Constitutive, stable intercellular adhesion is one of the distinguishing properties of metazoans, of which the sponges (Phylum Porifera) are the most primitive representatives. In sponges, intercellular adhesion is mediated by the large proteoglycan-like cell agglutinating molecule ‘aggregation factor’, which binds to cell surfaces via an oligosaccharide moiety. Previous studies indicated that this aggregation factor binds to two proteins associated with the surface of sponge cells. One of these, a 68 kDa peripheral membrane protein, was isolated by affinity chromatography on aggregation factor conjugated to Sepharose. This monomeric 68 kDa glycoprotein plays a key role in sponge cell adhesion since it potently inhibits the binding of aggregation factor to cell surfaces and completely prevents aggregation factor-mediated cell adhesion. The 68 kDa aggregation factor ligand binds with high affinity to both aggregation factor (KD = 2 × 10(−9) M) and cell surfaces (KD = 6 × 10(−8) M) providing evidence that it serves as an intramolecular bridge between the aggregation factor molecule and a cell surface receptor. Therefore, this early metazoan protein may represent one of the earliest extracellular matrix adhesion proteins to have arisen in the course of metazoan evolution.

REFERENCES

Albelda
S.
,
Buck
C.
(
1990
).
Integrins and other cell adhesion molecules.
FASEB J
4
,
2868
2880
Albelda
S.
,
Mette
B. A.
,
Elder
D. E.
,
Stewart
R.
,
Damjanovich
L.
,
Herlyn
M.
,
Buck
C.
(
1990
).
Integrin distribution in malignant melanoma: Association of the beta 3 subunit with tumor progression.
Cancer Res
50
,
6757
6764
Adelson
D. L.
,
Alliegro
M. C.
,
McClay
D. R.
(
1992
).
On the ultrastructure of hyalin, a cell adhesion protein of the sea urchin embryo extracellular matrix.
J. Cell Biol
116
,
1283
1289
Barondes
S. H.
,
Haywood-Reid
P. L.
,
Cooper
D. N.
(
1985
).
Discoidin I, an endogenous lectin, is externalized from Dictyostelium discoideum in multilamellar bodies.
J. Cell Biol
100
,
1825
33
Boucat
J.-C.
,
Darribiere
T.
,
Poole
T. J.
,
Aoyama
H. M.
,
Yamada
K.
,
Theiry
J. P.
(
1984
).
Biologically active synthetic peptides as probes of embryonic development: A competitive inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest cell migration in avian embryos.
J. Cell Biol
99
,
1822
1829
Bronner-Fraser
M.
,
Artinger
M.
,
Muschler
J.
,
Horwitz
A. F.
(
1992
).
Developmentally regulated expression of alpha 6 integrin in avian embryos.
Development
115
,
197
211
Brooks
P. C.
,
Montgomery
A. M. P.
,
Rosenfeld
M.
,
Reisfeld
R. A.
,
Hu
T.
,
Klier
G.
,
Cheresh
D. A.
(
1994
).
Integrinv antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels.
Cell
79
,
1157
1164
Brooks
P. C.
,
Clark
R. F.
,
Cheresh
D. A.
(
1994
).
Requirement of vascular integrinv for angiogenesis.
Science
264
,
569
571
Edelman
G. M.
(
1988
).
Morphoregulatory molecules.
Biochemistry
27
,
3533
43
Felding-Habermann
B.
,
Mueller
B.
,
Romerdahl
C.
,
Cheresh
D. A.
(
1992
).
Involvement of integrinv gene expression in human melanoma tumorigenicity.
J. Clin. Invest
89
,
2018
2022
Gabius
H. J.
,
Springer
W. R.
,
Barondes
S. H.
(
1985
).
Receptor for the cell binding site of discoidin I.
Cell
42
,
449
56
Giancotti
F. G.
,
Ruoslahti
E.
(
1990
).
Elevated levels of thereceptor suppresses the transformed phenotype of Chinese hamster ovary cells.
Cell
60
,
848
859
Hardin
J.
,
McClay
D. R.
(
1990
).
Target recognition by the archenteron during sea urchin gastrulation.
Dev. Biol
142
,
86
102
Hemler
M. E.
(
1990
).
VLA proteins in the integrin family: Structures, functions, and their role on leukocytes.
Annu. Rev. Immunol
8
,
365
400
Henkart
P.
,
Humphreys
S.
,
Humphreys
T.
(
1973
).
Characterization of sponge aggregation factor: a unique proteoglycan complex.
Biochemistry
12
,
3045
3050
Humphreys
T.
