ORGANIZATION AND ASSEMBLY OF PLANT AND ANIMAL EXTRACELLULAR MATRIX W STEVEN ADAIR Edited by Tufts University Schools of Medicine, Dentistry, and Veterinary Medicine Department of Anatomy and Cell Biology Boston, Massachusetts ROBERT P. MECHAM Department of Medicine Jewish Hospital at Washington University Medical Center St. Louis, Missouri ACADEMIC PRESS, INC. HARCOURT BRACE JOVANOVICH, PUBLISHERS SAN DIEGO NEW YORK BOSTON LONDON SYDNEY TOKYO TORONTO Front cover photographs: (Top) Cell membrane and cell wall of Chlamydomonas eugametos. (From Goodenough, U. W., and Heuser, J. E. (1988). /. Cell Sei. 90, 735-750, Fig. 1.) (Center) Cell wall of Chlamydomonas eugametos. (Ibid, Fig. 2.) (Bottom) Cell-wall crystals of Chlamydomonas reinhardtii. (From Goodenough, U. W., Gebhart, Â., Mecham, R. P., and Heuser, J. E. (1986). /. Cell Biol. 103, 405-417, Fig. 4.) This book is printed on acid-free paper. @ Copyright © 1990 by Academic Press, Inc. All Rights Reserved. No part of this publication 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. Academic Press, Inc. San Diego, California 92101 United Kingdom Edition published by Academic Press Limited 24-28 Oval Road, London NW1 7DX Library of Congress Cataloging-in-Publication Data Organization and assembly of plant and animal extracellular matrix / W. Steven Adair and Robert P. Mecham, editors, p. cm. — (Biology of extracellular matrix) Includes bibliographical references. ISBN 0-12-044060-1 (alk. paper) 1. Extracellular matrix. 2. Cell physiology. 3. Molecular biology. I. Adair, W. Steven. II. Mecham, Robert P. III. Series. [DNLM: 1. Cells-physiology. 2. Extracellular Matrix-physiology. 3. Molecular Biology. QU 105 068] QH603.E93074 1990 574.87-dc20 DNLM/DLC for Library of Congress 89-18633 CIP Printed in the United States of America 90 91 92 93 9 8 7 6 5 4 3 2 1 W Steven Adair (1946-1990) On March 27th, skiing alone on a difficult slope, Steve Adair collided with a tree and was killed instantly. He was an expert skier and a fearless one. The fearlessness cost him his life but also defined it. In the lab, in scientific discussion, in everything he did, Steve combined expertise and courage with marvelously creative results. His most im- portant intellectual insight—a recognition of the homology between sexual adhesion and cell-wall assembly in Chlamydomonas—repre- sented a discontinuous and critical leap in our understanding of both processes. The enormous range of approaches that he applied so suc- cessfully to his research is testimony to his technical skill and bravado. Those of us whose lives were touched by his warmth, generosity, and exuberance are saddened by his loss. Contributors Numbers in parentheses indicate the pages on which the authors' contributions begin. W. STEVEN ADAIR, Tufts University Schools of Medicine, Dentistry, and Veterinary Medicine, Department of Anatomy and Cell Biology, Boston, Massachusetts 02111 (15) MARK C. ALLIEGRO, Department of Zoology, Duke University, Durham, North Carolina 27706 (1) M. ANDREAE, Abteilung Cytologie, Pflanzenphysiologisches Institut und Botanischer Garten, der Universität Göttingen, Untere Karspüle 2, 3400 Göttingen, West Germany (283) STEVEN D. BLACK, Department of Zoology, Duke University, Durham, North Carolina 27706 (1) P. BLANKENSTEIN, Abteilung Cytologie, Pflanzenphysiologisches Institut und Botanischer Garten, der Universität Göttingen, Untere Karspüle 2, 3400 Göttingen, West Germany (283) ARISTIDIS S. CHARONIS, Department of Laboratory Medicine and Pathology, University of Minnesota Medical School, Minneapolis, Minnesota 55455 (85) CAROL M. CONDIT, Departments of Biochemistry and Plant Science, University of Nevada, Reno, Nevada 89557 (119) JACK E. DIXON, Department of Biochemistry, Purdue University, West Lafayette, Indiana 47907 (301) GEORGE C. FULLER, College of Pharmacy and Allied Health Professions, Wayne State University, Detroit, Michigan 48202 (301) xi xii CONTRIBUTORS NORBERTO A. GUZMAN1, Protein Research Unit, Princeton Biochemicals Inc., Princeton, New Jersey 08543 (301) BEAT KELLER, Swiss Federal Research Station for Agronomy, CH-8046 Zürich, Switzerland (119) WATSON M. LAETSCH, Department of Plant Biology, University of California, Berkeley, California 94720 (137) DAVID R. MCCLAY, Department of Zoology, Duke University, Durham, North Carolina 27706 (1) RAFAEL PONT-LEZICA, Department of Biology, Washington University, St Louis, Missouri 63130 (173) D. G. ROBINSON, Abteilung Cytologie, Pflanzenphysiologisches Institut und Botanisheer