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Basic
IMMUNOLOGY
FU NCTIO N S A N D D ISOR D ER S OF THE IM M U NE SYSTE M
This page intentionally left blank

     
 SIXTH EDITION

Basic
IMMUNOLOGY
FUNCTIONS A ND DISORDERS OF THE IMMUNE SYSTEM

Abul K. Abbas, MBBS Shiv Pillai, MBBS, PhD

Professor Emeritus, Pathology Professor of Medicine and Health Sciences
University of California San Francisco and Technology
San Francisco, California Harvard Medical School
Massachusetts General Hospital
Andrew H. Lichtman, MD, PhD Boston, Massachusetts
Professor of Pathology
Harvard Medical School
Illustrations by David L. Baker, MA
Brigham and Women’s Hospital
DNA Illustrations, Inc.
Boston, Massachusetts
BASIC IMMUNOLOGY: FUNCTIONS AND DISORDERS OF
THE IMMUNE SYSTEM, SIXTH EDITION ISBN: 978-0-323-54943-1
Copyright © 2020 by Elsevier Inc. All rights reserved.

No part of this publication may be reproduced or transmitted in any form or by any means, electronic or me-
chanical, including photocopying, recording, or any information storage and retrieval system, without permis-
sion in writing from the publisher. Details on how to seek permission, further information about the Publisher’s
permissions policies, and our arrangements with organizations such as the Copyright Clearance Center and the
Copyright Licensing Agency can be found at our website: www.elsevier.com/permissions.

This book and the individual contributions contained in it are protected under copyright by the Publisher (other
than as may be noted herein).

Notice

Practitioners and researchers must always rely on their own experience and knowledge in evaluating and
using any information, methods, compounds or experiments described herein. Because of rapid advances in
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from any use or operation of any methods, products, instructions, or ideas contained in the material herein.

Previous editions copyrighted 2016, 2014, 2011, 2009, 2006, 2004, and 2001.

International Standard Book Number: 978-0-323-54943-1

Executive Content Strategist: James Merritt

Senior Content Strategist: Jeremy Bowes
Director, Content Development: Rebecca Gruliow
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To our students
 P R E FAC E

The sixth edition of Basic Immunology has been revised also discussed immunologic diseases from the perspec-
to include recent important advances in our knowledge tive of principles, emphasizing their relation to normal
of the immune system. The original goals of this book, immune responses and avoiding details of clinical syn-
from the earliest edition, were to present current con- dromes and treatments. We have included selected clin-
cepts in immunology cogently and also in sufficient ical cases in an appendix to illustrate how the principles
detail that they would be understood by students of of immunology may be applied to common human dis-
the discipline, as well as to emphasize clinical aspects, eases. Finally, in order to make each chapter readable on
including disease pathogenesis and the development of its own, we have repeated key ideas in different places in
novel therapies based on the basic science of immunol- the book. We feel such repetition will help students to
ogy. These are the goals that we continue to strive for. grasp the most important concepts.
With improving understanding of the normal immune We hope that students will find this new edition of
response, we believe it is possible to present the funda- Basic Immunology clear, cogent, manageable, and enjoy-
mental knowledge in a concise way. In addition, there able to read. We hope the book will convey our sense
has been exciting progress in applying basic principles of excitement about how the field has evolved and how
to understanding and treating human diseases, a topic it continues to grow in relevance to human health and
that is of paramount interest for students of medicine disease. Finally, although we were spurred to tackle this
and allied health sciences. Foremost among these recent project because of our associations with medical school
advances is the development of cancer immunotherapy, courses, we hope the book will be valued by students of
which dramatically illustrates how foundational science allied health and biology as well. We will have succeeded
can be translated into clinical practice. if the book can answer many of the questions these stu-
More specifically, we have focused on the following dents have about the immune system and, at the same
objectives. First, we have presented the most important time, encourage them to delve even more deeply into
principles governing the function of the immune sys- immunology.
tem by synthesizing key concepts from the vast amount Several individuals played key roles in the writing of
of experimental data that have emerged in the field of this book. Our editor, James Merritt, has been an enthu-
immunology. Our judgment of what is most important siastic source of encouragement and advice. Our tal-
is based largely on what is most clearly established by ented illustrator, David Baker, continues to effectively
scientific investigation and is essential for understand- convert our ideas into pictures that are informative and
ing the major functions of the immune system. We aesthetically pleasing. Our development editor, Rebecca
have also prioritized content that is relevant to human Gruliow, has kept the project organized and on track
health and disease. We have realized that in any con- despite pressures of time and logistics. Clay Broeker
cise discussion of complex phenomena, it is inevitable has moved the book through the production process
that exceptions and caveats cannot be considered in in an efficient and professional manner. To all of them
detail, so these have largely been omitted. Second, we we owe our many thanks. Finally, we owe an enormous
have focused on immune responses against infectious debt of gratitude to our families, whose support and
microbes, and most of our discussions of the immune encouragement have been unwavering.
system are in this context. Third, we have made liberal
use of illustrations to highlight important principles, Abul K. Abbas
but we have reduced factual details that may be found Andrew H. Lichtman
in more comprehensive textbooks. Fourth, we have Shiv Pillai

