EXS 63 Comparative Molecular Neurobiology Edited by Y. Pichon Birkhauser Verlag Basel . Boston . Berlin Editor's address: Dr. Yves Pichon C.N.R.S.-Universite de Rennes I Equipe de Neurobiologie Bat. 13-Complexe Univ. de Beaulieu F-35042 Rennes Cedex France The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher cannot assume any legal responsibility for given data, especially as far as directions for the use and the handling of chemicals and drugs are concerned. This informa tion can be obtained from the manufacturers. Library of Congress Cataloging-in-Publication Data Comparative molecular neurobiology / edited by Y. Pichon. p. cm.-(EXS; 63) Includes bibliographical references and index. ISBN-13: 978-3-0348-7267-6 e-ISBN-13: 978-3-0348-7265-2 DOl: 10.1007/978-3-0348-7265-2 I. Comparative neurobiology. 2. Molecular neurobiology. I. Pichon, Y. (Yves), 1938- . II. Series. [DNLM: I. Ion Channels-physiology. 2. Receptors, Synaptic-physiology. WI E65 v. 63/ WL 102.5 C737] QP356.15.C65 1993 591.1 '88-dc20 DNLM/DLC Deutsche Bibliothek Cataloging-in-Publication Data Comparative molecular neurobiology / ed. by Y. Pichon. - Basel; Boston; Berlin: Birkhiiuser, 1993 (EXS; 63) ISBN-13: 978-3-0348-7267-6 NE: Pichon, Yves [Hrsg.]; GT This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically those of translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying machine or similar means, and storage in data banks. Under §54 of the German Copyright Law, where copies are made for other than private use, a fee is payable to 'Verwertungsgesellschaft Wort', Munich. © 1993 Birkhiiuser Verlag Softcover reprint of the hardcover 1s t edition 1993 P.O. Box 133 CH-4010 Basel Switzerland ISBN-13: 978-3-0348-7267-6 Contents Y. Pichon Foreword. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix Old concepts and new approaches A. Adoutte and H. Philippe The major lines of metazoan evolution: Summary of traditional evidence and lessons from ribosomal RNA sequence analysis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 A. Karschin Heterologous expression of the membrane proteins that control cellular excitability. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31 Ligand-gated ion channels M. G. Darlison, M. L. Hutton and R. J. Harvey Molluscan ligand-gated ion-channel receptors. . . . . . . . . . . . . . . . . 48 J. T. Fleming, C. Tornoe, H. A. Riina, J. Co adwell, J. A. Lewis and D. B. Sattelle Acetylcholine receptor molecules of the nematode Caenorhabditis elegans .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 C. A. Leech and D. B. Sattelle Acetylcholine receptor/channel molecules of insects. . . . . . . . . . . . 81 F. Hannan and L. M. Hall Muscarinic acetylcholine receptors in invertebrates: Comparisons with homologous receptors from vertebrates. . . . . . . . . . . . . . . . 98 A. Taylor, I. Bermudez and D. J. Beadle Pharmacology of the GABA receptor of insect central neurones in culture: A patch-clamp study. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 146 N. M. Anthony, J. B. Harrison and D. B. Sattelle GABA Receptor molecules of insects. . . . . . . . . . . . . . . . . . . . . . .. 172 VI R. H. fJrench-Constant Cloning of a putative GABA receptor from cyclodiene-resistant A Drosophila: A case study in the use of insecticide-resistant mutants to isolate neuroreceptors . . . . . . . . . . . . . . . . . . . . . . . . .. 210 P. Bochet and J. Rossier Molecular biology of excitatory amino acid receptors: Subtypes and subunits .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 224 C. M. Schuster, A. Ultsch, B. Schmitt and H. Betz Molecular analysis of Drosophila glutamate receptors. . . . . . . . .. 234 P. N. R. Usherwood, I. Mellor, L. Breedon, R. J. Harvey, E. A. Barnard and M. G. Darlison Channels formed by M2 peptides of a putative glutamate receptor subunit of locust. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 241 H. P. C. Robinson and N. Kawai Single channel properties at the synaptic site 250 Second messenger-linked receptors R. Hen Structural and functional conservation of serotonin receptors throughout evolution. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 266 G. A. Cottrell The wide range of actions of the FMRFamide-related peptides and the biological importance of peptidergic messengers . . . . . . . .. 279 P. D. Evans Molecular studies on insect octopamine receptors . . . . . . . . . . . .. 286 P. Vernier, H. Philippe, P. Samama and J. Mallet Bioamine receptors: Evolutionary and functional variations of a structural leitmotiv. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 297 Voltage-gated ion channels E. Y. Isacoff, Y. N. Jan and L. Y. Jan Molecular basis of K + channel inactivation gating . . . . . . . . . . .. 338 M. Amar and Y. Pichon Potassium conductance and potassium channels in a primitive insect: The cockroach Periplaneta americana. . . . . . . . . . . . . . .. 352 M. Saito and C. F. Wu Ionic channels in cultured Drosophila neurons . . . . . . . . . . . . . . .. 366 vii Receptor diversity and integrative properties of the neurons J. A. Benson The electrophysiological pharmacology of neurotransmitter recep- tors on locust neuronal somata . . . . . . . . . . . . . . . . . . . . . . . . . .. 390 R. M. Pitman, J. A. David and J. C. Hancox Modulation of insect neurone properties. . . . . . . . . . . . . . . . . . . .. 