Garten, der Universität Göttingen, Untere Karspüle 2, 3400 Göttingen, West Germany (283) DOMINIQUE RUMEAU2, Department of Botany, Molecular and Cellular Biology Program, Ohio University, Athens, Ohio 45701 (247) ALLAN M. SHOW ALTER, Department of Botany, Molecular and Cellular Biology Program, Ohio University, Athens, Ohio 45701 (247) WILLIAM J. SNELL, The University of Texas Southwestern Medical Center at Dallas, Department of Cell Biology and Neuroscience, Dallas, Texas 75235 (15) EFFIE C. TSILIBARY, Department of Laboratory Medicine and Pathology, University of Minnesota Medical School, Minneapolis, Minnesota 55455 (85) Present address: P. O. Box 1014, E. Brunswick, New Jersey 08816. Present address: Université Paul Sabatier, Centre de Physiologie Végétale, 118 route de Narbonne, 31062 Toulouse Cédex, France. CONTRIBUTORS xiii GERARDO R. VASTA, Department of Biochemistry, and Molecular Biology, Medical University of South Carolina, Charleston, South Carolina 29425 (173) VALERIE VREELAND, Department of Plant Biology, University of Carolina, Berkeley, California 94720 (137) Preface Over the past several years, the extracellular matrix has emerged as a central focus of studies on eukaryotic growth and development (normal and abnormal). In addition to their obvious structural roles, both animal and plant extracellular matrices (ECMs) are now known to play active roles in a wide range of biological processes, many re- quiring molecular recognition. Although functional parallels between certain plant and animal macromolecules have been known for some time, only recently has their potential significance been fully appreci- ated with the discovery of structural analogies between collagens and plant hydroxyproline-rich glycoproteins (HRGPs) and their associated polysaccharide polymers. This volume in the series of Biology of Extra- cellular Matrix is unique in that work on plant and animal systems is presented in a common forum. It was prompted by recent develop- ments of new methods and novel systems for studies of plant and ani- mal matrix recognition and assembly and an increasing body of knowl- edge suggesting that certain principles underlying establishment of complex three-dimensional architecture cross broad evolutionary boundaries. The collection of articles presents a state-of-the-art view of some of the most current experimental systems in plant and animal matrix biology. In the first chapter, McClay et al. review recent studies on the cellu- lar mechanisms responsible for storage, release, assembly, and func- tion of extracellular matrices during early sea urchin development. Among the most prominent constituents are proteins immunologically related to known vertebrate ECM molecules. The ontogenetic appear- ance of these and other matrix components demonstrates that the sea urchin egg is highly organized for storage and release of matrix mate- rial to a degree not previously appreciated. The second chapter (Adair and Snell) describes the structure, assembly, disassembly, and molecu- lar biology of the Chlamydomonas reinhardtii cell wall. Unlike higher plant cell walls, the extracellular matrix of this unicellular alga lacks prominent polysaccharide polymers, being constructed entirely from HRGPs, thus facilitating studies of HRGP assembly and characteriza- tion of cell-wall degrading enzymes (lysins). In the third chapter, Charonis and Tsilibary summarize the current state of work on base- ment membrane assembly. In describing the biochemistry, molecular XV xvi PREFACE interactions, and assembly activities of basement membrane compo- nents they provide important insights into approaches to identify criti- cal molecular domains and an appreciation of the complexity of relat- ing defined molecular associations to establishment of matrix architecture. In the fourth chapter, Condit and Keller describe a family of newly discovered cell wall genes that encode protein products containing up to 70% glycine. These unusual genes display developmental regula- tion, cellular specificity, and activation by wounding, suggesting that their gene products play important developmental and/or homeostatic roles that remain to be uncovered. In the fifth chapter, Vreeland and Laetsch describe the role of alginate self-assembly in cell wall forma- tion in Fucus. This marine brown alga has a cell wall made up almost entirely of carbohydrates, several of which bear similarities to animal glycosaminoglycans. Primary cell wall formation follows a defined pro- gram that