Extracellular Matrix Biology
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1 Extracellular Matrix Biology A subject collection from Cold Spring Harbor Perspectives in Biology
2 OTHER SUBJECT COLLECTIONS FROM COLD SPRING HARBOR PERSPECTIVES IN BIOLOGY Protein Homeostasis Calcium Signaling The Golgi Germ Cells The Mammary Gland as an Experimental Model The Biology of Lipids: Trafficking, Regulation, and Function Auxin Signaling: From Synthesis to Systems Biology The Nucleus Neuronal Guidance: The Biology of Brain Wiring Cell Biology of Bacteria Cell Cell Junctions Generation and Interpretation of Morphogen Gradients Immunoreceptor Signaling NF-kB: A Network Hub Controlling Immunity, Inflammation, and Cancer Symmetry Breaking in Biology The Origins of Life The p53 Family
3 Extracellular Matrix Biology A subject collection from Cold Spring Harbor Perspectives in Biology EDITED BY Richard O. Hynes Howard Hughes Medical Institute Massachusetts Institute of Technology Kenneth M. Yamada National Institutes of Health COLD SPRING HARBOR LABORATORY PRESS Cold Spring Harbor, New York
4 Extracellular Matrix Biology A Subject Collection from Cold Spring Harbor Perspectives in Biology Articles online at All rights reserved # 2012 by Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York Printed in the United States of America Executive Editor Managing Editor Production Editor Project Manager Permissions Administrator Production Manager/Cover Designer Publisher Richard Sever Maria Smit Diane Schubach Barbara Acosta Carol Brown Denise Weiss John Inglis Front cover artwork: Human fibroblast within a three-dimensional collagen extracellular matrix. This live primary human fibroblast, expressing fluorescently tagged vinculin (red-gold), was imaged in a three-dimensional collagen gel (reflection microscopy, cyan). The vinculin is clustered in prominent cell-matrix adhesions. Image provided by Ryan Petrie, NIDCR, NIH. Library of Congress Cataloging-in-Publication Data Extracellular matrix biology / edited by Richard O. Hynes, Kenneth M. Yamada. p. cm. Includes index. ISBN (hardcover : alk. paper) 1. Extracellular matrix. 2. Cell interaction. I. Hynes, Richard O. II. Yamada, Kenneth M. III. Title. QP88.23.E dc All World Wide Web addresses are accurate to the best of our knowledge at the time of printing. Authorization to photocopy items for internal or personal use, or the internal or personal use of specific clients, is granted by Cold Spring Harbor Laboratory Press, provided that the appropriate fee is paid directly to the Copyright Clearance Center (CCC). Write or call CCC at 222 Rosewood Drive, Danvers, MA ( ) for information about fees and regulations. Prior to photocopying items for educational classroom use, contact CCC at the above address. Additional information on CCC can be obtained at CCC Online at All Cold Spring Harbor Laboratory Press publications may be ordered directly from Cold Spring Harbor Laboratory Press, 500 Sunnyside Blvd., Woodbury, New York Phone: in Continental U.S. and Canada. All other locations: (516) FAX: (516) cshpress@cshl.edu. For a complete catalog of all Cold Spring Harbor Laboratory Press publications, visit our website at
5 Contents Preface, vii Overview of the Matrisome An Inventory of Extracellular Matrix Constituents and Functions, 1 Richard O. Hynes and Alexandra Naba Basement Membranes: Cell Scaffoldings and Signaling Platforms, 17 Peter D. Yurchenco The Collagen Family, 45 Silvie Ricard-Blum Heparan Sulfate Proteoglycans, 65 Stephane Sarrazin, William C. Lamanna, and Jeffrey D. Esko The Thrombospondins, 99 Josephine C. Adams and Jack Lawler Tenascins and the Importance of Adhesion Modulation, 129 Ruth Chiquet-Ehrismann and Richard P. Tucker Fibronectins, Their Fibrillogenesis, and In Vivo Functions, 149 Jean E. Schwarzbauer and Douglas W. DeSimone Integrin Structure, Activation, and Interactions, 169 Iain D. Campbell and Martin J. Humphries Cross Talk among TGF-b Signaling Pathways, Integrins, and the Extracellular Matrix, 183 John S. Munger and Dean Sheppard Molecular Architecture and Function of Matrix Adhesions, 201 Benjamin Geiger and Kenneth M. Yamada Genetic Analyses of Integrin Signaling, 223 Sara A. Wickström, Korana Radovanac, and Reinhard Fässler Integrins and Extracellular Matrix in Mechanotransduction, 245 Martin Alexander Schwartz Integrins in Cell Migration, 259 Anna Huttenlocher and Alan Rick Horwitz v