vi
 CONTENTS
  1 Introduction to the Immune System, 1   8 Effector Mechanisms of Humoral Immunity, 158
Nomenclature, General Properties, and Components Elimination of Extracellular Microbes and Toxins

  2 Innate Immunity, 23   9 Immunologic Tolerance and Autoimmunity, 177

The Early Defense Against Infections Self–Nonself Discrimination in the Immune System and Its
Failure
  3 Antigen Capture and Presentation to
Lymphocytes, 51 10 Immunology of Tumors and Transplantation, 196
What Lymphocytes See Immune Responses to Cancer Cells and Normal Foreign Cells

  4 Antigen Recognition in the Adaptive 11 Hypersensitivity, 218

Immune System, 73 Disorders Caused by Immune Responses
Structure of Lymphocyte Antigen Receptors and Development
12 Congenital and Acquired Immunodeficiencies, 235
of Immune Repertoires
Diseases Caused by Defective Immunity
  5 T Cell–Mediated Immunity, 96
Activation of T Lymphocytes  elected Readings, 252
S
Glossary, 260
  6 Effector Mechanisms of T Cell–Mediated
Appendix I: Principal Features of Selected
Immunity, 119
CD Molecules, 288
Functions of T Cells in Host Defense
Appendix II: Cytokines, 296
  7 Humoral Immune Responses, 137 Appendix III: Clinical Cases, 300
Activation of B Lymphocytes and Production of Antibodies Index, 313

vii
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Basic
IMMUNOLOGY
FU NCTIO N S A N D D ISOR D ER S OF THE IM M U NE SYSTE M
This page intentionally left blank

     
 1
Introduction to the
Immune System
Nomenclature, General
Properties, and Components

CHAPTER OUTLINE
Innate and Adaptive Immunity, 3 Antigen-Presenting Cells, 14
Types of Adaptive Immunity, 4 Tissues of the Immune System, 15
Properties of Adaptive Immune Responses, 6 Peripheral (Secondary) Lymphoid Organs and
Specificity and Diversity, 6 Tissues, 15
Memory, 7 Lymphocyte Recirculation and Migration into
Other Features of Adaptive Immunity, 8 Tissues, 20
Cells of the Adaptive Immune System, 9 Summary, 21
Lymphocytes, 9

The term “immunity” in a biologic context has his- a more inclusive definition of the immune response is a
torically referred to resistance to pathogens; however, reaction to microbes, as well as to other molecules that
reactions to some noninfectious substances including are recognized as foreign, regardless of the physiologic or
harmless environmental molecules, tumors, and even pathologic consequence of such a reaction. Immunology is
unaltered host components are also considered forms of the study of immune responses in this broader sense and of
immunity (allergy, tumor immunity, and autoimmunity, the cellular and molecular events that occur after an organ-
respectively). The collection of cells, tissues, and mole- ism encounters microbes and other foreign molecules.
cules that mediate these reactions is called the immune The importance of the immune system for health
system, and the coordinated response of these cells and is dramatically illustrated by the frequent observation
molecules to pathogens and other substances comprises that individuals with defective immune responses are
an immune response. susceptible to serious, often life-threatening infections.
The most important physiologic function of the Conversely, stimulating immune responses against
immune system is to prevent or eradicate infections microbes through vaccination is the most effective
(Fig. 1.1), and this is the principal context in which immune method for protecting individuals against infections;
responses are discussed throughout this book. In addition, this approach has led to the worldwide eradication of
it prevents the growth of some tumors, and some cancers smallpox, the only disease that has been eliminated
can be treated by stimulating immune responses against from civilization by human intervention (Fig. 1.2). The
tumor cells. The immune system also plays a major role in appearance of acquired immunodeficiency syndrome
the repair of damaged tissues. Because the immune system (AIDS) in the 1980s tragically emphasized the impor-
can respond to microbial and nonmicrobial substances tance of the immune system for defending individuals
and also can cause disease under some circumstances, against infection.

