The nuclear lamina comes of age

Many nuclear proteins form lamin-dependent complexes, including LEM-domain proteins, nesprins and SUN-domain proteins. These complexes have roles in chromatin organization, gene regulation and signal transduction. Some link the nucleoskeleton to cytoskeletal structures, ensuring that the nucleus and centrosome assume appropriate intracellular positions. These complexes provide new insights into cell architecture, as well as a foundation for the understanding of the molecular mechanisms that underlie the human laminopathies — clinical disorders that range from Emery–Dreifuss muscular dystrophy to the accelerated ageing seen in Hutchinson–Gilford progeria syndrome.

[1]  A. Sasseville,et al.  In vitro interaction of the carboxy‐terminal domain of lamin A with actin , 1998, FEBS letters.

[2]  P. Sarkar,et al.  Hutchinson-Guilford progeria syndrome , 2001, Postgraduate medical journal.

[3]  K. Wilson,et al.  Multiple and surprising new functions for emerin, a nuclear membrane protein. , 2004, Current opinion in cell biology.

[4]  A. Molofsky,et al.  The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye. , 2003, Molecular biology of the cell.

[5]  C. Vigouroux,et al.  Nuclear envelope disorganization in fibroblasts from lipodystrophic patients with heterozygous R482Q/W mutations in the lamin A/C gene. , 2001, Journal of cell science.

[6]  P. Traub,et al.  Maturation of nuclear lamin A involves a specific carboxy‐terminal trimming, which removes the polyisoprenylation site from the precursor; implications for the structure of the nuclear lamina , 1989, FEBS letters.

[7]  Y. Hiraoka,et al.  Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. , 2001, Journal of cell science.

[8]  T. Nakayama,et al.  Regulation of BMP/Dpp signaling during embryonic development , 2000, Cellular and Molecular Life Sciences CMLS.

[9]  K. Wilson,et al.  LAP2 binds to BAF·DNA complexes: requirement for the LEM domain and modulation by variable regions , 2001, The EMBO journal.

[10]  Sui Huang,et al.  Alteration of nuclear lamin organization inhibits RNA polymerase II–dependent transcription , 2002, The Journal of cell biology.

[11]  J. Sanes,et al.  Syne-1, A Dystrophin- and Klarsicht-related Protein Associated with Synaptic Nuclei at the Neuromuscular Junction* , 2000, The Journal of Biological Chemistry.

[12]  M. Krasnow,et al.  A nuclear lamin is required for cytoplasmic organization and egg polarity in Drosophila , 2001, Nature Cell Biology.

[13]  K. Wilson,et al.  Proteins that bind A-type lamins: integrating isolated clues , 2004, Journal of Cell Science.

[14]  Y. Hiraoka,et al.  Emerin binding to Btf, a death-promoting transcriptional repressor, is disrupted by a missense mutation that causes Emery-Dreifuss muscular dystrophy. , 2004, European journal of biochemistry.

[15]  U. Aebi,et al.  Actin in the nucleus: what form and what for? , 2002, Journal of structural biology.

[16]  A. Noegel,et al.  NUANCE, a giant protein connecting the nucleus and actin cytoskeleton. , 2002, Journal of cell science.

[17]  P. Collas,et al.  HA95 and LAP2β mediate a novel chromatin–nuclear envelope interaction implicated in initiation of DNA replication , 2003, The Journal of cell biology.

[18]  K. Wilson,et al.  Emerin Caps the Pointed End of Actin Filaments: Evidence for an Actin Cortical Network at the Nuclear Inner Membrane , 2004, PLoS biology.

[19]  Brian Burke,et al.  Loss of a-Type Lamin Expression Compromises Nuclear Envelope Integrity Leading to Muscular Dystrophy , 1999, The Journal of cell biology.

[20]  M. Han,et al.  Cytoplasmic dynein light intermediate chain is required for discrete aspects of mitosis in Caenorhabditis elegans. , 2001, Molecular biology of the cell.

[21]  C B Harley,et al.  Telomere length predicts replicative capacity of human fibroblasts. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. Vigouroux,et al.  LMNA mutations in atypical Werner's syndrome , 2003, The Lancet.

[23]  W. Lambert,et al.  Nonerythroid αII spectrin is required for recruitment of FANCA and XPF to nuclear foci induced by DNA interstrand cross-links , 2003, Journal of Cell Science.

