Different types of response to foreign
antigens by leech leukocytes
M. de Eguileor,
1
A. Grimaldi,
1
G. Tettamanti,
1
R. Valvassori,
1
E. L. Cooper,
2
G. Lanzavecchia
1
Abstract. We used morphological and immunocytochemical approaches to characterize and to show the
behavior of cells involved in leech inflammatory responses. Leeches were injected with bacterial lipopolysaccha-
ride, fluoresceinated yeasts, sulfate spheres and ciliates (Protozoa). Shortly after injection, migrating cells
appeared in the area of injection. The response of the cells occurred in relation to the injected micro or macro anti-
gens. Each injection first provoked a migration of cells towards the non-self material. Afterwards, different
responses (degranulation, phagocytosis, encapsulation, melanization) occurred. The migrating cells involved in
these series of processes have a similar behavior and are characterized by CD markers of macrophages, NK
cells and granulocytes, which are typical of many invertebrates and vertebrates. © 2000 Harcourt Publishers Ltd
Keywords: leeches, LPS, phagocytosis, degranulation, encapsulation, melanization
Introduction
Animal immune systems can recognize foreign antigens and
can respond with a wide repertoire of reactions. One
response is phagocytosis, which is defined as the capacity of
cells to engulf foreign material. This non-specific event,
linked to specific immune activity, has the prime function of
freeing organisms from unwanted, potentially pathogenic
agents (Cooper, 1981; Bilej, 1994; Porchet-Henneré, 1990;
Cooper et al., 1992; Dales & Kalaç, 1992; Porchet-Henneré
& Vernet, 1992; Porchet-Henneré et al., 1992; Cooper et al.,
1996; Blanco et al., 1997; Ottaviani & Franceschi, 1997).
Recently, phagocytosis has been more clearly defined and
associated with ‘an essential component of the innate,
natural, non-specific, non-anticipatory, non-clonal immune
system, largely confined to invertebrates but essential for
interaction with the more advanced and presumably less
ancient adaptive, induced, specific, anticipatory and clonal
immune system of all vertebrates (Stein et al., 1977; Cooper
et al., 1996; Fearon & Locksley, 1996; Hughes & Yeager,
1997; Medzhitov & Janeway, 1997). The issue of ancient
immune systems in invertebrates is indisputable, but the less
ancient is controversial, largely due to a dearth of studies
and the failure of certain studies to address the hallmarks of
specificity and memory.
Another type of response against very large non-self
material is encapsulation. The event occurs when the
foreign antigen is too cumbersome to phagocytose, and it is
found in all invertebrates from the most primitive to the
most evoluted (Parrinello & Rindone, 1981; Ratcliffe et al.,
1985; Gotz & Boman, 1986; Porchet-Henneré, 1990;
Soderhall et al., 1996; De Leo et al., 1997). In many inverte-
brates like sipunculids, a closely related group to annelids
(Blanco et al., 1997), the migrating cells involved in
defence processes have a similar behavior and show CD
markers of macrophages of vertebrates.
Despite an abundance of studies on phagocytosis, encap-
sulation, melanization in invertebrates, and CD markers,
there is little information on Hirudinea (Mann, 1962;
Sawyer, 1986).
We consequently have begun to analyse the inflamma-
tory and immune activity of leeches and present herein
results that characterize the complex responses to living and
non-living foreign bodies.
1
DBSF, University of Insubria, 21100 Varese, Italy
2
Laboratory of
Comparative Immunology, Department of Neurobiology, UCLA School of
Medicine, Los Angeles, CA 90095–1763, USA
Received 11 January 1999
Accepted 12 November 1999
Correspondence to: Magda de Eguileor, DBSF, Università dell’Insubria, Via
Dunant 3, 21100 Varese, Italy. Tel.: +39 332 421310; Fax: +39 332 421330;
E-mail: magda@mailserver.unimi.it
40
Tissue & Cell
Tissue & Cell, 2000 32 (1) 40–48
© 2000 Harcourt Publishers Ltd
DOI: 10.1054/tice.1999.0085, available online at http://www.idealibrary.com