Liquid-liquid immiscibility in model membranes activates secretory phospholipase A2

Biochimica et Biophysica Acta - Biomembranes

Volumn 1778, Issue 1, 2008, Pages 166-174

  Wagner, Kerstin ^a   Desbat, Bernard ^b   Brezesinski, Gerald ^a  

^a MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Cholesterol; Dimyristoylphosphatidylcholine (DMPC); Infrared reflection absorption spectroscopy (IRRAS); Lipolytic enzyme activation; Monolayer structure; Phase separation

Indexed keywords

CHOLESTEROL; DIMYRISTOYLPHOSPHATIDYLCHOLINE; PHOSPHOLIPASE A2; SNAKE VENOM;

ABSORPTION SPECTROSCOPY; ARTICLE; HYDROLYSIS; INFRARED SPECTROSCOPY; LIQUID; POLARIZATION; PRESSURE; PRIORITY JOURNAL;

EID: 38149115365     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2007.09.015     Document Type: Article

References (60)

1. Gambinossi F., Puggelli M., and Gabrielli G. Enzymatic hydrolysis reaction of phospholipids in monolayers. Colloids Surf., B Biointerfaces 23 (2002) 273-281
2. Murakami M., and Kudo I. Phospholipase A(2). J. Biochem. 131 (2002) 285-292
3. Balsinde J., Winstead M.V., and Dennis E.A. Phospholipase A(2) regulation of arachidonic acid mobilization. FEBS Lett. 531 (2002) 2-6
4. Yedgar S., Cohen Y., and Shoseyov D. Control of phospholipase A(2) activities for the treatment of inflammatory conditions. BBA-Mol. Cell. Biol. Lipids 1761 (2006) 1373-1382
5. Nakanishi M., and Rosenberg D.W. Roles of cPLA(2)alpha and arachidonic acid in cancer. BBA-Mol. Cell. Biol. Lipids 1761 (2006) 1335-1343
6. Schaloske R.H., and Dennis E.A. The phospholipase A(2) superfamily and its group numbering system. BBA-Mol. Cell. Biol. Lipids 1761 (2006) 1246-1259
7. Six D.A., and Dennis E.A. The expanding superfamily of phospholipase A(2) enzymes: classification and characterization. BBA-Mol. Cell. Biol. Lipids 1488 (2000) 1-19
8. Brown W.J., Chambers K., and Doody A. Phospholipase A(2) (PLA(2)) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 4 (2003) 214-221
9. Burack W.R., and Biltonen R.L. Lipid bilayer heterogeneities and modulation of phospholipase A(2) activity. Chem. Phys. Lipids 73 (1994) 209-222
10. Mouritsen O.G., Andersen T.L., Halperin A., Hansen P.L., Jakobsen A.F., Jensen U.B., Jensen M.O., Jorgensen K., Kaasgaard T., Leidy C., Simonsen A.C., Peters G.H., and Weiss M. Activation of interfacial enzymes at membrane surfaces. J. Phys.-Condens. Mater. 18 (2006) S1293-S1304
11. Op den Kamp J.A.F., Kauerz M.T., and Van Deenen L.L.M. Action of pancreatic phospholipase A2 on phosphatidyl-choline bilayers in different physical states. Biochim. Biophys. Acta 406 (1975) 169-177
12. Burack W.R., Yuan Q., and Biltonen R.L. Role of lateral phase-separation in the modulation of phospholipase-A2 activity. Biochemistry 32 (1993) 583-589
13. Honger T., Jorgensen K., Biltonen R.L., and Mouritsen O.G. Systematic relationship between phospholipase A(2) activity and dynamic lipid bilayer microheterogeneity. Biochemistry 35 (1996) 9003-9006
14. Hoyrup P., Jorgensen K., and Mouritsen O.G. Phospholipase A(2)-an enzyme that is sensitive to the physics of its substrate. Europhys. Lett. 57 (2002) 464-470
15. Nielsen L.K., Balashev K., Callisen T.H., and Bjornholm T. Influence of product phase separation on phospholipase A(2) hydrolysis of supported phospholipid bilayers studied by force microscopy. Biophys. J. 83 (2002) 2617-2624
16. Hoyrup P., Mouritsen O.G., and Jorgensen K. Phospholipase A(2) activity towards vesicles of DPPC and DMPC-DSPC containing small amounts of SMPC. Biochim. Biophys. Acta, Biomembr. 1515 (2001) 133-143
17. Grainger D.W., Reichert A., Ringsdorf H., and Salesse C. An enzyme caught in action - direct imaging of hydrolytic function and domain formation of phospholipase-A-2 in phosphatidylcholine monolayers. FEBS Lett. 252 (1989) 73-82
18. Grainger D.W., Reichert A., Ringsdorf H., and Salesse C. Hydrolytic action of phospholipase-A2 in monolayers in the phase-transition region - direct observation of enzyme domain formation using fluorescence microscopy. Biochim. Biophys. Acta 1023 (1990) 365-379