1
2 CHAPTER 1 Introduction to the Immune System

Role of the immune system Implications

Defense against infections Deficient immunity results in
increased susceptibility to
infections; exemplified by AIDS
Vaccination boosts immune
defenses and protects against
infections
Defense against tumors Potential for immunotherapy
of cancer
Control of tissue Repair of damaged tissues
regeneration and scarring
The immune system can Immune responses are the cause
injure cells and induce of allergic, autoimmune, and other
pathologic inflammation inflammatory diseases

The immune system Immune responses are barriers to

recognizes and responds transplantation and gene therapy
to tissue grafts and newly
introduced proteins
Fig. 1.1 Importance of the immune system in health and disease. This table summarizes some of the phys-
iologic functions of the immune system and its role in disease. AIDS, Acquired immunodeficiency syndrome.

In contrast to these beneficial roles, abnormal immune • H ow are the cells and tissues of the immune system
responses cause many inflammatory diseases with seri- organized to find and respond to microbes in ways
ous morbidity and mortality. The immune response is that lead to their elimination?
the major barrier to the success of organ transplantation, The basic principles introduced here set the stage for
which is often used to treat organ failure. The products more detailed discussions of immune responses in later
of immune cells can also be of great practical use. For chapters. A Glossary of the important terms used in this
example, antibodies, which are proteins made by certain book is provided near the end of the book.
cells of the immune system, are used in clinical labora-
tory testing and in research as highly specific reagents
for detecting a wide variety of molecules in the circu-
INNATE AND ADAPTIVE IMMUNITY
lation and in cells and tissues. Antibodies designed to Host defenses are grouped under innate immunity,
block or eliminate potentially harmful molecules and which provides immediate protection against micro-
cells are used widely for the treatment of immunologic bial invasion, and adaptive immunity, which develops
diseases, cancers, and other types of disorders. For all more slowly and provides more specialized defense
these reasons, the field of immunology has captured the against infections (Fig. 1.3). Innate immunity, also
attention of clinicians, scientists, and the lay public. called natural immunity or native immunity, is always
This chapter introduces the nomenclature of immu- present in healthy individuals (hence the term innate),
nology, important general properties of all immune prepared to block the entry of microbes and to rapidly
responses, and the cells and tissues that are the principal eliminate microbes that do succeed in entering host tis-
components of the immune system. In particular, the sues. Adaptive immunity, also called specific immunity
following questions are addressed: or acquired immunity, requires proliferation and differ-
• What types of immune responses protect individuals entiation of lymphocytes in response to microbes before
from infections? it can provide effective defense (i.e., it adapts to the pres-
• What are the important characteristics of immunity, ence of microbial invaders). Innate immunity is phylo-
and what mechanisms are responsible for these char- genetically older, and the more specialized and powerful
acteristics? adaptive immune response evolved later.
 CHAPTER 1 Introduction to the Immune System 3

Disease Maximum number Number of

of cases (year) cases in 2014
Diptheria 206,939 (1921) 0
Measles 894,134 (1941) 72
Mumps 152,209 (1968) 40
Pertussis 265,269 (1934) 311
Polio 21,269 (1952) 0
(paralytic)
Rubella 57,686 (1969) 0
Tetanus 1,560 (1923) 0
Hemophilus ~20,000 (1984) 134
influenzae
type B infection
Hepatitis B 26,611 (1985) 58
Fig. 1.2 Effectiveness of vaccination for some common infectious diseases in the United States. Many
infectious diseases for which effective vaccines have been developed have been virtually eradicated in the
United States and other developed countries. (Modified from Orenstein WA, Hinman AR, Bart KJ, Hadler SC.
Immunization. In: Mandell GL, Bennett JE, Dolin R, editors: Principles and practices of infectious diseases,
4th ed. New York: Churchill Livingstone, 1995; and MMWR 66, No. 1, 2017.)