6 Contents Extracellular Matrix Degradation and Remodeling in Development and Disease, 275 Pengfei Lu, Ken Takai, Valerie M. Weaver, and Zena Werb Extracellular Matrix in Development: Insights from Mechanisms Conserved between Invertebrates and Vertebrates, 299 Nicholas H. Brown Angiogenesis, 313 Donald R. Senger and George E. Davis Extracellular Matrix: Functions in the Nervous System, 333 Claudia S. Barros, Santos J. Franco, and Ulrich Müller Cell Extracellular Matrix Interactions in Normal and Diseased Skin, 357 Fiona M. Watt and Hironobu Fujiwara Extracellular Matrix Proteins in Hemostasis and Thrombosis, 371 Wolfgang Bergmeier and Richard O. Hynes Index, 389 vi
7 Preface THIRTY YEARS AGO, BETTY HAY ORGANIZED AN INFLUENTIAL VOLUME on the extracellular matrix (ECM) that emphasized the biological effects of the ECM on cells. 1 That timely book recognized an increasing emphasis on biology in a field that had been dominated previously by biochemical and structural analyses. It was published just prior to the beginning of the impact of molecular biology on studies of ECM proteins and, during the past 30 years, we have witnessed several major transformations in our ability to understand the biology as well as the biochemistry and structure of the ECM and its molecular constituents. Among the transformational advances that one can list are molecular biology, the use of genetically engineered mice, the sequencing of multiple genomes, progress in the genetics of ECM-based diseases, and advances in imaging of cells in culture and in intact animals. These advances have led to a much more profound understanding of the roles of ECM in biological processes. The original Hay volume served as a valuable resource for the field and was followed by a second edition 10 years later. 2 We felt that the time was ripe for an updated overview of the biology of ECM, and we agreed to take on this challenge when Richard Sever at Cold Spring Harbor Laboratory Press invited us to do so. Given the ubiquity and complexity of ECMs and the enormous advances made, this was indeed a daunting task. One cannot expect to cover, in a single volume, all that we now know about ECMs, the molecules that they contain, and the myriad effects that they have upon cellular behavior. So, although we have not attempted to assemble a complete treatise on ECMs and their constituents, we have endeavored to illustrate the manifold aspects of ECM biology. The first seven chapters review the overall composition and some of the major and best understood components of the ECM: collagens, proteoglycans, and major glycoproteins. In each case, the biochemical and structural data are linked to biological functions and in many cases to human diseases. The first chapter gives an overview of the diversity of ECM proteins as revealed by genomic analyses, which provides a reasonably complete picture of the universe of ECM proteins. Basement membranes and their constituents (laminins, type IV collagen, nidogens, and perlecan) are reviewed by Yurchenco with emphasis on assembly of basement membranes, a key form of ECM universal to all metazoa. Ricard-Blum discusses the many forms of collagen and their assembly into a variety of fibrils. Both chapters discuss the cellular receptors that interact with these forms of ECM. Sarrazin et al. review the important functions of heparan sulfate proteoglycans and their interactions with soluble factors and with cell-surface receptors. The following three chapters cover three of the most intensively studied ECM glycoprotein families: thrombospondins (Adams and Lawler), tenascins (Chiquet-Ehrismann and Tucker), and fibronectins (Schwarzbauer and DeSimone). Each of these families of glycoproteins has particular biologically interesting features that collectively illustrate very well the diversity of ECM functions across almost all of biology. Implicit in the concept that the ECM helps to regulate cellular behavior is a requirement for cellular receptors to receive, interpret, and transmit the inputs. At the time of the first Hay volume, we did not have any idea how cells recognize ECM, and it was not until the mid-1980s that the molecular nature of ECM receptors became clear. The most prominent ECM receptors are integrins, present in 1 Hay ED, ed Cell biology of extracellular matrix. Plenum, New York. 2 Hay ED, ed Cell biology of extracellular matrix, 2nd ed. Plenum, New York. vii