19. Gericke A., and Hühnerfuss H. IR reflection-absorption spectroscopy - a versatile tool for studying interfacial enzymatic processes. Chem. Phys. Lipids 74 (1994) 205-210
20. Grandbois M., Desbat B., and Salesse C. Monitoring of phospholipid monolayer hydrolysis by phospholipase A2 by use of polarization-modulated Fourier transform infrared spectroscopy. Biophys. Chem. 88 (2000) 127-135
21. Dahmen-Levison U., Brezesinski G., and Möhwald H. Enzymatic hydrolysis of monolayers: a polarization modulated-infrared reflection absorption spectroscopy study. Prog. Colloid Polym. Sci. 110 (1998) 269-274
22. Grandbois M., Clausen-Schaumann H., and Gaub H. Atomic force microscope imaging of phospholipid bilayer degradation by phospholipase A(2). Biophys. J. 74 (1998) 2398-2404
23. Kaasgaard T., Leidy C., Ipsen J.H., Mouritsen O.G., and Jorgensen K. In situ atomic force microscope imaging of supported lipid bilayers. Single Mol. 2 (2001) 105-108
24. Leidy C., Mouritsen O.G., Jorgensen K., and Peters N.H. Evolution of a rippled membrane during phospholipase A(2) hydrolysis studied by time-resolved AFM. Biophys. J. 87 (2004) 408-418
25. Hoyrup P., Callisen T.H., Jensen M.O., Halperin A., and Mouritsen O.G. Lipid protrusions, membrane softness, and enzymatic activity. Phys. Chem. Chem. Phys. 6 (2004) 1608-1615
26. Halperin A., and Mouritsen O.G. Role of lipid protrusions in the function of interfacial enzymes. Eur. Biophys. J. Biophys. Lett. 34 (2005) 967-971
27. Subramaniam S., and McConnell H.M. Critical mixing in monolayer mixtures of phospholipid and cholesterol. J. Phys. Chem. 91 (1987) 1715-1718
28. McConnell H.M., and Vrljic M. Liquid-liquid immiscibility in membranes. Annu. Rev. Biophys. Biomol. Struct. 32 (2003) 469-492
29. Okonogi T.M., and McConnell H.M. Contrast inversion in the epifluorescence of cholesterol-phospholipid monolayers. Biophys. J. 86 (2004) 880-890
30. Dahmen-Levison U., and Brezesinski G. Methyl-branched glycerophosphocholines: monolayer disorder and its effect on the rate of phospholipase A(2) catalyzed hydrolysis. Phys. Chem. Chem. Phys. 2 (2000) 4605-4608
31. Leidy C., Linderoth L., Andresen T.L., Mouritsen O.G., Jorgensen K., and Peters G.H. Domain-induced activation of human phospholipase A2 type IIA: local versus global lipid composition. Biophys. J. 90 (2006) 3165-3175
32. Flach C.R., Brauner J.W., Taylor J.W., Baldwin R.C., and Mendelsohn R. External reflection FTIR of peptide monolayer films in-situ at the air/water interface - experimental-design, spectra-structure correlations, and effects of hydrogen-deuterium exchange. Biophys. J. 67 (1994) 402-410
33. Blaudez D., Buffeteau T., Cornut J.C., Desbat B., Escafre N., Pezolet M., and Turlet J.M. Polarization modulation FTIR spectroscopy at the air-water-interface. Thin Solid Films 242 (1994) 146-150
34. Blaudez D., Buffeteau T., Cornut J.C., Desbat B., Escafre N., Pezolet M., and Turlet J.M. Polarization-modulated FT-IR spectroscopy of a spread monolayer at the air-water-interface. Appl. Spectrosc. 47 (1993) 869-874
35. Wang X.L., Zheng S.P., He Q., Brezesinski G., Möhwald H., and Li J.B. Hydrolysis reaction analysis of l-alpha-distearoylphosphatidyleholine monolayer catalyzed by phospholipase A(2) with polarization-modulated infrared reflection absorption spectroscopy. Langmuir 21 (2005) 1051-1054
36. Chaplin M. Molecular Vibration and Absorption. In: Chaplin M. (Ed). Water structure and behavior, Department of Applied Science, London South Bank University (2007). http://www.lsbu.ac.uk/water/vibrat http://www.lsbu.ac.uk/water/vibrat
37. Blume A., Hübner W., and Messner G. Fourier-transform infrared-spectroscopy of C-13 = O-labeled phospholipids hydrogen-bonding to carbonyl groups. Biochemistry 27 (1988) 8239-8249
38. Hübner W., and Mantsch H.H. Orientation of specifically C-13 = O labeled phosphatidylcholine multilayers from polarized attenuated total reflection FT-IR spectroscopy. Biophys. J. 59 (1991) 1261-1272
