Phylogenetic development of adaptive immunity`
Phylogenetic development of adaptive immunity'
BEN W. PAPERMASTER,2 RICHARD M. CONDIE,3
JOANNE K. FINSTAD,4 ROBERT A. GOOD,5
AND Al'l"
E. GABRIELSE 4
Pediatric Research Laboratories of the Variety Club Heart Hospital,
University of Minnesota, Minneapolis, Minnesota
IMMUNITY,
defined as the cellular changes
resulting in the capacity for immunologic memory, is
an attribute only of the higher vertebrates, and its
phylogenetic development apparently
parallels the
evolution of the thymus and probably also of the lymphoid cells. The cellular changes of adaptive immunity
are of extraordinary specificity, induced by very minor
antigenic differences, and include both cellular proliferation and specific protein synthesis. Their most
characteristic expression is immunologic memory: the
secondary immune response, the second-set reaction to
homografts, and the various forms of immediate and
delayed hypersensitivity.
ADAPTIVE
ADAPTIVE
IMMUNITY
IN INVERTEBRATES
Although invertebrates are prey to many of the same
microorganisms as vertebrates, they do not meet these
threats with adaptive immunity in this sense. Cellular
mechanisms apparently play a major role; in fact,
Metchnikoff's classical description of phagocytosis, in
1884, was based on his studies in Daphnia, a crustacean
('23)' Many studies of cellular immunity in the invertebrates followed; Cantacuzene (7) reviewed many of
the early studies in 19'23. In the 1930'S Cameron (5,6),
studying caterpillars and earthworms, described the
response of these organisms to bacteria and foreign
matter: phagocytosis, a proliferation of coelomic cells,
and sometimes a walling off of the foreign substance by
these coelomic cells into a cyst.
Humoral bactericidal substances are characteristic
of invertebrates, and these apparently increase in amount
l Aided
by grants from the National Foundation, the Public
Health Service, the Minnesota Division of the American Cancer
Society, American Heart Association, and the Minnesota Heart
Association.
2 Present
address: Dept. of Genetics, Stanford University
Medical Center, Palo Alto, Cal.
3 Research
Associate, Clinical Research Center, University
of Minnesota, National Institutes of Health, Grant H-6314.
4 Research
Fellow, Dept. of Pediatrics,
Grant HTS-5462,
National Institutes of Health.
5 American
Legion Memorial Heart Research Professor of
Pediatrics.
when the animal is challenged with bacteria; however,
the response does not seem to be specific to the organism
injected. Agglutinins have also been reported in some
forms, but again these are nonspecific.
Invertebrates apparently do not have homograft
immunity. Successful homotransplantation
in many
different invertebrate species has a long history, reviewed by Loeb ('21) and Favour (I I). In certain
larvae and worms ('26) organs have been transplanted
successfully between genera and even families, and
generally, the failure of heterografts in such animals
has been attributed to nonimmunologic factors. Recent
studies by Cushing (9) suggest that the absence of
homograft immunity is characteristic of higher invertebrates as well.
IMMUNITY
IN
LOWER
VERTEBRATES
Comparative immunology in the lower poikilothermic
vertebrates was first approached by Metchnikoff in the
late r qth century ('2'2), and later by other investigators
in Europe and the United States. Temperature was
shown to be an important variable in the immunologic
responsiveness of frogs as early as 1897 (3'2), and more
complete studies on the temperature dependence of
immunity in fishes were reported by Cushing in 194'2
(8).
Generally, the teleost fishes, amphibia and reptilia
were shown to have the basic forms of immunologic
responsiveness found in the mammal. Immunologic
memory, which we consider the sine qua non of adaptive
immunity, was clearly demonstrated in responses to
bacterial, particulate, and protein antigens, as well as
in the vigorous second-set response to homografts
(10, 13, 19, J. G. Thorbecke, personal communication,
R. A. Good, unpublished studies).
At the time of our original studies on immunity in
the lower vertebrates, we were not aware of studies of
adaptive immunity in the cyclostomes. Our attention
was focused on two of the lowest contemporary vertebrate
forms, the hagfish (specifically the California hagfish,
Eptatretus stoutii) and the lamprey (Petromyzon marinus).
On the basis of anatomic and biochemical characteris-
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