Lipoprotein-associated phospholipase A2 interacts with phospholipid vesicles via a surface-disposed hydrophobic α-helix

Biochemistry

Volumn 50, Issue 23, 2011, Pages 5314-5321

  Cao, Jian ^a   Hsu, Yuan Hao ^a   Li, Sheng ^b   Woods, Virgil L ^b   Dennis, Edward A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOVASCULAR EVENT; DIMYRISTOYLPHOSPHATIDYLCHOLINE; HUMAN DISEASE; HUMAN PLASMAS; HYDROGEN-DEUTERIUM EXCHANGE; INFLAMMATORY DISEASE; LIPID MEDIATORS; PEPTIDE AMIDES; PHOSPHOLIPASE A; PHOSPHOLIPID VESICLES; PLASMA LEVELS; PLATELET-ACTIVATING FACTORS;

AMIDES; DEUTERIUM; DISEASES; ENZYMES; HYDROPHOBICITY; LIPOSOMES; MASS SPECTROMETRY; PATHOLOGY;

PHOSPHOLIPIDS;

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; AMIDE; DEUTERIUM; DIMYRISTOYLPHOSPHATIDYLCHOLINE; HYDROGEN; LEUCINE; LIPOSOME; RECOMBINANT ENZYME; TRYPTOPHAN;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; DEUTERIUM EXCHANGE MASS SPECTROMETRY; DEUTERIUM HYDROGEN EXCHANGE; HYDROPHOBICITY; MASS SPECTROMETRY; MOLECULAR MODEL; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; SURFACE PROPERTY;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; CATALYSIS; DEUTERIUM EXCHANGE MEASUREMENT; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; PHOSPHOLIPIDS; PROTEIN STRUCTURE, SECONDARY; SURFACE PROPERTIES;

EID: 79958842003     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101916w     Document Type: Article

References (39)