8 Preface all metazoa and on virtually all cells. These are complex receptors, transmitting signals both into and out of cells and mediating the effects of ECM on cells and vice versa, so we have included a series of chapters covering their properties. Integrin structure and activation are reviewed by Campbell and Humphries, their ability to activate TGF-b through interactions with fibrillins and the latent TGF-b binding proteins in the ECM are covered by Munger and Sheppard, and their roles in assembling complex intracellular protein complexes with both structural and signal transduction functions are discussed by Geiger and Yamada. Wickström et al. illustrate the insights that can be gained from studies in mutant animals and contrast integrin connections to the actin-based cytoskeleton with those to intermediate filaments. These chapters lay the ground for considering the roles of integrin ECM interactions involved in mechanotransduction (Schwartz) and in cell migration (Huttenlocher and Horwitz). One of the prime reasons for interest in ECM proteins and their receptors comes from their roles in diverse biological processes, and the last third of this volume comprises a set of chapters addressing some of these processes and the involvement of the ECM. Matrix structure is not static; it is, in fact, very dynamic and the remodeling of the ECM plays an important role in development, physiology, and pathology (Lu et al. and Brown). Specific biological contexts in which ECM functions are particularly important are illustrated by angiogenesis (Senger and Davis), the nervous system (Barros et al.), normal and diseased skin (Watt and Fujiwara), and hemostasis and thrombosis (Bergmeier and Hynes). Each of these chapters illustrates different aspects of ECM functions. Collectively, these chapters encompass the diverse roles of ECM proteins, their effects on cells, and their importance in human diseases. Our increased understanding of the details of ECM structure and function coming from biochemistry; cellular, molecular, and structural biology; genetics; and genomics has confirmed their importance in the behavior of virtually all cells. Even erythrocytes, arguably the prototypical nonadherent cell type, have key interactions with the ECM during their development. It has become clear that cell ECM interactions and receptors are at least as important as those between soluble ligands (hormones, growth factors, cytokines) and their receptors. Indeed, many so-called soluble ligands actually function as ECM-bound solid-phase ligands, and many of them are completely dependent on concomitant input from ECM adhesion receptors. The central roles in development of the ECM suggested long ago by embryologists such as Clifford Grobstein have been amply confirmed, and there are preliminary indications that fundamental aspects of development and homeostasis, such as morphogen gradients and stem cell niches, rely on ECM involvement. Many human diseases arise from mutations in genes encoding ECM proteins as recognized by Victor McKusick, and cell-matrix adhesion and signaling are also affected in many autoimmune diseases. These important and fascinating topics are increasingly understood as we uncover the details of cell ECM interactions and their perturbations in disease. Drugs targeting ECM interactions are already in use in the clinic for many diseases, and it is evident that many other potential therapies will emerge from ongoing research. We hope that this collection of reviews by experts in the field will serve to promote research leading to discoveries and applications based on improved understanding of the roles of the ECM constituents, their interactions, and their receptors. RICHARD O. HYNES KENNETH M. YAMADA July 2011 viii
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