[24]  U. Aebi,et al.  The single nuclear lamin of Caenorhabditis elegans forms in vitro stable intermediate filaments and paracrystals with a reduced axial periodicity. , 2003, Journal of molecular biology.

[25]  Richard T. Lee,et al.  Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. , 2004, The Journal of clinical investigation.

[26]  H. Horvitz,et al.  unc-83 encodes a novel component of the nuclear envelope and is essential for proper nuclear migration. , 2001, Development.

[27]  Dennis E Discher,et al.  The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber , 2004, Journal of Cell Science.

[28]  Siqun Xu,et al.  Barrier to Autointegration Factor Interacts with the Cone-Rod Homeobox and Represses Its Transactivation Function* , 2002, The Journal of Biological Chemistry.

[29]  K. Schwartz,et al.  Nuclear envelope alterations in fibroblasts from LGMD1B patients carrying nonsense Y259X heterozygous or homozygous mutation in lamin A/C gene. , 2003, Experimental cell research.

[30]  Min Han,et al.  Role of ANC-1 in Tethering Nuclei to the Actin Cytoskeleton , 2002, Science.

[31]  C. Oomens,et al.  Decreased mechanical stiffness in LMNA-/- cells is caused by defective nucleo-cytoskeletal integrity: implications for the development of laminopathies. , 2004, Human molecular genetics.

[32]  D. Fatkin,et al.  Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. , 2004, The Journal of clinical investigation.

[33]  A. Noegel,et al.  Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. , 2004, Experimental cell research.

[34]  Y. Jan,et al.  Germ cell-less encodes a cell type-specific nuclear pore-associated protein and functions early in the germ-cell specification pathway of Drosophila. , 1994, Genes & development.

[35]  E. Hedgecock,et al.  A gene required for nuclear and mitochondrial attachment in the nematode caenorhabditis elegans , 1982, Cell.

[36]  Richard L. Frock,et al.  A-type lamins regulate retinoblastoma protein function by promoting subnuclear localization and preventing proteasomal degradation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[37]  E. Nedivi,et al.  A set of genes expressed in response to light in the adult cerebral cortex and regulated during development. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[38]  R. Foisner,et al.  Lamina-associated polypeptide 2 α binds intranuclear A-type lamins , 2022 .

[39]  C. Shanahan,et al.  The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300. , 2002, Genomics.

[40]  R. Hennekam,et al.  Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. , 2004, Human molecular genetics.

[41]  Paul A. Fisher,et al.  Barrier-to-autointegration factor plays crucial roles in cell cycle progression and nuclear organization in Drosophila , 2003, Journal of Cell Science.

[42]  K. Wilson,et al.  Transcriptional Repressor Germ Cell-less (GCL) and Barrier to Autointegration Factor (BAF) Compete for Binding to Emerin in Vitro * , 2003, The Journal of Biological Chemistry.

[43]  R. Heald,et al.  Nuclear actin and protein 4.1: Essential interactions during nuclear assembly in vitro , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. Shabanowitz,et al.  A myosin I isoform in the nucleus. , 2000, Science.

[45]  Xinran Liu,et al.  The Golgi-Associated Hook3 Protein Is a Member of a Novel Family of Microtubule-Binding Proteins , 2001, The Journal of cell biology.

[46]  Juliet A. Ellis,et al.  The Emery-Dreifuss muscular dystrophy phenotype arises from aberrant targeting and binding of emerin at the inner nuclear membrane. , 1999, Journal of cell science.

[47]  H. Worman,et al.  How do mutations in lamins A and C cause disease? , 2004, The Journal of clinical investigation.

[48]  P. Gönczy,et al.  Cytoplasmic Dynein Is Required for Distinct Aspects of Mtoc Positioning, Including Centrosome Separation, in the One Cell Stage Caenorhabditis elegans Embryo , 1999, The Journal of cell biology.

[49]  M. Cohen,et al.  Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina. , 2001, Trends in biochemical sciences.

[50]  U Aebi,et al.  Nuclear lamins: their structure, assembly, and interactions. , 1998, Journal of structural biology.

[51]  H. Waterham,et al.  Autosomal Recessive HEM/Greenberg Skeletal Dysplasia Is Caused by 3β-Hydroxysterol Δ14-Reductase Deficiency Due to Mutations in the Lamin B Receptor Gene , 2003 .

