in chromatin decondensation

  2017cites this paper
• Mechanisms and functions of nuclear envelope remodelling

  2017cites this paper
• Cell Biology of the Plant Nucleus.

  2017cites this paper
• A DNA Crosslinker Collects Mitotic Chromosomes.

  2017cites this paper
• Dynein pulling forces on ruptured nuclei counteract lamin-mediated nuclear envelope repair mechanisms in vivo

  2017cites this paper
• Closing a gap in the nuclear envelope.

  2016cites this paper
• Nuclear Reformation at the End of Mitosis.

  2016cites this paper
• Recent advances in understanding nuclear size and shape

  2016influential citation
• Nuclear envelope rupture is induced by actin-based nucleus confinement

  2016cites this paper
• Nuclear Egress of Herpesviruses: The Prototypic Vesicular Nucleocytoplasmic Transport.

  2016cites this paper
• Non-canonical roles of the nucleoporin Nup153 in influenza A virus infection, intracellular transport, and cellular architecture

  2016cites this paper
• Perforating the nuclear boundary – how nuclear pore complexes assemble

  2016cites this paper
• LEM2 recruits CHMP7 for ESCRT-mediated nuclear envelope closure in fission yeast and human cells

  2016cites this paper
• On the mechanism of transport of Inner Nuclear Membrane Proteins

  2016cites this paper
• The lysine demethylase LSD1 is required for nuclear envelope formation at the end of mitosis

  2015cites this paper
• Spatial Reorganization of the Endoplasmic Reticulum during Mitosis Relies on Mitotic Kinase Cyclin A in the Early Drosophila Embryo

  2015cites this paper
• The lysine demethylase LSD1 regulates nuclear envelope formation at the end of mitosis

  2015influential citation
• Nucleosome functions in spindle assembly and nuclear envelope formation

  2015cites this paper
• The Inner Nuclear Membrane Protein Src1 Is Required for Stable Post-Mitotic Progression into G1 in Aspergillus nidulans

  2015cites this paper
• Nuclear envelope and chromatin, lock and key of genome integrity.

  2015cites this paper
• Traffic to the inner membrane of the nuclear envelope.

  2014cites this paper
• Breaching the nuclear envelope in development and disease

  2014cites this paper
• Nuclear assembly as a target for anti-cancer therapies

  2014cites this paper
• Induction of polyploidy by nuclear fusion mechanism upon decreased expression of the nuclear envelope protein LAP2β in the human osteosarcoma cell line U2OS

  2014influential citation
• Localization of Daucus carota NMCP1 to the nuclear periphery: the role of the N-terminal region and an NLS-linked sequence motif, RYNLRR, in the tail domain

  2014cites this paper
• NETs and cell cycle regulation.

  2014cites this paper
• Cancer Biology and the Nuclear Envelope

  2014cites this paper
• Control of nuclear size by NPC proteins.

  2014cites this paper
• Imaging the assembly, structure, and function of the nuclear pore inside cells.

  2014cites this paper
• JCB_201402003 1..9

  2014cites this paper
• Enclosing chromatin: reassembly of the nucleus after open mitosis.

  2013cites this paper
• Functional Characterization of the Nup93 Complex in Nuclear Pore Complex Assembly

  2013cites this paper
• Regulation and coordination of nuclear envelope and nuclear pore complex assembly

  2013cites this paper
• Catastrophic nuclear envelope collapse in cancer cell micronuclei.

  2013cites this paper
• Werner complex deficiency in cells disrupts the Nuclear Pore Complex and the distribution of lamin B1.

  2013cites this paper
• Partitioning and remodeling of the Schizosaccharomyces japonicus mitotic nucleus require chromosome tethers.

  2013cites this paper
• Specific nuclear envelope transmembrane proteins can promote the location of chromosomes to and from the nuclear periphery

  2013cites this paper
• LEM-4 promotes rapid dephosphorylation of BAF during mitotic exit

  2013cites this paper
• Nuclear division: giving daughters their fair share.

  2013cites this paper
• The transport of integral membrane proteins across the nuclear pore complex

  2012cites this paper
• Inner nuclear membrane proteins: targeting and influence on genome organization

  2012cites this paper
• A change in nuclear pore complex composition regulates cell differentiation.

  2012cites this paper
• Visualizing the high curvature regions of post-mitotic nascent nuclear envelope membrane

  2012cites this paper
• Transient nuclear envelope rupturing during interphase in human cancer cells

  2012influential citation
• Nuclear lamina at the crossroads of the cytoplasm and nucleus.

  2012cites this paper
• The C-terminal domain of Nup93 is essential for assembly of the structural backbone of nuclear pore complexes

  2012cites this paper
• Fission yeast Lem2 and Man1 perform fundamental functions of the animal cell nuclear lamina

  2012cites this paper
• Reduced Lymphocyte Longevity and Homeostatic Proliferation in Lamin B Receptor-Deficient Mice Results in Profound and Progressive Lymphopenia

  2012cites this paper
• Building a nuclear envelope at the end of mitosis: coordinating membrane reorganization, nuclear pore complex assembly, and chromatin de-condensation

  2012influential citation
• Repo-Man-PP1

  2012cites this paper
• The nucleoporin ELYS/Mel28 regulates nuclear envelope subdomain formation in HeLa cells

  2012cites this paper
• Dimerization and direct membrane interaction of Nup53 contribute to nuclear pore complex assembly

  2012cites this paper
• How reticulon gets the ER into shape

  2011cites this paper
• Formation of the postmitotic nuclear envelope from extended ER cisternae precedes nuclear pore assembly

  2011cites this paper
• Traversing the NPC along the pore membrane

  2011cites this paper
• Nuclear envelope dynamics during plant cell division suggest common mechanisms between kingdoms.

  2011cites this paper
• and Progressive Lymphopenia Receptor-Deficient Mice Results in Profound Homeostatic Proliferation in Lamin B Reduced Lymphocyte Longevity and

  2011cites this paper
• Temporal control of nuclear envelope assembly by phosphorylation of lamin B receptor

  2011influential citation
• A dominant-negative form of POM121 binds chromatin and disrupts the two separate modes of nuclear pore assembly

  2011cites this paper
• Cell cycle-dependent differences in nuclear pore complex assembly in metazoa.

  2010cites this paper
• Martin Hetzer: Taking the nuclear membrane beyond the barrier

  2010cites this paper
• Genome-nuclear lamina interactions and gene regulation.

  2010cites this paper
• Mad2 prolongs DNA damage checkpoint arrest caused by a double-strand break via a centromere-dependent mechanism.

  2010cites this paper
• Nuclear reformation after mitosis requires downregulation of the Ran GTPase effector RanBP1 in mammalian cells

  2010cites this paper