Comp. Biochem. Physiol. Vol. 105B, No. I, pp. 79-85, 1993 0305-0491/93 $6.00 + 0.00
Printed in Great Britain © 1993 Pergamon Press Ltd
AGGLUTINATION ACTIVITY OF LIMULUS POLYPHEMUS
COAGULOGEN FOLLOWING LIMITED PROTEOLYSIS
CONSUELO L. FORTES-DIAs,* CONCEI~.~O A. S. A. MINETTI, YUAN Ll~q and TEH-YuNG LIU~"
Division of Biochemistry and Biophysics, Center for Biologics Evaluation and Research, Food and Drug
Administration, Bethesda, MD 20892, U.S.A.
(Received 14 October 1992; accepted 18 November 1992)
Abstract--l. A 14 kDa protein with cell agglutination properties has been purified from endotoxin-
activated L. polyphemus amebocyte lysate. Amino terminal sequence analysis indicates that this protein
corresponds to a proteolytically cleaved product (coagulin) of coagulogen.
2. Similar cell agglutination activity can be generated, in vitro, by proteolytic cleavage of the coagulogen
with either trypsin, endogenous protease or an a2M/enzyme complex isolated from amebocytes.
3. Studies with [t2~I]-labeledcoagulogen showed that only coagulin, not the intact coagulogen, binds
to rabbit erythrocytes and formalin-fixed amebocytes.
4. The cell agglutination activity of coagulin towards erythrocytes was not inhibited by various sugars
tested, and was not Ca~ +-dependent.
5. These findings suggest that coagulogen and coagulin are reminiscent of their mammalian counter-
parts, fibrinogen and fibrin, in their clotting and relative adhesive properties.
INTRODUCTION
Coagulogen is a major protein in the hemolymph of
many invertebrates and its role as a substrate in clot
formation has been studied extensively (Nakamura
et al., 1976; Tai et al., 1977; Moseson et al., 1979;
Takagl et al., 1984; Cheng et al., 1986). The complete
amino acid sequences of coagulogens have been
reported for four species of horseshoe crabs (Tai
et al., 1977; Takagi et al., 1984; Cheng et al., 1986;
Miyata et al., 1984a,b; Srimai et al., 1985b). In
Limulus polyphemus, coagulogen is a 175 amino acid
protein containing eight disulfide bonds. During the
last step of the clotting process, the endotoxin-
induced clotting enzyme cleaves coagulogen be-
tween amino acids 18-19 and 46-47 to release to
peptide fragment of 28 amino acids. The 18 amino
acid-peptide at the N-terminus remains linked to the
rest of the molecule through a disulfide bond and the
resultant cleaved product, coagulin, polymedzes to
form an insoluble clot (Miyata et al., 1984b).
Previous studies have shown the presence of a
transglutaminase-catalyzed covalent cross-linking re-
action of polypeptide chains during clot formation
(Chung et al., 1977). However, there is no substantial
evidence to demonstrate that the coagulin generated
Abbreviations--Me2SO: dimethylsulfoxide; PMSF: phenyl-
methylsulfonylfluoride; HPLC: high-performance liquid
chromatography; EDTA: ethylenediaminetetraacetic
acid.
*Visiting Fellow from Fundae~o Ezequiel Dias, Belo Hori-
zonte, MG, Brazil. Supported by Conselho National
de Pesquisa Cientifica e Technologica (CNPq proc.
201124/0).
tTo whom correspondence should be addressed.
following cleavage of coagulogen is a substrate for
such an enzyme. In contrast to the fibrin clot pro-
duced in the mammalian system, the coagulin clot can
be dissociated either by simple mechanical disruption
or dilution (Roth et al., 1989). Among a variety
of biologically active components, a 55 kDa protein
from L. polyphemus amebocytes with cell adhesion-
promoting properties has been isolated and charac-
terized at both the protein and eDNA levels (Liu
et al., 1991). A 24 kDa agglutinin has been isolated,
but not fully characterized from the amebocytes of an
Indian horseshoe crab, Carcinoscorpius rotundicauda
(Srimal et al., 1985a). Agglutination activities have
also bccn observed in the hemolymph of other species
of horseshoe crabs (Marchalonis and Edelman, 1968;
Pistole, 1976; Shishikura and Sekiguchi, 1983). These
iectin-like agglutination activities in invertebrates
bear some similarities to the vertebrate immune sys-
tem and could assume a crucial role in the recognition
of foreign substances, resulting in their ultimate
removal from the circulation (Vasta, 1990).
During the course of our studies of proteins with
agglutinin/lectin activities from L. polyphemus ame-
bocytes, we have observed that the ability of total
amebocyte lysate to promote cell agglutination of
rabbit erythrocytes or human leukocytes increases
upon activation by endotoxin of the clotting cascade.
Several other studies also suggest that agglutination
activities observed either in the amebocytes (Srimal
et al., 1985a) or in the hemolymph (Shishikura and
Sekiguchi, 1983) could arise from activation of the
clotting cascade and further granular extrusion via
exocytosis. In the present study, we investigated the
course of the proteolytic reactions which occur
during activation of the clotting cascade with the
cero IO~/~--F 79