Organization and Assembly of Plant and Animal Extracellular Matrix

364 Pages·1990·11.82 MB·English

by  W. Steven Adair (Eds.)

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
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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.)
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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.