Living Together: The Biology of Animal Parasitism

460 Pages·1986·33.48 MB·English

by  William Trager (auth.)

Living Together
The Biology of
Animal Parasitism
Living Together
The Biology of
Animal Parasitism
William Trager
The Rockefeller University
New York, New York
Library of Congress Cataloging in Publication Data
Trager, William, 1910-
Living together.
Includes bibliographical references and index.
1. Host-parasite relationships. I. Title. II. Title: Biology of animal parasitism.
QL757.T67 1986 591.5'249 86-15097
First Printing-September 1986
Second Printing-February 1988
© 1986 Plenum Press, New York
Softcover reprint of the hardcover 1s t edition 1988
A Division of Plenum Publishing Corporation
233 Spring Street, New York, N.Y. 1000
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
ISBN: 13: 978-1-4615-9467-3 e-ISBN- 13: 978-1-4615-9465-9
DOl: 10.1007/978-1-4615-9465-9
To Ida
Foreword
William Trager has been an avid student of parasites for over 50 years at the
Rockefeller University. Around the turn of this century, parasitology enjoyed
a certain vogue, inspired by colonial responsibilities of the technically ad-
vanced countries, and by the exciting etiological and therapeutic discoveries
of Ross, Manson, Ehrlich, and others. For some decades, the Western hemi-
sphere's interest in animal parasites has been eclipsed by concern for bacteria
and viruses as agents of transmissible disease. Only very recently, initiatives
like the Tropical Disease Research programs of WHO-World Bank-UNDP,
and the Great Neglected Disease networks of the Rockefeller and MacArthur
Foundations have begun to compensate for the neglect of these problems by
United States federal health research agencies. Throughout that period, how-
ever, the Rockefeller Institute (later University) has given high priority to the
challenges of parasitism, corresponding during a formidable period with Dr.
Trager's own career.
The present work then, is a distillation of the insight collected by our
principal doyen of parasite biology, informed but by no means confined to
his own research. It is addressed to the reader of broad biological interest
and training, not to the specialist. The disarmingly unpretentious style makes
the work readily accessible to college undergraduates or even to gifted high
school students; but do not be deceived thereby, as it has an enormous range
of factual information and theoretical insight, familiar to few, but potentially
important to most biologists. This was a shrewd and well-contrived choice,
and I am sure the book will add much to the current momentum of interest
in the field.
Trager's work is organized by themes of biological interest, not by the
taxonomy of the parasites or of the disease syndromes of the hosts; but these
are not neglected where pertinent. As the title implies it concerns the biology
of parasitism, not just a survey of parasites. The writing is therefore in the
tradition of Theobald Smith, McFarlane Burnet, and Rene Dubos whose writ-
ings have been so important in bringing bacteria and viruses, and their par-
asitic behavior, into the mainstream framework of evolutionary biology. Like
these forerunners, Trager focuses on the developmental, biochemical, and
vii
viii FOREWORD
genetic adaptations by which the parasite exploits its special ecological niche,
and by which the host seeks to retain its own Malthusian fitness in the face
of that challenge. Extraordinarily, he is able to unite a half-century of expe-
rience with the latest findings and perspectives of molecular biology, which
is, of course, bringing this field of study into a revolutionary new phase.
What impressed me, and what will enrich a generation of new molecular
parasitology entrants seeking key research problems, is the range of fabulous
stories in this book. It is a veritable Arabian Nights of narrative, not of the
human imagination, but of Nature's, in the exposition of phenomena of ad-
aptation and specificity. On every page, the author exhibits his profound
awareness of the conundrums they pose for physico-chemical and devel-
opmental-genetic principles still to be elaborated-to explain specificity for
hosts and organs, tropisms, response to host rhythms, and endocrinology;
the morphogenetic cycling of vegetative/reproductive phases, and the ques-
tions these raise for the differential control of gene expression. Nothing in
the biology of the parasitic relationship escapes notice, be it the nutritional
requirements of the parasite, the molecular genetics of the kinetoplasts, the
mechanisms of pathogenesis, the host defenses, or the rationale and means
of chemotherapy. Amusing and challenging are the reports of ways in which
parasites alter host behavior and even growth towards the ends of the parasite.
I am tempted to borrow his examples; but that would be transparent and
redundant plagiarism-the reader has but to turn to random pages, or scan
the logically organized Contents. The work is also enriched by a systematic
set of life cycle diagrams, indispensable for an overview of parasite natural
history. For writing so easily digested, it is also fully documented in the
bibliography following each chapter. It should be said that parasite here is
meant to embrace animal parasites of other animal species, though the prin-
ciples will be of great pertinence to parasitism by fungi, bacteria, and even
viruses.
Many young scientists will, I hope, read this work: There are enough
research challenges to keep them all fully occupied in an area which is as rich
with human needs as it is with challenges to biological imagination. Others
will find great stimulation and enjoyment, and a small lament that we do not
have multiple lifetimes to enjoy and observe what the next decades of research
will bring to the field, which Trager sings of so eloquently.
Joshua Lederberg
President
The Rockefeller University
New York, New York
Acknowledgments
Much of this book was written during several summers at the Marine Bio-
logical Laboratory at Woods Hole, Massachusetts. I have been very fortunate
in having available to me the resources of two outstar'lding biological libraries:
one at the Marine Biological Laboratory and the other at the Rockefeller Uni-
versity, my scientific home for over 50 years. I have also been fortunate in
having a dedicated staff. In particular I want to thank Mr. James Stanorski
for accurate and rapid preparation of the manuscript and Mr. Erminio Gubert
for skillful mounting of the illustrations. My laboratory work, meanwhile,
was kept going through the outstanding ability of Mrs. Marika Tershakovec,
research technician, and the devoted help of Mrs. Cora Fields.
