Table Of ContentEXS 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
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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
