About POPs

    Pyrococcus furiosus is a hyperthermophilic member of the domain Archaea, one of the three major phylogenetic divisions of life. There is a paucity of comparative data on the mechanisms of homologous enzymes from the three domains (Archaea, Bacteria, and Eukarya). Such data have the potential to enhance our understanding of the evolutionary history of proteins and organisms, and will certainly contribute to understanding of enzyme function at high temperatures.
    Comparisons of hyperthermostable enzymes with their counterparts from mesophilic organisms have discovered great similarities in enzyme mechanisms. The beta-glucosidase of P. furiosus has been compared to its homologue from the mesophilic bacterium Agrobacterium faecalis (1). The substrates that are involved in the transition states for these enzymes are extremely similar, indicating that the mechanism is highly conserved. Mechanistic and structural studies of the beta-glucosidase (2) and glutamate dehydrogenase (3, 4) from P. furiosus have demonstrated the similarities between enzyme homologues from organisms with very different temperature optima, and that structural data obtained for mesophilic proteins can be useful for predicting the structure of hyperthermostable proteins. Recently, the gene for the prolyl oligopeptidase of P. furiosus was cloned and overexpressed in E. coli as a functional protease (5). The recombinant prolyl oligopeptidase displayed characteristics identical to those of the enzyme expressed in P. furiosus (5), affording the opportunity to readily obtain sufficient quantities of this protein for kinetic studies.
    The prolyl oligopeptidase from P. furiosus (EC 3.4.21.26, formerly termed prolyl endopeptidase) is a serine protease of unusual specificity, as it cleaves the sequence X-Pro-Y (where X and Y are any amino acid) on the carboxyl side of proline. Although it possesses the catalytic triad composed of serine, histidine, and aspartate that is characteristic of the serine proteases, its primary structure is otherwise unrelated to that of the chymotrypsin, trypsin, or elastase classes of serine proteases (6-8). In fact, the order of the amino acids in the primary structure is different for prolyl oligopeptidase (Ser, Asp, His) than it is for either the chymotrypsin (His, Asp, Ser) or subtilisin (Asp, His, Ser) families (9). Prolyl oligopeptidases (POPs) were first isolated from human tissue (10), and subsequently from the tissues of other mammals (11, 12), fungi (13, 14), bacteria, (15-17) and archaea (5).
    In spite of its wide distribution, little is known about the physiological role(s) of POP in any organism. Nevertheless, the presence of the enzyme in mammalian brain tissue and its ability to cleave proline-containing neuroactive peptides (18, 19) have led to the suggestion that it plays a role in regulation of these peptides.  Evidence is emerging which suggests that POP influences memory in mammals since POP inhibitors have antiamnesiac properties (20).
    As a first step in the detailed investigation of P. furiosus (Pfu) POP, its substrate specificity, pH activity profiles, temperature-dependent activity profile, and influences by anions were studied. In addition, a structural model of Pfu POP was constructed based on the folding patterns from the POP crystal structure from Sus scrufa (pig) (21), in which the two enzymes share 32% identity and 57% similarity at the amino acid level (7). The mammalian (porcine) and archaeal POPs are compared on the basis of the kinetic studies and molecular model.

Kinetic and Mechanistic Studies of Prolyl Oligopeptidase from the Hyperthermophile  Pyrococcus furiosus
Accepted for publication in the Journal of Biological Chemistry 2001 (abstract)
Michael N. Harris1, Jeffry D. Madura3, Li-June Ming*1, Valerie J. Harwood*2
1 Department of Chemistry and Institute for Biomolecular Science, University of South Florida, 4202 East Fowler Avenue, Tampa, FL 33620
2 Department of Biology, University of South Florida, 4202 East Fowler Avenue, Tampa, FL 33620
3 Department of Chemistry and Biochemistry, Duquesne University, 600 Forbes Avenue, Pittsburgh, PA 15282-1530

A Y401--> F401 mutant has been prepared!  Kinetic and thermodynamic studies will follow soon!

References

  1. Bauer, M.W. and Kelly, R.M. (1998) Biochemistry 37, 1710-1718.
  2. Kaper, T., Lebbink, J.H.G., Pouwels, J., Kopp, J., Schulz, G.E., van der Oost, J., and de Vos, W.M. (2000) Biochemistry 39, 4963-4970.
  3. Britton, K.L., Baker, P.J., Borges, K.M., Engel, P.C., Pasquo, A., Rice, D.W., Robb, F.T., Scandurra, R., Stillman, T.J., and Yip, K.S. (1995) Eur. J. Biochem. 29:688-695.
  4. Vetriani, C., Maeder, D., Tolliday, N., Yip, K.S., Stillman, T.J., Britton, K.L., Rice, D.W., Klump, H.H., and Robb, T.T. (1998) Proc. Natl. Acad. Sci. U.S.A. 95:12300-12305.
  5. Harwood, V.J.,  Denson, J.D., Robinson-Bidle, K.A., and Schreier, H.J. (1997) J. Bacteriol.  179, 3613-3618.
  6. Koida, M. and Walter, R. (1976) J. Biol. Chem. 251, 7593-7599.
  7. Robinson, K.A., Bartley, D.A., Robb, F.T., and Schreier, H.J. (1995) Gene 152, 103-106.
  8. Rennex, D., Hemmings, B.A.,Hofsteenge, J., and Stone, S.R. (1991) Biochemistry 30, 2195.
  9. Rawlings, N.D., and  Barrett, A.J. (1994) Meth. Enzymol. 244, 19-61.
  10. Walter, R., Shlank, H., Glass, J.D., Schwartz, I.L., and Kerenyi, T.D. (1971) Science 173, 827-829.
  11. Yoshimoto, T., Nishimura, T., Kita, T., and Tsuru, D. (1983) J. Biochem. 94:1179-1190.
  12. Yoshimoto, T., Simmons, W.H., Kita, T. and Tsuru, D. (1981) J. Biochem. 90, 325-334.
  13. Sattar, A.K.M.A., Yoshimoto, T., Yamamoto, N., and Tsuru, D. (1990) J. Biochem. 107, 256-261.
  14. Yoshimoto, T., Sattar, A.K.M.A., Hirose, W., and Tsuru, D. (1988) J. Biochem. 104, 622-627.
  15. Kantani, A., Yoshimoto, T., Kitazono, A., Kokubo, T., and Tsuru, D. (1993) J. Biochem. 113, 790-796.
  16. Chevallier, S. P., Goeltz, P. T., Banville, D., and Gagnon J.(1992) J. Biol. Chem. 267, 8192-8199.
  17. Szwajcer-Dey, E., Rasmussen, J., Meldal, M., and Breddam, K. (1992) J. Bacteriol. 174, 2454-2459.
  18. Blumberg, S., Teichberg, V.I., Charli, J.L., Hersh, L.B., and McKelvy, J.F. (1980) Brain Res.  192, 477-486.
  19. Hersh, L.B.,and McKelvy, J.F.. (1979) Brain Res. 168, 553-564.
  20. Yoshimoto, T., Kado, K., Matsubara, F., Koriyama, N., Kaneto, H., and Tsuru, D. (1987) J.  Pharmacobio-Dyn 10, 730-735.