39. Volkov V.V., Nuti F., Takaoka Y., Chelli R., Papini A.M., and Righini R. Hydration and hydrogen bonding of carbonyls in dimyristoyl-phosphatidylcholine bilayer. J. Am. Chem. Soc. 128 (2006) 9466-9471
40. Arrondo J.L.R., Goni F.M., and Macarulla J.M. Infrared-spectroscopy of phosphatidylcholines in aqueous suspension-a study of the phosphate group vibrations. Biochim. Biophys. Acta 794 (1984) 165-168
41. Hübner W., and Blume A. Interactions at the lipid-water interface. Chem. Phys. Lipids 96 (1998) 99-123
42. Albrecht O., Matsuda H., Eguchi K., and Nakagiri T. The dissolution of myristic acid monolayers in water. Thin Solid Films 338 (1999) 252-264
43. Wacklin H.P., Tiberg F., Fragneto G., and Thomas R.K. Distribution of reaction products in phospholipase A2 hydrolysis. Biochim. Biophys. Acta, Biomembr. 1768 (2007) 1036-1049
44. Brauner J.W., Flach C.R., Xu Z., Bi X.H., Lewis R., McElhaney R.N., Gericke A., and Mendelsohn R. Quantitative functional group orientation in Langmuir films by infrared reflection-absorption spectroscopy: C{double bond, long}O groups in behenic acid methyl ester and sn2-C-13-DSPC. J. Phys. Chem., B 107 (2003) 7202-7211
45. Jensen L.B., Burgess N.K., Gonda D.D., Spencer E., Wilson-Ashworth H.A., Driscoll E., Vu M.P., Fairbourn J.L., Judd A.M., and Bell J.D. Mechanisms governing the level of susceptibility of erythrocyte membranes to secretory phospholipase A(2). Biophys. J. 88 (2005) 2692-2705
46. Jain M.K., and Berg O.G. Coupling of the i-face and the active site of phospholipase A(2) for interfacial activation. Curr. Opin. Chem. Biol. 10 (2006) 473-479
47. Lin Y., Nielsen R., Murray D., Hubbell W.L., Mailer C., Robinson B.H., and Gelb M.H. Docking phospholipase A(2) on membranes using electrostatic potential-modulated spin relaxation magnetic resonance. Science 279 (1998) 1925-1929
48. Pande A.H., Qin S., Nemec K.N., He X.M., and Tatulian S.A. Isoform-specific membrane insertion of secretory phospholipase A(2) and functional implications. Biochemistry 45 (2006) 12436-12447
49. Vacklin H.P., Tiberg F., Fragneto G., and Thomas R.K. Phospholipase A(2) hydrolysis of supported phospholipid bilayers: A neutron reflectivity and ellipsometry study. Biochemistry 44 (2005) 2811-2821
50. Jensen U.B., and Simonsen A.C. Shape relaxations in a fluid supported membrane during hydrolysis by phospholipase A(2). Biochim. Biophys. Acta, Biomembr. 1715 (2005) 1-5
51. Simonsen A.C., Jensen U.B., and Hansen P.L. Hydrolysis of fluid supported membrane islands by phospholipase A(2): Time-lapse imaging and kinetic analysis. J. Colloid Interface Sci. 301 (2006) 107-115
52. Wagner K., and Brezesinski G. Phospholipase D activity is regulated by product segregation and the structure formation of phosphatidic acid within model membranes. Biophys. J. 93 (2007) 2373-2383
53. Slotte J.P. Lateral domain heterogeneity in cholesterol phosphatidylcholine monolayers as a function of cholesterol concentration and phosphatidylcholine acyl-chain length. Biochim. Biophys. Acta, Biomembr. 1238 (1995) 118-126
54. Hagen J.P., and McConnell H.M. Critical pressures in multicomponent lipid monolayers. Biochim. Biophys. Acta, Biomembr. 1280 (1996) 169-172
55. Scott D.L., White S.P., Otwinowski Z., Yuan W., Gelb M.H., and Sigler P.B. Interfacial catalysis-the mechanism of phospholipase-A2. Science 250 (1990) 1541-1546
56. Winget J.M., Pan Y.H., and Bahnson B.J. The interfacial binding surface of phospholipase A2s. BBA-Mol. Cell. Biol. Lipids 1761 (2006) 1260-1269
57. Keller S.L., Radhakrishnan A., and McConnell H.M. Saturated phospholipids with high melting temperatures form complexes with cholesterol in monolayers. J. Phys. Chem., B 104 (2000) 7522-7527
58. Liu F., and Chong P.L.G. Evidence for a regulatory role of cholesterol superlattices in the hydrolytic activity of secretory phospholipase A2 in lipid membranes. Biochemistry 38 (1999) 3867-3873
59. Veatch S.L., and Keller S.L. Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta, Mol. Cell Res. 1746 (2005) 172-185
60. Simons K., and Toomre D. Lipid rafts and signal transduction. Nat. Rev., Mol. Cell Biol. 1 (2000) 31-39