[52]  N. Maraldi,et al.  Association of emerin with nuclear and cytoplasmic actin is regulated in differentiating myoblasts. , 2003, Biochemical and biophysical research communications.

[53]  M. Taira,et al.  XMAN1, an inner nuclear membrane protein, antagonizes BMP signaling by interacting with Smad1 in Xenopus embryos , 2003, Development.

[54]  A. B. Mukherjee,et al.  Aneuploidy analysis in fibroblasts of human premature aging syndromes by FISH during in vitro cellular aging , 1998, Mechanisms of Ageing and Development.

[55]  K. Wilson,et al.  Matefin, a Caenorhabditis elegans germ line-specific SUN-domain nuclear membrane protein, is essential for early embryonic and germ cell development. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[56]  D. Davis,et al.  Myne-1, a spectrin repeat transmembrane protein of the myocyte inner nuclear membrane, interacts with lamin A/C. , 2002, Journal of cell science.

[57]  H. Horvitz,et al.  UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. , 1999, Development.

[58]  N. L. La Thangue,et al.  Integration of a growth‐suppressing BTB/POZ domain protein with the DP component of the E2F transcription factor , 1999, The EMBO journal.

[59]  R. Foisner,et al.  Nuclear envelope and nuclear matrix: interactions and dynamics , 2001, Cellular and Molecular Life Sciences CMLS.

[60]  N. Stuurman,et al.  Interactions among Drosophila Nuclear Envelope Proteins Lamin, Otefin, and YA , 1998, Molecular and Cellular Biology.

[61]  R. Hegele,et al.  Hutchinson–Gilford progeria syndrome , 2004, Clinical genetics.

[62]  K Weber,et al.  Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. , 2000, Molecular biology of the cell.

[63]  Y. Hiraoka,et al.  BAF is required for emerin assembly into the reforming nuclear envelope. , 2001, Journal of cell science.

[64]  M. Bergo,et al.  Biochemical Studies of Zmpste24-deficient Mice* , 2001, The Journal of Biological Chemistry.

[65]  E. Markiewicz,et al.  Increased solubility of lamins and redistribution of lamin C in X-linked Emery-Dreifuss muscular dystrophy fibroblasts. , 2002, Journal of structural biology.

[66]  U. Aebi,et al.  The nuclear lamina is a meshwork of intermediate-type filaments , 1986, Nature.

[67]  G. Krohne,et al.  Two novel LEM-domain proteins are splice products of the annotated Drosophila melanogaster gene CG9424 (Bocksbeutel). , 2004, European journal of cell biology.

[68]  G. Morris.  The role of the nuclear envelope in Emery-Dreifuss muscular dystrophy. , 2001, Trends in molecular medicine.

[69]  C. Stewart,et al.  The laminopathies: nuclear structure meets disease. , 2003, Current opinion in genetics & development.

[70]  R. Habas,et al.  Msx1 Cooperates with Histone H1b for Inhibition of Transcription and Myogenesis , 2004, Science.

[71]  R. Foisner,et al.  Intermediate filaments: novel assembly models and exciting new functions for nuclear lamins , 2003, Cellular and Molecular Life Sciences CMLS.

[72]  Yosef Gruenbaum,et al.  The nuclear lamina and its functions in the nucleus. , 2003, International review of cytology.

[73]  H. Worman,et al.  Inner nuclear membrane proteins: functions and targeting , 2001, Cellular and Molecular Life Sciences CMLS.

[74]  D. Gilbert,et al.  Actin up in the nucleus , 2004, Nature Reviews Molecular Cell Biology.

[75]  M Krause,et al.  Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleoprotein complex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Jun Fan,et al.  Golgi localization of Syne-1. , 2003, Molecular biology of the cell.

[77]  J. Ahringer,et al.  The C. elegans Hook Protein, ZYG-12, Mediates the Essential Attachment between the Centrosome and Nucleus , 2003, Cell.

[78]  E. C. Schirmer,et al.  Involvement of the Lamin Rod Domain in Heterotypic Lamin Interactions Important for Nuclear Organization , 2001, The Journal of cell biology.

[79]  T. Volk,et al.  A Drosophila Dystrophin-related protein, MSP-300, is required for embryonic muscle morphogenesis , 1996, Mechanisms of Development.

