Carbohydrate self-recognition mediates marine sponge cellular adhesion.
Sponges (Porifera), the simplest and earliest multicellular organisms, are thought to have evolved from their unicellular ancestors about 1 billion years ago by developing cell-recognition and adhesion mechanisms to discriminate against "non-self." Consequently, they are used as models for investigating recognition phenomena. Cellular adhesion of marine sponges is an event involving adherence of extracellular proteoglycan-like molecules, otherwise known as aggregation factors (AFs). In a calcium-independent process the AFs adhere to the cell surface, and in a calcium-dependent process they exhibit AF self-association. A mechanism which has been implied but not definitely proven to play a role in the calcium-dependent event is self-recognition of defined carbohydrate epitopes. For the red beard sponge, Microciona prolifera, two carbohydrate epitopes, a sulfated disaccharide and a pyruvylated trisaccharide, have been implicated in cellular adhesion. To investigate this phenomenon a system has been designed, by using surface plasmon resonance detection, to mimic the role of carbohydrates in cellular adhesion of M. prolifera. The results show self-recognition of the sulfated disaccharide to be a major force behind the calcium-dependent event. The interaction is not simply based on electrostatic interactions, as other sulfated carbohydrates analyzed by using this procedure did not self-associate. Furthermore, the interaction is completely eradicated on substitution of Ca(2+) ions by either Mg(2+) or Mn(2+) ions. This physiologically relevant recognition mechanism confirms the existence of true carbohydrate self-recognition, and may have significant implications for the role of carbohydrates in cellular recognition of higher organisms.
Haseley
S R
SR
Bijvoet Center for Biomolecular Research, Department of Bio-Organic Chemistry, Utrecht University, P.O. Box 80.075, NL-3508 TB Utrecht, The Netherlands.
Vermeer
H J
HJ
Kamerling
J P
JP
Vliegenthart
J F
JF
D000818:Animals; D002118:Calcium / Q000378:metabolism; D002236:Carbohydrate Conformation; D002240:Carbohydrate Sequence; D002448:Cell Adhesion; D006001:Glycoconjugates / Q000737:chemistry / Q000378:metabolism*; D016256:Lewis X Antigen / Q000378:metabolism; D008386:Marine Biology; D008969:Molecular Sequence Data; D019906:Nuclear Magnetic Resonance, Biomolecular; D011161:Porifera / Q000166:cytology* / Q000378:metabolism; D016339:Spectrometry, Mass, Fast Atom Bombardment; D020349:Surface Plasmon Resonance
D006001:Glycoconjugates; D016256:Lewis X Antigen; D002118:Calcium