nuclear envelope dynamics in embryos and somatic cells

Philippe Collas Nuclear Envelope Dynamics in Embryos and Somatic Cells MOLECULAR BIOLOGY INTELLIGENCE UNIT 23 Philippe Collas, Ph.D. Institute of Medical Biochemistry University of Oslo Oslo, Norway Nuclear Envelope Dynamics in Embryos and Somatic Cells MOLECULAR BIOLOGY INTELLIGENCE UNIT 23 K LUWER A CADEMIC / P LENUM P UBLISHERS NEW YORK, NEW YORK U.S.A L ANDES B IOSCIENCE / E UREKAH . COM GEORGETOWN, TEXAS U.S.A Library of Congress Cataloging-in-Publication Data CIP information applied for but not received at time of publishing. NUCLEAR ENVELOPE DYNAMICS IN EMBRYOS AND SOMATIC CELLS Molecular Biology Intelligence Unit 23 Landes Bioscience / Eurekah.com and Kluwer Academic / Plenum Publishers Copyright ©2002 Eurekah.com and Kluwer Academic/Plenum Publishers All rights reserved. No part of this book may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in writing from the publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system; for exclusive use by the Purchaser of the work. Printed in the U.S.A. Kluwer Academic / Plenum Publishers, 233 Spring Street, New York, New York, U.S.A. 10013 http://www.wkap.nl/ Please address all inquiries to the Eurekah.com / Landes Bioscience: Eurekah.com / Landes Bioscience, 810 South Church Street, Georgetown, Texas, U.S.A. 78626 Phone: 512/ 863 7762; FAX: 512/ 863 0081; www.Eurekah.com; www.landesbioscience.com. Landes tracking number: 1-58706-150-3 Nuclear Envelope Dynamics in Embryos and Somatic Cells edited by Philippe Collas/CRC, 184 pp. 6 x 9/ Landes/Kluwer dual imprint/ Landes series: Molecular Biology Intelligence Unit 23, ISBN 0-306-47439-5 While the authors, editors and publishers believe that drug selection and dosage and the specifications and usage of equipment and devices, as set forth in this book, are in accord with current recommend- ations and practice at the time of publication, they make no warranty, expressed or implied, with respect to material described in this book. In view of the ongoing research, equipment development, changes in governmental regulations and the rapid accumulation of information relating to the biomedical sciences, the reader is urged to carefully review and evaluate the information provided herein. CONTENTS Preface ix 1. Dynamics of the Vertebrate Nuclear Envelope 1 Malini Mansharamani, Katherine L. Wilson and James M. Holaska Abstract 1 Interphase Nuclear Envelope Structure 1 Nuclear Envelope Disassembly 3 Nuclear Assembly 5 Concluding Remarks 8 2. Dynamics of Nuclear Envelope Proteins During the Cell Cycle in Mammalian Cells 15 Jan Ellenberg Abstract 15 Why Should Nuclear Envelope Proteins Be Dynamic? 15 What is the Nuclear Envelope Made of? 16 Studying Nuclear Envelope Protein Dynamics 17 Dynamics in Interphase 17 Chromosomes Do not Move Much in Interphase 21 Dynamics in Mitosis 21 INM Proteins: Switching Retention Off and Back On 21 Lamina: Tearing of a Polymer, Dispersion and Re-Import of Monomers 23 Pore Complex Disassembly and Assembly: Many Open Questions 24 Chromosomes: A Complex Template for Nuclear Assembly 25 Concluding Remarks 25 3. Targeting and Retention of Proteins in the Inner and Pore Membranes of the Nuclear Envelope 29 Cecilia Östlund, Wei Wu and Howard J. Worman Abstract 29 Targeting of Integral Membrane Proteins to the Inner Nuclear Membrane 29 Targeting and Retention of Integral Membrane Proteins to the Pore Membrane 35 Targeting of Peripheral Membrane Proteins to the Inner Nuclear Membrane 36 Conclusion 38 4. Dynamic Connections of Nuclear Envelope Proteins to Chromatin and the Nuclear Matrix 43 Roland Foisner Abstract 43 Introduction 43 Major Components of the Peripheral Nuclear Lamina 44 Lamina Proteins in the Nuclear Interior 46 Interactions at the Interface Between the Lamina and the Nuclear Scaffold/Chromatin 47 Potential Functions of Lamina Proteins in Interphase 49 Dynamics and Functions of Lamina-Chromatin Interactions During Mitosis 50 Conclusions and Future Prospects 53 5. Role of Ran GTPase in Nuclear Envelope Assembly 61 Chuanmao Zhang and Paul R. Clarke Abstract 61 Background 61 Control of Nuclear Envelope Assembly by Ran 64 6. Mitotic Control of Nuclear Pore Complex Assembly 73 Khaldon Bodoor and Brian Burke Introduction 73 The Nuclear Lamina 73 The Inner Nuclear Membrane 73 Nuclear Pore Complexes 74 Dynamics of the Nuclear Envelope During Mitosis 76 Nuclear Envelope Breakdown 76 Nuclear Envelope Reformation 77 NPC Assembly 77 When Does the NPC Become Functional? 