1. McIntyre, T. M., Prescott, S. M., and Stafforini, D. M. (2009) The emerging roles of PAF acetylhydrolase J. Lipid Res. 50, S255-259
2. Stafforini, D. M., Prescott, S. M., and McIntyre, T. M. (1987) Human plasma platelet-activating factor acetylhydrolase. Purification and properties J. Biol. Chem. 262, 4223-4230 (Pubitemid 17102640)
3. Schaloske, R. H. and Dennis, E. A. (2006) The phospholipase A2 superfamily and its group numbering system Biochim. Biophys. Acta 1761, 1246-1259 (Pubitemid 44755364)
4. Stremler, K. E., Stafforini, D. M., Prescott, S. M., and McIntyre, T. M. (1991) Human plasma platelet-activating factor acetylhydrolase. Oxidatively fragmented phospholipids as substrates J. Biol. Chem. 266, 11095-11103 (Pubitemid 21906916)
5. Min, J. H., Wilder, C., Aoki, J., Arai, H., Inoue, K., Paul, L., and Gelb, M. H. (2001) Platelet-activating factor acetylhydrolases: broad substrate specificity and lipoprotein binding does not modulate the catalytic properties of the plasma enzyme Biochemistry 40, 4539-4549 (Pubitemid 32374642)
6. Stafforini, D. M., Sheller, J. R., Blackwell, T. S., Sapirstein, A., Yull, F. E., McIntyre, T. M., Bonventre, J. V., Prescott, S. M., and Roberts, L. J., 2nd. (2006) Release of free F2-isoprostanes from esterified phospholipids is catalyzed by intracellular and plasma platelet-activating factor acetylhydrolases J. Biol. Chem. 281, 4616-4623 (Pubitemid 43847720)
7. Shimizu, T. (2009) Lipid mediators in health and disease: enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation Annu. Rev. Pharmacol. Toxicol. 49, 123-150
8. Prescott, S. M., Zimmerman, G. A., Stafforini, D. M., and McIntyre, T. M. (2000) Platelet-activating factor and related lipid mediators Annu. Rev. Biochem. 69, 419-445
9. Stafforini, D. M. (2009) Biology of platelet-activating factor acetylhydrolase (PAF-AH, lipoprotein associated phospholipase A2) Cardiovasc. Drugs Ther. 23, 73-83
10. Stafforini, D. M. (2009) Functional Consequences of Mutations and Polymorphisms in the Coding Region of the PAF Acetylhydrolase (PAF-AH) Gene Pharmaceuticals 2, 94-117
11. Casas, J. P., Ninio, E., Panayiotou, A., Palmen, J., Cooper, J. A., Ricketts, S. L., Sofat, R., Nicolaides, A. N., Corsetti, J. P., Fowkes, F. G., Tzoulaki, I., Kumari, M., Brunner, E. J., Kivimaki, M., Marmot, M. G., Hoffmann, M. M., Winkler, K., Marz, W., Ye, S., Stirnadel, H. A., Khaw, K. T., Humphries, S. E., Sandhu, M. S., Hingorani, A. D., and Talmud, P. J. (2010) PLA2G7 Genotype, Lipoprotein-Associated Phospholipase A2 Activity, and Coronary Heart Disease Risk in 10 494 Cases and 15 624 Controls of European Ancestry Circulation 121, 2284-2293
12. Wilensky, R. L. and Macphee, C. H. (2009) Lipoprotein-associated phospholipase A(2) and atherosclerosis Curr. Opin. Lipidol. 20, 415-420
13. Burke, J. E. and Dennis, E. A. (2009) Phospholipase A2 structure/function, mechanism, and signaling J. Lipid Res. 50, S237-242
14. Tjoelker, L. W., Eberhardt, C., Unger, J., Trong, H. L., Zimmerman, G. A., McIntyre, T. M., Stafforini, D. M., Prescott, S. M., and Gray, P. W. (1995) Plasma platelet-activating factor acetylhydrolase is a secreted phospholipase A2 with a catalytic triad J. Biol. Chem. 270, 25481-25487
15. Samanta, U. and Bahnson, B. J. (2008) Crystal structure of human plasma platelet-activating factor acetylhydrolase: structural implication to lipoprotein binding and catalysis J. Biol. Chem. 283, 31617-31624
16. Gelb, M. H., Min, J. H., and Jain, M. K. (2000) Do membrane-bound enzymes access their substrates from the membrane or aqueous phase: interfacial versus non-interfacial enzymes Biochim. Biophys. Acta 1488, 20-27
17. Woods, V. L., Jr. and Hamuro, Y. (2001) High resolution, high-throughput amide deuterium exchange-mass spectrometry (DXMS) determination of protein binding site structure and dynamics: utility in pharmaceutical design J. Cell. Biochem. Suppl. 37, 89-98 (Pubitemid 34135911)
18. Konermann, L., Tong, X., and Pan, Y. (2008) Protein structure and dynamics studied by mass spectrometry: H/D exchange, hydroxyl radical labeling, and related approaches J. Mass Spectrom. 43, 1021-1036
19. Engen, J. R. (2009) Analysis of protein conformation and dynamics by hydrogen/deuterium exchange MS Anal. Chem. 81, 7870-7875
20. Burke, J. E., Hsu, Y. H., Deems, R. A., Li, S., Woods, V. L., Jr., and Dennis, E. A. (2008) A phospholipid substrate molecule residing in the membrane surface mediates opening of the lid region in group IVA cytosolic phospholipase A2 J. Biol. Chem. 283, 31227-31236
21. Burke, J. E., Karbarz, M. J., Deems, R. A., Li, S., Woods, V. L., Jr., and Dennis, E. A. (2008) Interaction of group IA phospholipase A2 with metal ions and phospholipid vesicles probed with deuterium exchange mass spectrometry Biochemistry 47, 6451-6459 (Pubitemid 351874236)
