Ciliary and Flagellar Membranes Ciliary and Flagellar Metnbranes Edited by Robert A. Bloodgood University qf Virginia School of Medicine Charlottesville, Virginia PLENUM PRESS • NEW YORK AND LONDON Library of Congress Cataloging-In-Publication Data Ciliary and flagellar me~branes I edited by Robert A. Bloodgood. p. cm. Includes bibliographical references. ISBN-13: 978-1-4612-7845-0 e-ISBN-13: 978-1-4613-0515-6 DOI: 10.1007/978-1-4613-0515-6 1. Cell membranes. 2. Cilia and ciliary motion. 3. Flagella (Microbiology) I. Bloodgood, Robert A. [DNLM, 1. Cell Me.brane--physiology. 2. Cell Movement. 3. Cllia­ -physiology. 4. Flagella--physiology. 5. Protozoa--physiology. CS 532.5.E7 c5721 CHSO 1.C55 1989 574.87·S4--dc20 DNLM/DLC for Library of Congress 89-23227 CIP © 1990 Plenum Press, New York A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013 Softcover reprint of the hardcover 1st edition 1990 All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfIlming, recording, or otherwise, without written permission from the Publisher Contributors Joseph C. Besharse Department of Anatomy and Cell Biology, Emory University School of Medicine, Atlanta, Georgia 30322; present address: Department of Anat­ omy and Cell Biology, The University of Kansas Medical Center, Kansas City, Kansas 66103 Robert A. Bloodgood Department of Anatomy and Cell Biology, University of Virginia School of Medicine, Charlottesville, Virginia 22908 Emmanuelle Boisvieux-Ulrich Centre de Biologie Cellulaire C.N.R.S., 94205 Ivry sur Seine Cedex, France G. B. Bouck Department of Biological Sciences, University of lllinois, Chicago, lllinois 60680 Richard A. Cardullo Worcester Foundation for Experimental Biology, Shrews- bury, Massachusetts 01545 Bernadette Chailley Centre de Biologie Cellulaire C.N.R.S., 94205 Ivry sur Seine Cedex, France William L. Dentler Department of Physiology and Cell Biology, University of Kansas, Lawrence, Kansas 66045 Cynthia J. Horst Department of Anatomy and Cell Biology, Emory University School of Medicine, Atlanta, Georgia 30322 Edna S. Kaneshiro Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221-0006 F. M. Klis Department of Molecular Cell Biology, University of Amsterdam, 1098 SM Amsterdam, The Netherlands P. J. Levasseur Department of Biological Sciences, University of lllinois, Chicago, lllinois 60680 A. Musgrave Department of Molecular Cell Biology, University of Amsterdam, 1098 SM Amsterdam, The Netherlands Robin R. Preston Laboratory of Molecular Biology, University of Wisconsin, Madison, Wisconsin 53706 v Preface While there have been many recent books on the cell surface and a few on the topic of cilia and flagella, this is the fIrst volume that attempts to bring together the available informa­ tion on ciliary and flagellar membranes. This reflects a slow awakening by cell biologists and other scientists to the signifIcance of ciliary and flagellar surfaces. When Michael Sleigh edited an excellent book entitled Cilia and Flagella in 1974, not one of the sixteen chapters was devoted to ciliary or flagellar surfaces. When W. B. Amos and J. G. Duckett edited the very fIne 25th Symposium of the Society for Experimental Biology on Prokaryotic and Eukaryotic Flagella in 1982, only two of the twenty chapters on eu­ karyotic cilia and flagella were devoted to ciliary and flagellar surfaces. Only in 1989 has the timing become right to produce a volume entirely devoted to the nonaxonemal struc­ tures and functions of eukaryotic cilia and flagella. The fIfteen chapters in this volume cover a wide spectrum of organisms (from protozoa and algae to birds and mammals) and an equally wide spectrum of topics (from sexual interactions in the algae to the binding of pathogens in the lung). It is hoped that almost any biological or medical scientist will fInd at least a few chapters of interest and I will bet that few who peruse this book will fail to discover at least a couple of roles for ciliary and flagellar surfaces that they had never imagined. For those readers who may be relatively new to the subject, Dr. George Witman has prepared an introductory chapter that introduces the reader to the general features of cilia and flagella and in particular to those aspects of their structure and function that influence or are influenced by the phenomena occurring at the ciliary or flagellar surface. Eukaryotic cilia and flagella are essentially specialized cytoplasmic domains contain­ ing a highly structured cytoskeleton incompletely bounded by a specialized domain of the plasma membrane. For that reason, they are excellent systems in which to study mem­ brane-cytoskeletal interactions and indeed many of the functions of ciliary and flagellar