[80]  Y. Hiraoka,et al.  Dynamic interaction between BAF and emerin revealed by FRAP, FLIP, and FRET analyses in living HeLa cells. , 2004, Journal of structural biology.

[81]  P. Dijke,et al.  New insights into TGF-β–Smad signalling , 2004 .

[82]  D. E. Olins,et al.  Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger–Huët anomaly) , 2002, Nature Genetics.

[83]  G. Albrecht-Buehler,et al.  Rigidity of the nucleus during nuclear rotation in 3T3 cells. , 1988, Experimental cell research.

[84]  R. Foisner,et al.  Lamina-associated polypeptide 2alpha binds intranuclear A-type lamins. , 2000, Journal of cell science.

[85]  K. Wilson,et al.  BAF: roles in chromatin, nuclear structure and retrovirus integration. , 2004, Trends in cell biology.

[86]  John R Yates,et al.  Nuclear Membrane Proteins with Potential Disease Links Found by Subtractive Proteomics , 2003, Science.

[87]  D. Hodzic,et al.  Sun2 Is a Novel Mammalian Inner Nuclear Membrane Protein* , 2004, Journal of Biological Chemistry.

[88]  M. Paulin-Levasseur,et al.  MAN1, an Inner Nuclear Membrane Protein That Shares the LEM Domain with Lamina-associated Polypeptide 2 and Emerin* , 2000, The Journal of Biological Chemistry.

[89]  R. Goldman,et al.  Nuclear Lamins a and B1: Different Pathways of Assembly during Nuclear Envelope Formation in Living Cells , 2000 .

[90]  M. L. Watson.  THE NUCLEAR ENVELOPE: ITS STRUCTURE AND RELATION TO CYTOPLASMIC MEMBRANES , 1955 .

[91]  R. Goldman,et al.  Disruption of Nuclear Lamin Organization Alters the Distribution of Replication Factors and Inhibits DNA Synthesis , 1997, The Journal of cell biology.

[92]  Min Han,et al.  Lamin-dependent localization of UNC-84, a protein required for nuclear migration in Caenorhabditis elegans. , 2002, Molecular biology of the cell.

[93]  Peter Teague,et al.  Differences in the Localization and Morphology of Chromosomes in the Human Nucleus , 1999, The Journal of cell biology.

[94]  R. Goldman,et al.  A role for nuclear lamins in nuclear envelope assembly , 2001, The Journal of cell biology.

[95]  R. Foisner,et al.  Distinct Functions of the Unique C Terminus of LAP2α in Cell Proliferation and Nuclear Assembly* , 2002, The Journal of Biological Chemistry.

[96]  A. Bowcock,et al.  Multisystem dystrophy syndrome due to novel missense mutations in the amino-terminal head and alpha-helical rod domains of the lamin A/C gene. , 2002, The American journal of medicine.

[97]  K. Furukawa.  LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. , 1999, Journal of cell science.

[98]  N. Copeland,et al.  Nuclear membrane protein LAP2beta mediates transcriptional repression alone and together with its binding partner GCL (germ-cell-less). , 2001, Journal of cell science.

[99]  K. Wilson,et al.  MAN1 and emerin have overlapping function(s) essential for chromosome segregation and cell division in Caenorhabditis elegans , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[100]  Yosef Gruenbaum,et al.  Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson–Gilford progeria syndrome , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[101]  A. Fainsod,et al.  On the function of BMP‐4 in patterning the marginal zone of the Xenopus embryo. , 1994, The EMBO journal.

[102]  Juliet A. Ellis,et al.  Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. , 2001, Journal of cell science.

[103]  L. Mestroni,et al.  Lamin A/C gene mutation associated with dilated cardiomyopathy with variable skeletal muscle involvement. , 2000, Circulation.

[104]  T. Tsukahara,et al.  CDNA microarray analysis of gene expression in fibroblasts of patients with x‐linked Emery–Dreifuss muscular dystrophy , 2002, Muscle & nerve.

[105]  Min Han,et al.  ANChors away: an actin based mechanism of nuclear positioning , 2003, Journal of Cell Science.

[106]  K. Wilson,et al.  Nesprin‐1α self‐associates and binds directly to emerin and lamin A in vitro , 2002 .

[107]  L. Englmeier,et al.  An Alternative Domain Containing a Leucine-rich Sequence Regulates Nuclear Cytoplasmic Localization of Protein 4.1R* , 2003, The Journal of Biological Chemistry.