81 Summary 82 7. Structure, Function and Biogenesis of the Nuclear Envelope in the Yeast Saccharomyces cerevisiae 87 George Simos Introduction 87 Overview of the Yeast NPC and its Function in Transport 88 Composition and Structure-Function Relationships of the Yeast NPC 89 Biogenesis of the Yeast NPCs and Their Role in the Organization of the NE 93 Integral Membrane Proteins of the Yeast NE and Their Function 96 8. Nuclear Envelope Breakdown and Reassembly in C. elegans: Evolutionary Aspects of Lamina Structure and Function 103 Yonatan B. Tzur and Yosef Gruenbaum Abstract 103 The Structure and Protein Composition of the Nuclear Lamina in C. elegans 103 Possible Functions of the Nuclear Lamina in C. elegans 104 Nuclear Dynamics in C. elegans During Mitosis 106 9. Nuclear Envelope Assembly in Gametes and Pronuclei 111 D. Poccia, T. Barona, P. Collas and B. Larijani Abstract 111 Introduction 111 Background 111 Sperm Nuclear Envelope Disassembly 112 Membrane Vesicle Fractions Contributing to the Nuclear Envelope 113 Binding of Egg Cytoplasmic Vesicles to Sperm Chromatin and Nuclear Envelope Remnants 115 Fusion of Nuclear Envelope Precursor Vesicles 117 Completion of Male Pronuclear Envelope Formation 123 Comparison with Other Systems and Speculations 123 Issues for Future Investigation 127 10. Nuclear Envelope Dynamics in Drosophila Pronuclear Formation and in Embryos 131 Mariana F. Wolfner Drosophila Nuclear Envelopes 131 Developmental Changes in Nuclear Envelopes Around the Time of Fertilization 132 Conclusion 138 11. The Distribution of Emerin and Lamins in X-Linked Emery-Dreifuss Muscular Dystrophy 143 G. E. Morris, S. Manilal, I. Holt, D. Tunnah, L. Clements, F.L. Wilkinson, C.A. Sewry and Nguyen thi Man Introduction 143 A Brief History of EDMD 143 The Normal Distribution of Emerin and Lamins 145 Distribution of Emerin and Lamins in X-Linked EDMD 148 12. Laminopathies: One Gene, Two Proteins, Five Diseases 153 Corinne Vigouroux and Gisèle Bonne Abstract 153 Introduction 153 Disorders of Cardiac and/or Skeletal Muscles Linked to LMNA Alterations 154 Lipodystrophies and the Familial Partial Lipodystrophy of the Dunnigan Type (FPLD) 159 Familial Partial Lipodystrophy of the Dunnigan Type (FPLD) 162 Could Some Patients with LMNA Mutations be Affected by Both Skeletal or Cardiac Muscular Symptoms and Lipodystrophy? 163 Experimental Models of Lamin A/C Alterations 163 Nuclear Alterations in Cells Harboring LMNA Mutations 164 Conclusion 166 Addendum 167 Index 173 Philippe Collas, Ph.D. Institute of Medical Biochemistry University of Oslo Oslo, Norway Chapter 9 EDITOR CONTRIBUTORS Teresa Barona Biology Program University Lusofona Lisbon, Portugal Chapter 9 Khaldon Bodoor Department of Anatomy and Cell Biology University of Florida Gainesville, Florida, U.S.A. Chapter 6 Gisele Bonne Institut de Myologie INSERM Paris, France Chapter 12 Brian Burke Department of Anatomy and Cell Biology University of Florida Gainesville, Florida, U.S.A. Chapter 6 Paul R. Clarke Biomedical Research Centre University of Dundee Dundee, Scotland Chapter 5 L. Clements MRIC Biochemistry Group North East Wales Institute Wrexham, England Chapter 11 Jan Ellenberg Gene Expression and Cell Biology/ Biophysics Programmes European Molecular Biology Laboratory Heidelberg, Germany Chapter 2 Roland Foisner Department of Biochemistry and Molecular Cell Biology University of Vienna Vienna, Austria Chapter 3 Yosef Gruenbaum Department of Genetics The Hebrew University of Jerusalem Jerusalem, Israel Chapter 8 James M. Holaska Department of Cell Biology and Anatomy, Johns Hopkins University School of Medicine Baltimore, Maryland, U.S.A Chapter 1 I. Holt MRIC Biochemistry Group North East Wales Institute Wrexham, England Chapter 11 Banafshe Larijani Cell Biophysics Laboratory Imperial Cancer Research Fund London, England Chapter 9 S. Manilal MRIC Biochemistry Group North East Wales Institute Wrexham, England Chapter 11 M. Mansharamani Department of Cell Biology and Anatomy, Johns Hopkins University School of Medicine Baltimore, Maryland, U.S.A Chapter 1 G.E. Morris MRIC Biochemistry Group North East Wales Institute Wrexham, England Chapter 11 Cecilia Östlund Department of Medicine Columbia University New York, New York, U.S.A. Chapter 4 Dominic L. Poccia Department of Biology Amherst