Kinetic and structural properties of disulfide engineered phospholipase A2: Insight into the role of disulfide bonding patterns

Biochemistry

Volumn 44, Issue 9, 2005, Pages 3369-3379

  Yu, Bao Zhu ^a   Pan, Ying H ^a   Janssen, Marcel J W ^b,c   Bahnson, Brian J ^a   Jain, Mahendra K ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BONDING; CALCIUM; CATALYSIS; LIVING SYSTEMS STUDIES; MUTAGENESIS; PARAMETER ESTIMATION; PHOSPHOLIPIDS;

DISULFIDE ARCHITECTURE; INTERFACIAL KINETICS; MUTANTS; STRUCTURAL CHANGES;

ENZYME KINETICS;

DISULFIDE; PHOSPHOLIPASE A2;

ARTICLE; CALCIUM BINDING; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME KINETICS; ENZYME RELEASE; ENZYME STRUCTURE; HUMAN; MATHEMATICAL ANALYSIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; SPECTROSCOPY; SWINE;

ALKYLATION; ANIMALS; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DIPHENYLHEXATRIENE; DISULFIDES; ENZYME INHIBITORS; GLYCEROPHOSPHATES; HISTIDINE; HUMANS; HYDROLYSIS; ISOENZYMES; KINETICS; LIGANDS; MODELS, CHEMICAL; PHOSPHOLIPASES A; PROTEIN ENGINEERING; SODIUM DODECYL SULFATE; SPECTROMETRY, FLUORESCENCE; SWINE;

EID: 14644413488     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0482147     Document Type: Article

References (47)