(
1963
).
Chemical and in vitro reconstitution of sponge cell adhesion. I. Isolation and functional demonstration of the components involved.
Dev. Biol
8
,
27
47
Hynes
R. O.
(
1992
).
Integrins: versatility, modulation and signalling in cell adhesion.
Cell
69
,
11
25
Hynes
R. O.
,
Lander
A. D.
(
1992
).
Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons.
Cell
68
,
303
322
Jumblatt
J.
,
Schlup
V.
,
Burger
M. M.
(
1980
).
Cell-cell recognition: Specific binding of Microciona sponge aggregation factor to homotypic cells and the role of calcium ions.
Biochemistry
12
,
3045
3050
Kemler
R.
,
Ozawa
M.
,
Ringwald
M.
(
1989
).
Calcium-dependent cell adhesion molecules.
Curr. Opin. Cell Biol
1
,
892
897
Kintner
C.
(
1992
).
Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain.
Cell
69
,
225
236
Laemmli
U. K.
(
1970
).
Cleavage of structural proteins during assembly of the head of bacteriophage T4.
Nature
227
,
680
685
Lallier
T.
,
Bronner-Fraser
M.
(
1993
).
Inhibition of neural crest cell attachment by integrin antisense oligonucleotides.
Science
259
,
692
695
Lee
G.
,
Hynes
R. O.
,
Kirschner
M.
(
1984
).
Temporal and spatial regulation of fibronectin in early Xenopus development.
Cell
36
,
729
740
McClay
D. R.
(
1991
).
Gastrulation.
Curr. Opin. Genet. Dev
1
,
191
5
Meredith
J. E.
,
Fazeli
B.
,
Schwartz
M. A.
(
1993
).
The extracellular matrix as a cell survival factor.
Mol. Biol. Cell
4
,
953
961
Misevic
G.
,
Jumblatt
J.
,
Burger
M. M.
(
1982
).
Cell binding fragments from a sponge proteoglycan-like aggregation factor.
J. Biol. Chem
257
,
6931
6936
Misevic
G.
,
Burger
M. M.
(
1986
).
Reconstitution of high cell binding affinity of a marine sponge aggregation factor by cross-linking of small low affinity fragments into a large polyvalent polymer.
J. Biol. Chem
261
,
2853
2859
Misevic
G.
,
Burger
M. M.
(
1990
).
The species-specific cell-binding site of the aggregation factor from the sponge Microciona prolifera is a highly repetitive novel glycan containing glucuronic acid, fucose and mannose.
J. Biol. Chem
265
,
20577
20584
Misevic
G.
,
Burger
M. M.
(
1993
).
Carbohydrate-carbohydrate interactions of a novel acidic glycan can mediate sponge cell adhesion.
J. Biol. Chem
268
,
4922
4929
Muller
W. E. G.
,
Conrad
G.
,
Pondeljack
V.
,
Steffan
R.
,
Zahn
R.
(
1982
).
Electron microscopical characterization of sponge aggregation factors.
Tissue & Cell
14
,
219
233
Ruoslahti
E.
(
1991
).
Integrins.
J. Clin. Invest
87
,
1
5
Springer
T. A.
(
1990
).
Adhesion receptors of the immune system.
Nature
346
,
425
434
Springer
W. R. D.
,
Cooper
W. W.
,
Barondes
S.
(
1984
).
Discoidin I is implicated in cell-substratum attachment and ordered cell migration of Dictyostelium discoideum and resembles fibronectin.
Cell
39
,
557
564
Takeichi
M.
(
1991
).
Cadherin cell adhesion receptors as a morphogenetic regulator.
Science
251
,
1451
1455
Towbin
H.
,
Staehlin
T.
,
Gordan
J.
(
1979
).
Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
Proc. Nat. Acad. Sci. USA
76
,
4350
4354
Varner
J.
,
Burger
M. M.
,
Kaufman
J.
(
1988
).
Two cell surface proteins bind the sponge Microciona prolifera aggregation factor.
J. Biol. Chem
263
,
8498
8508
Varner
J. A.
,
Emerson
D. A.
,
Juliano
R. L.
(
1995
).
Integrinnegatively regulates cell growth: Reversal by attachment to fibronectin
.
Mol. Biol. Cell
6
Wilson
H. V.
(
1907
).
On some phenomena of coalescence and regeneration in sponges.
J. Exp. Zool
5
,
245
–.
Zetter
B. R.
(
1990
).
The cellular basis of site-specific tumor metastasis.
New. Engl. J. Med
322
,
605
612
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