Abstract
Studies of crab egg hatching and larval release behavior in the crab,Rhithropanopeus harrisii, generated a model describing the process. In the model, carboxyl terminal arginine peptides serve as pheromones that synchronize larval release. In response to the peptides, the female performs Stereotypic larval release behavior and casts larvae into the water column. The peptides originate from trypsin-like enzymatic activity as part of the egghatching process. Hatching can be simulated experimentally by incubating ovigerous crabs in either bovine or porcine trypsin. The female performs the larval release behavior. Eggs detach from the female, and immobile larvae hatch prematurely. Preincubation of trypsin with trypsin inhibitors eliminates these effects. Approximately nanomolar concentrations of five different polypeptide trypsin inhibitors evoke the female's larval release behavior. Because both peptides and trypsin inhibitors evoke larval release behavior and because trypsin inhibitors bind to both the peptide receptor and the enzyme with high affinity, the receptor binding site and trypsin catalytic site must be very similar. A relationship between the binding site of a peptide receptor and the catalytic site of trypsin is postulated. The difference may be substitution by a basic amino acid for the catalytic site serine. Molecular graphics modeling indicates that all necessary conditions for receptor binding can be met by substitution with lysine for the active site serine in the trypsin catalytic site. This substitution eliminates catalytic activity, maintains the binding affinity for trypsin inhibitors, and increases binding strength for peptides.
Similar content being viewed by others
References
Bishop, P.D., Makus, D.J., Pearce, G., andRyan, C.A. 1981. Protease inhibitor-inducing factor activity in tomato leaves resides in oligosaccharides enzymatically released from cell walls.Proc. Natl. Acad. Sci. U.S.A. 78:3536–3540.
Brodrick, J.W., Largman, C., Hsiang, M.W., Johnson, J.H., andGeokas, M.C. 1978. Structural basis for the specific activation of human cationic trypsinogen by human enteropeptidase.J. Biol. Chem. 253:2737–2742.
Castellino, F.J. 1979. A unique enzyme-protein substrate modifier reaction: Plasmin/streptokinase interaction.Trends Biochem. Sci. 4:1–5.
Chester-Jones, I., Ingleton, P.M., andPhillips, J.G. (eds.). 1987. Fundamentals of Comparative Vertebrate Endocrinology. Plenum Press, New York. 666 pp.
Davie, E.W., andFujikawa, K. 1975. Basic mechanisms in blood coagulation.Annu. Rev. Biochem. 44:799–829.
Forward, R.B., Jr. 1987. Larval release rhythms of decapod crustaceans: An overview.Bull. Mar. Sci. 41:165–176.
Forward, R.B., Jr., andLohmann, K.J. 1983. Control of egg hatching in the crabRhithropanopeus harrisii (Gould).Biol. Bull. 165:154–166.
Forward, R.B., Jr., Lohmann, K., andCronin, T.W. 1982. Rhythms in larval release by an estuarine crab (Rhithropanopeus harrisii).Biol. Bull. 163:287–300.
Forward, R.B., Jr., Rittschof, D., andDevries, M. 1987. Peptide pheromones synchronize crustacean egg hatching and larval release.Chem. Senses 12:491–498.
Hruby, V.J., andRich, D.H. 1983. Peptides, structure and function: Proceedings of the eighth American peptide symposium. Pierce Chemical Co., Rockford, Illinois. 927 pp.
Jackson, K.W., andTang, J. 1982. Complete amino acid sequence of streptokinase and its homology with serine proteases.Biochemistry 21:6620–6625.
Kassell, B. 1970. Naturally occurring inhibitors of proteolytic enzymes.Methods Enzymol. 19:839–906.
Lakowski, M., JR., andKuto, I. 1980. Protein inhibitors of proteinases.Annu. Rev. Biochem. 49:593–626.
Magnusson, S., Scottrup-Jensen, L., Pedersen, T.E., Dudek-Wojciecheowska, D., andClaeys, H. 1976. Homologous “kringle” structures common to plasminogen and prothrombin. Substrate specificity of enzymes activating prothrombin and plasminogen, pp. 203–238,in D.W. Ribbons and K. Brew (eds.). Proteolysis and Physiological Regulation. Academic Press, New York.
Marous, S., Baratti, J., andDesnuelle, P. 1971. Purification and specificity of porcine enterokinase.J. Biol. Chem. 246:5031–5039.
Muller-Esterl, W., andFritz, H. 1981. Sperm acrosin.Methods Enzymol. 80(C):621–632.
Neurath, H. 1984. Evolution of proteolytic enzymes.Science 224:350–357.
Norman, A.W., andLitwack, G. 1987. Hormones. Academic Press, San Diego, CA. 805 pp.
Reid, K.B.M., andPorter, R.R. 1981. The proteolytic activation systems of complement.Annu. Rev. Biochem. 50:433–464.
Rittschof, D., Forward, R.B., Jr. andMott, D.D. 1985. Larval release in the crabRhithropanopeus harrisii (Gould): Chemical cues from hatching eggs.Chem. Senses 10:567–577.
Rittschof, D.,Forward, R.B., Jr.,Simons, D.A.,Reddy, P.A., andErickson, B.W. 1989. Peptide analogues of the mud crab pumping pheromone: Structure-function studies.Chem. Senses In press.
Sottrup-Jensen, L., Claeys, H., Zajdel, M., Pedersen, T.E., andMagnusson, S. 1978. The primary structure of human plasminogen: Isolation of two lysine-binding fragments and one “mini-” plasminogen (M.W., 38,000) by elastase-catalyzed-specific limited proteolysis, pp. 191–209,in J.F. Davidson et al. (eds.). Progress in Chemical Fibrinolysis and Thrombosis. Raven Press, New York.
Unson, C.G., Erickson, B.W., andHugli, T.E. 1984. Active site of C3a anaphylatoxin: Contributions of the lipophilic and orienting residues.Biochemistry 23:585–589.
Vogel, R., Trautschold, I., andWerle, E. 1968. Natural Proteinase Inhibitors. Academic Press, New York. 159 pp.
Walpole, R.E. 1974. Introduction of Statistics. Macmillan, New York. 340 pp.
Woodbury, R.G., andNeurath, H. 1980. Structure specificity and localization of the serine proteases of connective tissue.FEBS Lett. 114:189–196.
Young, C.L., Barker, W.C., Tomaselli, C.M., andDayhoff, M.O. 1978. Serine proteases, pp. 73–93,in M.O. Dayhoff (ed.). Atlas of Protein Sequence and Structure. Vol. 5, Suppl. 3. National Biomedical Research Foundation, Washington, D.C.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rittschof, D., Forward, R.B. & Erickson, B.W. Larval release in brachyuran crustaceans Functional similarity of peptide pheromone receptor and catalytic site of trypsin. J Chem Ecol 16, 1359–1370 (1990). https://doi.org/10.1007/BF01021032
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01021032