can be studied in a synchronous population allowing de- tailed analysis of carbohydrate—carbohydrate assembly interactions. The sixth chapter (Vasta and Pont-Lezica) addresses the issue of pro- tein-carbohydrate recognition with a detailed discussion of plant and animal lectins. Members of this broad class of carbohydrate-binding proteins have been found in almost all living systems and have been implicated in a wide variety of biological processes involving molecu- lar recognition. While important in their own right, these proteins have recently gained additional significance with the identification of lectinlike domains in a variety of other proteins, including receptors for matrix components and some enzymes. In the seventh chapter, Showalter and Rumeau discuss a family of genes that encode higher plant HRGPs. Like their functional animal counterparts, the collagens, plant HRGPs are members of a large fam- ily of molecules that have evolved to perform an array of structural, developmental, and homeostatic roles. Showalter and Rumeau exam- ine the relationships between the HRGP genes cloned to date and their protein products, their proposed functions and molecular interactions; and their possible relations with other plant and animal proteins. The final two chapters are devoted to one of the most important classes of protein modifying enzymes for extracellular matrix formation and function, the prolyl hydroxylases. Robinson et al. describe the isola- tion, characterization, and localization of a plant prolyl hydroxylase, while Guzman et al. discuss the isolation, substrate-specificity, and physiological significance of a large group of genetically distinct classes of prolyl 4-hydroxylases, enzymes that appear to play impor- tant roles at several levels during matrix formation. This volume appears at a time when research on extracellular ma- trix touches on almost all areas of cell, molecular, and developmental PREFACE xvii biology. As the body of knowledge increases and it becomes more and more difficult for the individual researcher to keep abreast of develop- ments in areas outside his or her own area of expertise, it is important to provide forums that display a diversity of experimental approaches and paradigms. This is particularly important when work crosses broad evolutionary boundaries. It is hoped that this presentation of current work on plant and animal matrix together will allow workers in both areas to benefit from information, approaches, and ideas that they may not normally encounter. W. STEVEN ADAIR ROBERT P. MECHAM The Ontogenetic Appearance of Extracellular Matrix during Sea Urchin Development David R. McClay, Mark C. Alliegro, and Steven D. Black Department of Zoology, Duke University, Durham, North Carolina 27706 I. Introduction II. Compartmentalization of Extracellular Matrix in the Oocyte III. Movement of Vesicles before and after Fertilization IV. Polarization of Cells in ECM Component Release V. Hyaline Layer Requirement for Blastocoel Formation VI. Hyaline Layer Support of Morphogenetic Movements at Mesenchyme Blastula and Gastrula Stages VII. Basal Lamina as a Substrate for Morphogenesis I. INTRODUCTION An extracellular matrix (ECM) is present throughout the life of an organism. In the sea urchin even the unfertilized egg is protected by the vitelline layer which is a matrix of varying thickness depending upon the species. At fertilization the vitelline layer is elevated away from the zygote and is replaced by secretion of a new matrix, the hya- line layer, onto the cell surface. During cleavage, ECM molecules are also released into the nascent basal lamina that will underlie the epi- thelium for the remainder of the organism's life. When the embryo comprises several hundred cells, morphogenetic movements are initiated that alter the spherical shape of the embryo. Many studies in vitro and in vivo suggest that the ECM is important in morphogenesis as a substrate for the movement of cells as well as being the structure that provides different mechanical properties to a variety of tissues. In addition, cellular differentiation appears to re- quire cell-matrix interactions. If cells are separated from the matrix, or if the matrix is not provided to cells, a number of morphogenetic events do not occur. Since the ECM molecules are released from the zygote so early, the ι Organization and Assembly of Plant Copyright © 1990 by Academic Press, Inc. and Animal Extracellular Matrix All rights of reproduction in any form reserved.