414 Subject Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 425 lX Foreword It is generally accepted that all living organisms present on earth derive from one single primordial cell born several billion years ago. One important step in the evolution occurred some 1.5 billion years ago with the transition from small procaryote cells with relatively simple internal structures such as bacteria to larger and more compleX: eucaryotic cells such as those found in higher animals and plants. Large membrane proteins which enable the cells to communicate appeared early in evolution, and it is believed that the nerve membrane receptors and ionic channels which are observed today in both invertebrate and vertebrate species derive from a common ancestor. Basically, the three identified superfamilies, 1) ionotropic receptors (i.e. receptors containing an integral ionic channel), 2) metabotropic receptors (receptors coupled to G proteins) and 3) voltage-dependent ionic channels (Na+, K + and Ca2+ channels) were already well differentiated when vertebrates separated from invertebrate species. The large number of subtypes which are observed in each superfamily may be of more recent evolutionary origin. To understand how this happened, the best approach was to compare the sequences and the properties of the receptors and ionic channels in species sufficiently distant in the evolutionary tree. In the present volume, many of the best specialists in the field of comparative molecular neurobiology, several of them working on vertebrate and invertebrate species, have accepted to report their most recent findings. Mter two important intro ductory chapters, one on the lines of metazoan evolution, the other on a powerful new method of heterologous expression of membrane proteins, the volume is divided into four parts, the first three corresponding to the above-mentioned three superfamilies of receptors, the last one, which contains two chapters concerning the general properties of insect neurons. This book contains new information for those interested in the evolution of nerve membrane proteins and their relative contribution to membrane excitability. This significant topic is likely to develop very rapidly during the coming years, thanks to the use of powerful new biochemical and biophysical techniques ofi nvestigation. This information can be used to design more specific drugs and pesticides. It is also very important for the critical evaluation of the extent to which invertebrate species can be used instead of vertebrates for animal experimentation. June 1992 Y. Pichon Comparative Molecular Neurobiology ed.by Y. Pichon © 1993 Birkhiiuser Verlag BaseVSwitzerland The major lines of metazoan evolution: Summary of traditional evidence and lessons from ribosomal RNA sequence analysis Andre Adoutte and Herve Philippe Laboratoire de Biologie Cellulaire 4 (URA D-I134 CNRS), Batiment 444, Universite Paris XI, F-91405 Orsay Cedex (France) Contrary to a widespread belief among biologists, and to diagrams still found in many elementary biology or zoology textbooks, the general pattern of the phylogeny of Metazoa (the multicellular animals) is far from being settled. While there is a strong body of essentially congruent morphological, paleontological and molecular data concern ing the branching pattern within some phyla or classes, most notably the vertebrates, the problem of the overall relationships of the inverte brate phyla is much more open (see Fig. 1 for a summary of conflicting schemes). These 32-36 phyla, however, account by far for most of the biological diversity of animals. They include some huge groups such as Arthopoda or Mollusca, to which many of the favorite experimental organisms discussed at this meeting belong as well as many additional groups also containing experimentally important species (e.g. Ne matoda: Caenorhabditis; Echinodermata: the various sea urchins, both extensively used models in developmental biology; Annelida and Platy helminthes, classical organisms for the study of embryology and regen eration, etc.). As illustrated in detail in books recently devoted to the subject (Barnes, 1987; Brusca and Brusca, 1990; Willmer, 1990), sum marizing and updating over 200 years of comparative anatomy and embryology, defining a phylum is usually straightforward, but it is the establishment of the evolutionary relationships linking the different phyla that is difficult to achieve. The major reasons for this situation are twofold. First, at this level of analysis there often is a paucity of appropriate, phylogenetically useful characters. To understand this statement, the most rigorous procedure used to construct genealogical relationships must be briefly recalled (Hennig, 1966; Wiley, 1981; Mayr and Ashlock, 1991). One first iden tifies characters that appear to be similar between taxa. Then, similarity is more precisely studied to determine whether the topological connex ions of the organ under analysis with surrounding structures in the two 2 taxa are indeed the same. Only in that case can similarity be equated with homology, i.e. similarity due to common ancestry. The coelom and pseudocoelom of invertebrates for example are not homologous: al though both take the form of superficially similar body cavities, their mode of origin and connections with surrounding tissues are quite different (see below). The scales and feathers of vertebrates, in contrast, are a homologous trait. 1 ~::':rorua Deuterostomia '--___ Echinodermata Coelomata =~l Protostomia U I '----- Mo usca - - - - - - - - . Nematoda, Rotifera,... PseJutloc-oelo-mata L--1..--_--_-_-C__=_=_=_ Platyhelminthes Cnidaria Ctenophora '--____________ FlageUata r------------- A --I Pmnera Flagellata Lophophorata Chordata Deuterostomia Hemichordata Echinodermata Coelomata Arthropoda Protostomia Mollusca Platyhelminthes ] Acoelomata B Cnidaria aom. ]_ Hemichmdata Echinodermata Lophophorata Coelomata ]p- Arthropoda Annelida Mollusca Nematoda, Rotifera, ... Pseutlocoelomata Platyhelminthes Cnidaria Acoelomata Ctenophora 1 C Pmnera