College Amherst, Massachusetts, U.S.A. Chapter 9 C.A. Sewry MRIC Biochemistry Group North East Wales Institute Wrexham, England Chapter 11 George Simos Laboratory of Biochemistry University of Thessaly Larissa, Greece Chapter 7 N. thi Man MRIC Biochemistry Group North East Wales Institute Wrexham, England Chapter 11 D. Tunnah MRIC Biochemistry Group North East Wales Institute Wrexham, England Chapter 11 Yonatan B. Tzur Department of Genetics The Hebrew University of Jerusalem Jerusalem, Israel Chapter 8 Corinne Vigouroux Laboratoire de Biologie Cellulaire INSERM Paris, France Chapter 12 F.L. Wilkinson MRIC Biochemistry Group North East Wales Institute Wrexham, England Chapter 11 K.L. Wilson Department of Cell Biology and Anatomy, Johns Hopkins University School of Medicine Baltimore, Maryland, U.S.A Chapter 1 Mariana F. Wolfner Department of Molecular Biology and Genetics Cornell University Ithaca, New York, U.S.A. Chapter 10 Howard J. Worman Department of Medicine Columbia University New York, New York, U.S.A. Chapter 4 Wei Wu Department of Medicine Columbia University New York, New York, U.S.A. Chapter 4 Chuanmao Zhang Biomedical Research Centre University of Dundee Dundee, Scotland Chapter 5 R oughly twenty-five years of studies of the nuclear envelope have revealed that it is more than just a bag of membranes enwrapping chromosomes. The nuclear envelope consists of several domains that interface the cell cytoplasm and the nucleus: the outer and inner nuclear membranes, connected by the pore membrane, the nuclear pore complexes and the filamentous nuclear lamina. Each domain is marked by specific sets of proteins that mediate interactions with cytoplasmic components (such as cytoskeletal proteins) or nuclear structures (such as chromosomes). The nuclear envelope is a highly dynamic structure that reversibly disassembles when cells divide. How these nuclear envelope domains and proteins are sorted at mitosis, and how they are targeted back onto chromosomes of the reforming nuclei in each daughter cell are two fascinating questions that have dominated the field for many years. Another item which in my mind makes the field of the nuclear envelope exciting is the range of organisms in which it has been studied: yeast, sea urchin, star fish, C. elegans, Drosophila, Xenopus, mammalian cells and more. Each model organism displays com- mon features in the ways the nuclear envelope breaks down and reforms, but also pins differences in its organization and dynamics. Another source of enthusiasm is the variety of experimental systems that have been developed to investigate the dynamics of the nuclear envelope. These range from cell- free extracts (again, from eggs or cells of many organisms), to the use of synthetic beads (which a priori have nothing to do with a nucleus), genetic studies in C. elegans and recent elaborate 4-D imaging studies in living mam- malian cells. All these provide unique angles to our view of nuclear envelope behavior. Finally, for many, the nuclear envelope has experienced a ‘rebirth’ after the identification of mutations in two of its components, the inner nuclear membrane protein emerin, and nuclear lamins A and C. Mutations in these proteins are the cause of several forms of dystrophies of skeletal and cardiac muscles and are life-threatening. In twelve chapters, prominent experts in their field deliver the latest views on how molecules and pathways are orchestrated to build, or disassemble, the nuclear envelope. Each chapter is meant to lead the reader to a specific domain of the nuclear envelope or to a particular process, whether this takes place in an egg, an embryo or a somatic—healthy or diseased—cell. Editing this book would have not been possible without the formidable contributions from all authors—many thanks to all of them, an initiative from Ron Landes and the technical support from Cynthia Dworaczyk. I hope this volume will provide the reader with a better appreciation of the biology of the nuclear envelope. Have a good time reading it. Philippe Collas PREFACE [...]