1. Berg, O. G., and Jain, M. K. (2002) Interfacial Enzyme Kinetics, Wiley, London.
2. Berg, O. G., Gelb, M. H., Tsai, M. D., and Jain, M. K. (2001) Interfacial enzymology: the secreted phospholipase A2-paradigm, Chem. Rev. 101, 2613-54.
3. Valentin, E., and Lambeau, G. (2000) Increasing molecular diversity of secreted phospholipases A(2) and their receptors and binding proteins, Biochim. Biophys. Acta 1488, 59-70.
4. Six, D. A., and Dennis, E. A. (2000) The expanding superfamily of phospholipase A(2) enzymes: classification and characterization, Biochim. Biophys. Acta 1488, 1-19.
5. Singer, A. G., Ghomashchi, F., Le Calvez, C., Bollinger, J., Bezzine, S., Rouault, M., Sadilek, M., Nguyen, E., Lazdunski, M., Lambeau, G., and Gelb, M. H. (2002) Interfacial kinetic and binding properties of the complete set of human and mouse groups I, II, V, X, and XII secreted phospholipases A2, J. Biol. Chem. 277, 48535-49.
6. Janssen, M. J., Verheij, H. M., Slotboom, A. J., and Egmond, M. R. (1999) Engineering the disulphide bond patterns of secretory phospholipases A2 into porcine pancreatic isozyme. The effects on folding, stability and enzymatic properties, Eur. J. Biochem. 261, 197-207.
7. Pan, Y. H., Epstein, T. M., Jain, M. K., and Bahnson, B. J. (2001) Five coplanar anion binding sites on one face of phospholipase A2: relationship to interface binding, Biochemistry 40, 609-17.
8. Pan, Y. H., Yu, B. Z., Singer, A. G., Ghomashchi, F., Lambeau, G., Gelb, M. H., Jain, M. K., and Bahnson, B. J. (2002) Crystal structure of human group X secreted phospholipase A2. Electrostatically neutral interfacial surface targets zwitterionic membranes, J. Biol. Chem. 277, 29086-93.
9. Nieuwenhuizn, W., Steenbergh, P., and de Haas, G. (1973) The isolation and properties of two prephospholipase A2 from porcine pancreas, Eur. J. Biochem. 40, 1-7.
10. Jain, M. K., Rogers, J., Jahagirdar, D. V., Marecek, J. F., and Ramirez, F. (1986) Kinetics of interfacial catalysis by phospholipase A2 in intravesicle scooting mode, and heterofusion of anionic and zwitterionic vesicles, Biochim. Biophys. Acta 860, 435-47.
11. Berg, O. G., Yu, B. Z., Rogers, J., and Jain, M. K. (1991) Interfacial catalysis by phospholipase A2: determination of the interfacial kinetic rate constants, Biochemistry 30, 7283-97.
12. Berg, O. G., Rogers, J., Yu, B. Z., Yao, J., Romsted, L. S., and Jain, M. K. (1997) Thermodynamic and kinetic basis of interfacial activation: resolution of binding and allosteric effects on pancreatic phospholipase A2 at zwitterionic interfaces, Biochemistry 36, 14512-30.
13. Berg, O. G., Yu, B. Z., Chang, C., Koehler, K. A., and Jain, M. K. (2004) Cooperative binding of monodisperse anionic amphiphiles to the i-face: Phospholipase A2-paradigm for interfacial binding, Biochemistry 43, 7999-8013.
14. Jancarik, J., and Kim, S. H. (1991) Sparse matrix sampling: a screening method for crystallization of proteins, J. Appl. Crystallogr. 24, 409-11.
15. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-26.
16. Navaza, J. (2001) Implementation of molecular replacement in AMoRe, Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 1367-72.
17. Brunger, A. T., Adams, P. D., Clore, G. M., Delano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, N., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR systems (CNS): A new software system for macromolecular structure determination, Acta Crystallogr. D54, 905-21.
18. Sack, J. S., and Quiocho, F. A. (1997) CHAIN: A crystallographic modeling program, Methods Enzymol. 277, 158-73.
19. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr., Sect. A 47, 110-9.
20. Brunger, A. T. (1992) The free R value: A novel statistical quantity for assessing the accuracy of crystal structures, Nature 355, 472-4.
21. Cajal, Y., Rogers, J., Berg, O. G., and Jain, M. K. (1996) Intermembrane molecular contacts by polymyxin B mediate exchange of phospholipids, Biochemistry 35, 299-308.
22. Jain, M. K., Rogers, J., Berg, O., and Gelb, M. H. (1991) Interfacial catalysis by phospholipase A2: activation by substrate replenishment, Biochemistry 30, 7340-8.
23. Cajal, Y., Berg, O. G., and Jain, M. K. (1995) Direct vesicle-vesicle exchange of phospholipids mediated by polymyxin B, Biochem. Biophys. Res. Commun. 210, 746-52.
24. Cajal, Y., Rogers, J., Berg, O. G., and Jain, M. K. (1996) Intermembrane molecular contacts by polymyxin B mediate exchange of phospholipids, Biochemistry 35, 299-308.
25. Rogers, J., Yu, B. Z., Tsai, M. D., Berg, O. G., and Jain, M. K. (1998) Cationic residues 53 and 56 control the anion-induced interfacial k*cat activation of pancreatic phospholipase A2, Biochemistry 37, 9549-56.