22. Hsu, Y. H., Burke, J. E., Stephens, D. L., Deems, R. A., Li, S., Asmus, K. M., Woods, V. L., Jr., and Dennis, E. A. (2008) Calcium binding rigidifies the C2 domain and the intradomain interaction of GIVA phospholipase A2 as revealed by hydrogen/deuterium exchange mass spectrometry J. Biol. Chem. 283, 9820-9827
23. Burke, J. E., Babakhani, A., Gorfe, A. A., Kokotos, G., Li, S., Woods, V. L., Jr., McCammon, J. A., and Dennis, E. A. (2009) Location of inhibitors bound to group IVA phospholipase A2 determined by molecular dynamics and deuterium exchange mass spectrometry J. Am. Chem. Soc. 131, 8083-8091
24. Hsu, Y. H., Burke, J. E., Li, S., Woods, V. L., Jr., and Dennis, E. A. (2009) Localizing the membrane binding region of Group VIA Ca2+-independent phospholipase A2 using peptide amide hydrogen/deuterium exchange mass spectrometry J. Biol. Chem. 284, 23652-23661
25. Stafforini, D. M., McIntyre, T. M., and Prescott, S. M. (1990) Platelet-activating factor acetylhydrolase from human plasma Methods Enzymol. 187, 344-357 (Pubitemid 20309300)
26. Szoka, F., Jr. and Papahadjopoulos, D. (1980) Comparative properties and methods of preparation of lipid vesicles (liposomes) Annu. Rev. Biophys. Bioeng. 9, 467-508
27. Min, J. H., Jain, M. K., Wilder, C., Paul, L., Apitz-Castro, R., Aspleaf, D. C., and Gelb, M. H. (1999) Membrane-bound plasma platelet activating factor acetylhydrolase acts on substrate in the aqueous phase Biochemistry 38, 12935-12942
28. Zhang, Z. and Smith, D. L. (1993) Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation Protein Sci. 2, 522-531 (Pubitemid 23119303)
29. Bai, Y., Milne, J. S., Mayne, L., and Englander, S. W. (1993) Primary structure effects on peptide group hydrogen exchange Proteins 17, 75-86 (Pubitemid 23261059)
30. Hamuro, Y., Anand, G. S., Kim, J. S., Juliano, C., Stranz, D. D., Taylor, S. S., and Woods, V. L., Jr. (2004) Mapping intersubunit interactions of the regulatory subunit (RIalpha) in the type I holoenzyme of protein kinase A by amide hydrogen/deuterium exchange mass spectrometry (DXMS) J. Mol. Biol. 340, 1185-1196 (Pubitemid 38968710)
31. Tew, D. G., Southan, C., Rice, S. Q., Lawrence, M. P., Li, H., Boyd, H. F., Moores, K., Gloger, I. S., and Macphee, C. H. (1996) Purification, properties, sequencing, and cloning of a lipoprotein-associated, serine-dependent phospholipase involved in the oxidative modification of low-density lipoproteins Arterioscler. Thromb. Vasc. Biol. 16, 591-599
32. Kruse, S., Mao, X. Q., Heinzmann, A., Blattmann, S., Roberts, M. H., Braun, S., Gao, P. S., Forster, J., Kuehr, J., Hopkin, J. M., Shirakawa, T., and Deichmann, K. A. (2000) The Ile198Thr and Ala379Val variants of plasmatic PAF-acetylhydrolase impair catalytical activities and are associated with atopy and asthma Am. J. Hum. Genet. 66, 1522-1530 (Pubitemid 30463071)
33. Gardner, A. A., Reichert, E. C., Topham, M. K., and Stafforini, D. M. (2008) Identification of a domain that mediates association of platelet-activating factor acetylhydrolase with high density lipoprotein J. Biol. Chem. 283, 17099-17106
34. Macphee, C. H., Nelson, J., and Zalewski, A. (2006) Role of lipoprotein-associated phospholipase A2 in atherosclerosis and its potential as a therapeutic target Curr. Opin. Pharmacol. 6, 154-161 (Pubitemid 43362129)
35. Wilensky, R. L., Shi, Y., Mohler, E. R., III, Hamamdzic, D., Burgert, M. E., Li, J., Postle, A., Fenning, R. S., Bollinger, J. G., Hoffman, B. E., Pelchovitz, D. J., Yang, J., Mirabile, R. C., Webb, C. L., Zhang, L., Zhang, P., Gelb, M. H., Walker, M. C., Zalewski, A., and Macphee, C. H. (2008) Inhibition of lipoprotein-associated phospholipase A2 reduces complex coronary atherosclerotic plaque development Nature Med. 14, 1059-1066
36. Pande, A. H. and Tillu, V. A. (2011) Membrane lipid composition differentially modulates the function of human plasma platelet activating factor-acetylhydrolase Biochim. Biophys. Acta. 1118, 46-56
37. Stafforini, D. M., Tjoelker, L. W., McCormick, S. P., Vaitkus, D., McIntyre, T. M., Gray, P. W., Young, S. G., and Prescott, S. M. (1999) Molecular basis of the interaction between plasma platelet-activating factor acetylhydrolase and low density lipoprotein J. Biol. Chem. 274, 7018-7024
38. Winget, J. M., Pan, Y. H., and Bahnson, B. J. (2006) The interfacial binding surface of phospholipase A2s Biochim. Biophys. Acta 1761, 1260-1269 (Pubitemid 44738707)
39. Pan, Y. H. and Bahnson, B. J. (2010) Structure of a premicellar complex of alkyl sulfates with the interfacial binding surfaces of four subunits of phospholipase A2 Biochim. Biophys. Acta 1804, 1443-1448