In innate immunity, the first line of defense is pro- recognize a much wider variety of molecules produced
vided by epithelial barriers of the skin and mucosal by microbes, as well as noninfectious molecules. Any
tissues and by cells and natural antibiotics present in molecule that is specifically recognized by lymphocytes
epithelia, all of which function to block the entry of or antibodies is called an antigen. Adaptive immune
microbes. If microbes do breach epithelia and enter the responses often use the cells and molecules of the innate
tissues or circulation, several other components of the immune system to eliminate microbes. For example,
innate immune system defend against them, includ- antibodies (a component of adaptive immunity) bind to
ing phagocytes and innate lymphoid cells, and several microbes, and these coated microbes avidly bind to and
plasma proteins, such as the complement system. In activate phagocytes (a component of innate immunity),
addition to providing early defense against infections, which ingest and destroy the microbes. Examples of the
innate immune responses are required to initiate adap- cooperation between innate and adaptive immunity are
tive immune responses against the infectious agents. discussed in later chapters.
The components and mechanisms of innate immunity By convention, the term immune response generally
are discussed in detail in Chapter 2. refers to adaptive immunity, and that is the focus of
The adaptive immune system consists of lympho- most of this chapter.
cytes with highly diverse and variable receptors for The cells of the immune system are located in dif-
foreign substances, and the products of these cells, ferent tissues and serve different roles in host defense.
such as antibodies. Adaptive immune responses are Most of these cells are derived from bone marrow pre-
essential for defense against infectious microbes that are cursors that circulate in the blood and are called leuko-
pathogenic for humans (i.e., capable of causing disease) cytes (white blood cells). Others are present in tissues at
and may have evolved to resist innate immunity. The cells all times. Some of these cells function mainly in innate
and molecules of innate immunity recognize structures immunity, others in adaptive immunity, and some func-
shared by classes of microbes, whereas the lymphocytes tion in both types of responses. These cells are grouped
of adaptive immunity express receptors that specifically into two broad categories—lymphoid cells (most of
Discovering Diverse Content Through
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 168. See Appendix, note 52.

169. Richardson de la Peinture, vol. i. p. 74.

170. Geschichte der Kunst, p. 347.

171. Not Apollodorus, but Polydorus. Pliny is the only one who mentions these
artists, and I am not aware that the manuscripts differ in the writing of the name.
Had such been the case, Hardouin would certainly have noticed it. All the older
editions also read Polydorus. Winkelmann must therefore have merely made a
slight error in transcribing.

172. Ἀθηνόδωρος δὲ καὶ Δαμέας ... οὗτοι δὲ Ἀρκάδες εἰσὶν ἐκ Κλείτορος.

Phoc. cap. ix. p. 819 (edit. Kuhn).

173. Plinius, lib. xxxiv. sect. 19.

174. Lib. xxxvi. sect. 4. “Nor are there many of great repute the number of
artists engaged on celebrated works preventing the distinction of individuals; since
no one could have all the credit, nor could the names of many be rehearsed at once:
as in the Laocoon, which is in the palace of the emperor Titus, a work surpassing
all the results of painting or statuary. From one stone he and his sons and the
wondrous coils of the serpents were sculptured by consummate artists, working in
concert: Agesander, Polydorus, and Athenodorus, all of Rhodes. In like manner
Craterus with Pythodorus, Polydectes with Hermolaus, another Pythodorus with
Artemon, and Aphrodisius of Tralles by himself, filled the palaces of the Cæsars on
the Palatine with admirable statuary. Diogenes, the Athenian, decorated the
Pantheon of Agrippa, and the Caryatides on the columns of that temple rank
among the choicest works, as do also the statues on the pediment, though these,
from the height of their position, are less celebrated.”

175. Bœotic. cap. xxxiv. p. 778 (edit. Kuhn).

176. Plinius, lib. xxxvi. sect. 4, p. 730.

177. Geschichte der Kunst, part ii. p. 331.

178. Plinius, xxxvi. sect. 4.... “which would make the glory of any other place.
But at Rome the greatness of other works overshadows it, and the great press of
business and engagements turns the crowd from the contemplation of such things;
for the admiration of works of art belongs to those who have leisure and great
quiet.”