I am indebted to the following fellow scientists who kindly reviewed
particular sections of the book and gave me the benefit of their comments
and suggestions. Professor P.A. 0' Alesandro, School of Public Health, Co-
lumbia University; Professor Joel E. Cohen, Population Laboratory, the Rock"
efeller University; Professor G.A.M. Cross, Laboratory of Molecular Parasi-
tology, the Rockefeller University; Professor D. Despommier, School of Public
Health, Columbia University; Professor H.N. Lanners, Tulane University
Medical School; Professor F. von Lichtenberg, Harvard University Medical
School; Professor A.J. Macinnis, Department of Zoology, University of Cal-
ifornia, Los Angeles; Professor M. Miiller, Laboratory of Biochemical Cytol-
ogy, the Rockefeller University; Professor N. Noguiera, New York University
Medical School; Professor Margaret Perkins, Laboratory of Biochemical Cy-
tology, the Rockefeller University; Dr. A. Sher, Laboratory of Parasitic Dis-
eases, National Institute of Allergy and Infectious Diseases; Professor L. Simp-
son, Biology Department, University of California, Los Angeles; Professor
M.J. Ulmer, Iowa State University and University of Bridgeport, Connecticut;
Professor c.c. Wang, Department of Pharmaceutical Chemistry, University
of California, San Francisco; and Professor L.P. Weiss, School of Veterinary
Medicine, University of Pennsylvania.
I am especially grateful to Dr. Joshua Lederberg, President of the Rock-
efeller University, for having been so kind as to write the Foreword.
William Trager
IX
Contents
1. Introduction................................................. 1
2. The Establishment of Infection. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 29
3. Site Selection within the Host: Entry into Specific Organs
and Cells. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
4. The Host-Parasite Interface I: In Extracellular Parasites ...... . .. 71
5. The Host-Parasite Interface II: In Intracellular Parasites
(Protozoa and the Nematode Trichinella spira lis) ............... 81
6. The Uptake of Nutrients. Digestion. .... . . .. . . . . . . . . . . . . .... .. 97
7. Nutritional Requirements. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 109
8. Cultivation of Parasites in Vitro with Special Reference to
Differentiation in the Life Cycle .............................. 121
9. Metabolism: Energy Sources. Respiration ...................... 147
10. Genetics. Developmental Biology ............................. 171
11. The Kinetoplast and Kinetoplast DNA. . . . . . . . . . . . . . . . . . . . . . . .. 185
12. Parasite-Induced Modifications of the Host: Growth Factors.
Effects on Behavior. Parasitic Castration ....................... 201
13. Modification of Host Cells Produced by Intracellular Protozoa. .. 209
14. Innate Resistance ............................................ 227
xi
xii CONTENTS
15. The Spleen .................................................. 239
16. Immunity in Invertebrates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 247
17. The Immune System of Vertebrates in Relation to
Parasitic Infections. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 253
18. Immune Reactions to Trypanosomes and How They Are Evaded.
Ablastin. Antigenic Variation ................................. 265
19. Immunity to Malaria and Related Intracellular Protozoa. . . . . . . .. 281
20. Immunology of Leishmaniasis and American Trypanosomiasis
(Chagas'Disease) ............................................ 309
21. Schistosomiasis and Concomitant Immunity ................... 321
22. Entamoeba histolytica and Other Intestinal Protozoa.
Pathogenesis and Immunology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 337
23. Acquired Immunity to Intestinal Nematodes and to Ticks ....... 347
24. Symbiosis ................................................... 367
25. Chemotherapy ............................................... 385
26. Ecology and Population Biology of Parasites. Sanitation and
Vector Control. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 423
Epilogue ......................................................... 449
Taxonomic Index to the Parasites and Vectors Considered ........... 453
Subject Index .................................................... 459
CHAPTER 1
Introduction
Parasitism involves an intimate association between two different kinds of
organisms. One of these, the host, provides food and shelter for the other,
the parasite. The host mayor may not be injured by the parasite. It may soon
expel the parasite, or it may harbor it for many years. Since the parasite
cannot exist in nature without its host, it is not to the parasite's advantage
to destroy its host. At least it must not destroy it until it is ready to move to
another. Some hosts are benefited by certain parasites and some are actually
dependent on their parasites, a special type of association called mutualism.
Such mutualistic or symbiotic associations may have been at the origin of
chloroplasts and mitochondria, and so at the basis of most eukaryotic cells.
Throughout the living world, from prokaryotes to man, parasitic asso-
ciations are very common. There is no organism (except for the viruses) that
does not have its parasites. Furthermore, all the major taxonomic groups
include organisms that are parasitic. To study parasites as organisms in their
own right is relatively simple and straightforward. But to study the interre-
lations between the parasite and its host, i.e., to study parasitism, requires
all the disciplines of biology from ecology to biophysics. It is this approach,
study of the physiology, biochemistry, and cell biology of host-parasite re-
lationships, that will constitute the main body of future work in parasitology,
and it is this approach that will be followed in this book.
I begin with a discussion of the establishment of infection. How do par-
asites get from one host to another? How do they recognize and enter ap-
propriate hosts and then find their way to particular organs and cells? Equally
important are the factors in the host permitting it to accept the parasite. We
must remember that all organisms are well equipped with mechanisms for
the rejection of foreign structures, living as well as dead. This discussion will
lead in a logical way to consideration of what occurs at the parasite-host
interface, the roles of surfaces and membranes in sheltering and nourishing
the parasite. It is here that uptake of nutrients occurs. I then treat the nutri-
tional requirements of the parasites for growth and differentiation, with some
emphasis on their cultivation in vitro. This is followed by discussions of the
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