26. Yu, B. Z., Poi, M. J., Ramagopal, U. A., Jain, R., Ramakumar, S., Berg, O. G., Tsai, M. D., Sekar, K., and Jain, M. K. (2000) Structural Basis of the Anionic Interface Preference and Activation of Pancreatic Phospholipase A(2), Biochemistry 39, 12312-23.
27. Beers, S. A., Buckland, A. G., Koduri, R. S., Cho, W., Gelb, M. H., and Wilton, D. C. (2002) The antibacterial properties of secreted phospholipases A2: a major physiological role for the group IIA enzyme that depends on the very high pI of the enzyme to allow penetration of the bacterial cell wall, J. Biol. Chem. 277, 1788-93.
28. 2, Biochemistry 42, 7326-38.
29. Jain, M. K., Tao, W. J., Rogers, J., Arenson, C., Eibl, H., and Yu, B. Z. (1991) Active-site-directed specific competitive inhibitors of phospholipase A2: novel transition-state analogues, Biochemistry 30, 10256-68.
30. Yu, B. Z., Berg, O. G., and Jain, M. K. (1999) Hydrolysis of monodisperse phosphatidylcholines by phospholipase A2 occurs on vessel walls and air bubbles, Biochemistry 38, 10449-56.
31. Berg, O. G., Yu, B. Z., Apitz-Castro, R. J., and Jain, M. K. (2004) Phosphatidylinositol-specific phospholipase C forms different complexes with monodisperse and micellar phosphatidylcholine, Biochemistry 43, 2080-90.
32. Jain, M. K., Rogers, J., Hendrickson, H. S., and Berg, O. G. (1993) The chemical step is not rate-limiting during the hydrolysis by phospholipase A2 of mixed micelles of phospholipid and detergent, Biochemistry 32, 8360-7.
33. Jain, M. K., Ranadive, G., Yu, B. Z., and Verheij, H. M. (1991) Interfacial catalysis by phospholipase A2: monomeric enzyme is fully catalytically active at the bilayer interface, Biochemistry 30, 7330-40.
34. Yu, B. Z., Rogers, J., Nicol, G. R., Theopold, K. H., Seshadri, K., Vishweshwara, S., and Jain, M. K. (1998) Catalytic significance of the specificity of divalent cations as KS* and kcat* cofactors for secreted phospholipase A2, Biochemistry 37, 12576-87.
35. 2 from berries of Schnscinius terebinthifolius, Phytochemistry 39, 537-47.
36. Yu, B. Z., Berg, O. G., and Jain, M. K. (1993) The divalent cation is obligatory for the binding of ligands to the catalytic site of secreted phospholipase A2, Biochemistry 32, 6485-92.
37. Yu, B. Z., Ghomashchi, F., Cajal, Y., Annand, R. R., Berg, O. G., Gelb, M. H., and Jain, M. K. (1997) Use of an imperfect neutral diluent and outer vesicle layer scooting mode hydrolysis to analyze the interfacial kinetics, inhibition, and substrate preferences of bee venom phospholipase A2, Biochemistry 36, 3870-81.
38. Yu, B. Z., Apitz-Castro, R., Tsai, M. D., and Jain, M. K. (2003) Interaction of monodisperse anionic amphiphiles with the i-face of secreted phospholipase A2, Biochemistry 42, 6293-301.
39. Steiner, R. A., Rozeboom, H. J., de Vries, A., Kalk, K. H., Murshudov, G. N., Wilson, K. S., and Dijkstra, B. W. (2001) X-ray structure of bovine pancreatic phospholipase A2 at atomic resolution, Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 516-26.
40. Scott, D. L., White, S. P., Browning, J. L., Rosa, J. J., Gelb, M. H., and Sigler, P. B. (1991) Structures of free and inhibited human secretory phospholipase A2 from inflammatory exudate, Science 254, 1007-10.
41. Yu, B. Z., Rogers, J., Ranadive, G., Baker, S., Wilton, D. C., Apitz-Castro, R., and Jain, M. K. (1997) Gossypol modification of Ala-1 of secreted phospholipase A2: a probe for the kinetic effects of sulfate glycoconjugates, Biochemistry 36, 12400-11.
42. Dijkstra, B. W., Kalk, K. H., Hol, W. G., and Drenth, J. (1981) Structure of bovine pancreatic phospholipase A2 at 1.7 Å resolution, J. Mol. Biol. 147, 97-123.
43. Thunnissen, M. M., Ab, E., Kalk, K. H., Drenth, J., Dijkstra, B. W., Kuipers, O. P., Dijkman, R., de Haas, G. H., and Verheij, H. M. (1990) X-ray structure of phospholipase A2 complexed with a substrate-derived inhibitor, Nature 347, 689-91.
44. Scott, D. L., White, S. P., Otwinowski, Z., Yuan, W., Gelb, M. H., and Sigler, P. B. (1990) Interfacial catalysis: the mechanism of phospholipase A2, Science 250, 1541-6.
45. Liu, X., Zhu, H., Huang, B., Rogers, J., Yu, B. Z., Kumar, A., Jain, M. K., Sundaralingam, M., and Tsai, M. D. (1995) Phospholipase A2 engineering. Probing the structural and functional roles of N-terminal residues with site-directed mutagenesis, X-ray, and NMR, Biochemistry 34, 7322-34.
46. Pan, Y. H., Yu, B. Z., Berg, O. G., Jain, M. K., and Bahnson, B. J. (2002) Crystal structure of phospholipase A2 complex with the hydrolysis products of platelet activating factor: equilibrium binding of fatty acid and lysophospholipid-ether at the active site may be mutually exclusive, Biochemistry 41, 14790-800.
47. Zhu, H., Dupureur, C. M., Zhang, X., and Tsai, M. D. (1995) Phospholipase A2 engineering. The roles of disulfide bonds in structure, conformational stability, and catalytic function, Biochemistry 34, 15307-14.