surfaces will only be understood as deriving from a functional interaction of the mem­ brane with the underlying cytoskeleton. Eukaryotic cilia and flagella also constitute ideal systems for studying a defIned plasma membrane domain because the act of deciliation or deflagellation immediately isolates a specialized domain of the plasma membrane; there is little contamination with other membrane material because these organelles lack any internal membranes. While cilia and flagella have been recognized as motile organelles from the time of their discovery by Leeuwenhoek in approximately 1676, it is only recently that biologists have come to appreciate that cilia and flagella perform many other roles aside from the movement of cells through a liquid medium or the movement of fluid (or mucus) across a ciliated epithelium. Many of these additional functions derive from properties of ciliary vii viii Preface and flagellar surfaces, here defined as the ciliary or flagellar membrane along with all of its associated appendages (coats, scales, mastigonemes). In fact, the first paper that dealt with the surface of eukaryotic cilia or flagella was probably that published in 1889 by Loeffler; he included a clear photograph of the mastigonemes (or Flimmergeissel) on the flagellar surface of a chrysophycean algal cell. The first person to seriously study the flagellar surface using the electron microscope was probably Manton (see Manton, 1952, for a review). One of the biggest technical advances in the study of cilia and flagella came from the ability to isolate cilia and flagella, extract them with nonionic detergents, and obtain axonemes that could be reactivated to produce patterns of bending motility strikingly similar to those seen in vivo (Gibbons, 1981). Ironically, at the same time that this opened up much detailed study of the motile functions of ciliary and flagellar axonemes, it drew attention away from the study of ciliary and flagellar surfaces. In fact, many scientists studying cilia and flagella routinely discard all of the membrane and soluble components of these organelles down the laboratory sink as so much unnecessary junk! Although the naked axoneme can exhibit motile behavior, the normal regulation of the motile activity of cilia and flagella is dependent upon the ciliary or flagellar mem­ brane. An elegant combination of genetic, biochemical, and electrophysiological ap­ proaches using the ciliate protozoan Paramecium has demonstrated how the behavior of the ciliary axoneme (and the entire organism) is controlled by a complicated array of ion channels and pumps within the ciliary membrane (see chapter by Preston and Saimi in this volume). In fact, the general field of sensory transduction and membrane signaling is one of the more exciting ways in which ciliary and flagellar membranes are being utilized to study basic biological problems. From the avoidance response in Paramecium to the initial sexual contact in Chlamydomonas gametes to the very human appreciation of an expensive perfume, signal transduction mechanisms in cilia and flagella are at work. While the chapters in this book range widely in a phylogenetic and functional sense, there is no claim of completeness. For lack of space, a few interesting functions of ciliary and flagellar membranes have not been reviewed in this volume. For example, the ciliary membranes of olfactory receptor cells are responsible for binding the odorant molecules (Snyder et al.• 1989); this binding initiates a transmembrane signaling process involving G protein activation of a membrane-associated adenylate cyclase, an increase inintracili­ ary cyclic nucleotide level, and a direct cyclic nucleotide gating of ciliary membrane sodium channels (Nakamura and Gold, 1987; Lancet, 1988). The adhesion of certain free­ living marine invertebrates is known to occur by means of specializations of the ciliary surface (Tyler, 1973). A third topic not represented in the present volume is a considera­ tion of the evolution of ciliary and flagellar surface specializations, a topic that has been studied by Bardele (1981, 1983). Despite these few omissions, the vast majority of research related to ciliary and flagellar membranes is reviewed within the present volume. My sincere thanks go to all of the chapter authors; their excellent and timely contributions have made this unique volume possible. Special thanks go to Mary Phillips Born and Susan Woolford at Plenum Publish­ ing for their efforts on behalf of this volume. Robert A. Bloodgood Charlottesville. Virginia Preface ix References Bardele, C. F., 1981, Functional and phylogenetic aspects of the ciliary membrane: A comparative freeze­ fracture study,