179. See Appendix, note 53.

180. Plinius, xxxvi. sect. 4.

 181. Geschichte der Kunst, part ii. p. 347.

182. Lib. xxxvi. sect. 4.

183. See Appendix, note 54.

184. Prefatio Edit. Sillig. “Lest I should seem to find too much fault with the
Greeks, I would be classed with those founders of the art of painting and sculpture,
recorded in these little volumes, whose works, although complete and such as
cannot be sufficiently admired, yet bear a suspended title, as Apelles or Polycletus
‘was making’; as if the work were always only begun and still incomplete, so that
the artist might appeal from criticism as if himself desirous of improving, had he
not been interrupted. Wherefore from modesty they inscribed every work as if it
had been their last, and in hand at their death. I think there are but three with the
inscription, ‘He made it,’ and these I shall speak of in their place. From this it
appeared that the artists felt fully satisfied with their work, and these excited the
envy of all.”

185. See Appendix, note 55.

186. Geschichte der Kunst, part i. p. 394.

187. Cap. i. “He was also reckoned among their greatest leaders, and did many
things worthy of being remembered. Among his most brilliant achievements was
his device in the battle which took place near Thebes, when he had come to the aid
of the Bœotians. For when the great leader Agesilaus was now confident of victory,
and his own hired troops had fled, he would not surrender the remainder of the
phalanx, but with knee braced against his shield and lance thrust forward, he
taught his men to receive the attack of the enemy. At sight of this new spectacle,
Agesilaus feared to advance, and ordered the trumpet to recall his men who were
already advancing. This became famous through all Greece, and Chabrias wished
that a statue should be erected to him in this position, which was set up at the
public cost in the forum at Athens. Whence it happened that afterwards athletes
and other artists [or persons versed in some art] had statues erected to them in the
same position in which they had obtained victory.”

188. See Appendix, note 56.

189. Περὶ Ὕψους, τμῆμα, ιδ’ (edit. T. Fabri), ρ. 36, 39. “But so it is that
rhetorical figures aim at one thing, poetical figures at quite another; since in poetry
emphasis is the main object, in rhetoric distinctness.”

190. “So with the poets, legends and exaggeration obtain and in all transcend
belief; but in rhetorical figures the best is always the practicable and the true.”

191. De Pictura Vet. lib. i. cap. 4, p. 33.

 192. Von der Nachahmung der griech. Werke, &c., 23.

193. Τμῆμα, β. “Next to this is a third form of faultiness in pathos, which

Theodorus calls parenthyrsus; it is a pathos unseasonable and empty, where
pathos is not necessary; or immoderate, where it should be moderate.”

194. Geschichte der Kunst, part i. p. 136.

195. Herodotus de Vita Homeri, p. 756 (edit. Wessel).

196. Iliad, vii.

197. Geschichte der Kunst, part i. p. 176. Plinius, lib. xxxv. sect. 36. Athenæus,
lib. xii. p. 543.

198. Geschichte der Kunst, part ii. p. 353. Plinius, lib. xxxvi. sect. 4.

199. See Appendix, note 57.

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literature.”—Buffalo Courier.

“Let no intelligent reader be deterred from its diligent perusal by

the learned name which introduces the interesting book now offered
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word Sanskrit has an abstruse sound to unenlightened ears, but
there is nothing abstruse in the subject as here presented, and
nothing difficult to be understood by persons of ordinary culture....
The writer’s treatment of the subject is much to be commended. It is
bright, fresh, earnest, and strong. She arouses the reader’s attention
from the beginning, charms his imagination by choice extracts from
the literary treasures of past ages, pleases his taste by drawing
parallelisms between the myths of the past and the fables of the
present, convinces him that one literature unites different nations
and different centuries, and that each nation is a link in the great
chain of development of the human mind. We earnestly commend
this work to all who would understand the unity and continuity of
literature. It is full of general information and instruction, the style is
earnest and easy, the enthusiasm sympathetic, and the presentation
specially thought-stirring and satisfactory.”—Providence Journal.
 TRANSCRIBER’S NOTES
1. Silently corrected palpable typographical errors;
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