... Mammalian Cells 19 Figure 2 Selective retention in interphase and mitosis Schematic illustrating how INM proteins can be localized to the ER and INM-subdomain in interphase and mitosis ER /nuclear membranes contain a typical chromatin binding INM protein (dots) and are in close proximity to chromatin In interphase binding is enabled (arrows), the INM protein can exchange between ER and INM by diffusion and. .. nuclear lamins, which are abundant near the inner membrane We will refer to the lamin Nuclear Envelope Dynamics in Embryos and Somatic Cells, edited by Philippe Collas ©2002 Eurekah.com and Kluwer Academic/Plenum Publishers 2 Nuclear Envelope Dynamics in Embryos and Somatic Cells filaments and lamin-binding proteins collectively as the nuclear lamina The lamina comprises a major element of nuclear architecture... retained in the INM by binding to chromatin In prometaphase binding is disabled (arrows) by phosphorylation and the INM protein dissociates from chromatin and equilibrates with the ER by diffusion In telophase binding is switched back on (arrows) by dephosphorylation and INM proteins diffusing in ER cisternae that come in contact with chromatin are retained and thus reform the INM subdomain by attaching... the lamina and/ or the INM In interphase these four units of NE architecture are connected by a multitude of protein-protein interactions and the NE appears as a complex, highly cross-linked structural protein network (Fig 1).16 Studying Nuclear Envelope Protein Dynamics True insight into NE protein dynamics has mostly come from studying these proteins in their natural environment in living cells In mammalian... non-histone chromatin-associated proteins, named heterochromatin binding protein 1 (HP-1) and Barrier to autointegration factor (BAF), interact with one or many nuclear membrane proteins HP-1 localizes to chromatin during metaphase and binds LBR.33,34,102 The other chromatin-associated protein, BAF, is proposed to interact with all LEM domain proteins, including LAP2, emerin, MAN1, and LEM-3 and otefin.12,64,103... higher affinity for A-type lamins,49 and specifically lamin C.50 The nuclear localization of emerin depends on lamins, since deletion of the only lamin in C elegans causes the loss of emerin protein from the nuclear envelope. 51 Another inner nuclear membrane protein, named RFBP (RING Finger Binding Protein) binds the SWI2/SNF2 related RUSH transcription factors.11 RFBP has nine transmembrane domains; it... fluorescently-labeled nuclear envelope proteins in both fixed and living cells. 56,96,97 ER membranes gain access to chromatin during late anaphase and telophase, and membrane-chromatin contacts are likely to be stabilized by the binding of nuclear membrane proteins to their appropriate ligands on chromatin Chromatin contacts gradually increase in number as additional inner membrane proteins reach the chromatin surface... of nuclear pores doubles during this time.7 Secondly, nuclear architecture needs to be remodeled in response to external stimuli It Nuclear Envelope Dynamics in Embryos and Somatic Cells, edited by Philippe Collas ©2002 Eurekah.com and Kluwer Academic/Plenum Publishers 16 Nuclear Envelope Dynamics in Embryos and Somatic Cells Figure 1 Schematic view of the organization of the interphase nuclear envelope. .. BAF is highly conserved in metazoans,46 but is absent (along with lamins and all other nuclear envelope proteins discussed here) in yeast and plants Like the B-type lamins, BAF is essential for the viability of dividing cells, suggesting fundamental roles in nuclear structure and function.48 Emerin directly binds both A- and B-type lamins as determined by in vitro binding assays and coimmunoprecipitations,... Signals and structural features involved in integral membrane protein targeting to the inner nuclear membrane J Cell Biol 1995; 130:15-27 28 Ellenberg J, Siggia ED, Moreira JE et al Nuclear membrane dynamics and reassembly in living cells: Targeting of an inner nuclear membrane protein in interphase and mitosis J Cell Biol 1997; 138:1193-1206 29 Wu W, Lin F, Worman HJ Intracellular trafficking of MAN1, . near the inner membrane. We will refer to the lamin Nuclear Envelope Dynamics in Embryos and Somatic Cells 2 filaments and lamin-binding proteins collectively as the nuclear lamina. The lamina comprises a. Nuclear Lamina 44 Lamina Proteins in the Nuclear Interior 46 Interactions at the Interface Between the Lamina and the Nuclear Scaffold/Chromatin 47 Potential Functions of Lamina Proteins in Interphase. analysis of nuclear membrane proteins. Nuclear Envelope Dynamics in Embryos and Somatic Cells 6 Nuclear Membrane Protein Targeting to Chromatin Despite being dispersed throughout the ER, most nuclear- specific