Effects of cholesterol on physical properties of human erythrocyte membranes: Impact on susceptibility to hydrolysis by secretory phospholipase A2

Biophysical Journal

Volumn 94, Issue 8, 2008, Pages 3084-3093

  Heiner, Anne L ^a   Gibbons, Elizabeth ^a   Fairbourn, Jeremy L ^a   Gonzalez, Laurie J ^a   McLemore, Chisako O ^a   Brueseke, Taylor J ^a   Judd, Allan M ^a   Bell, John D ^a  

^a BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; SECRETORY PHOSPHOLIPASE A2;

ARTICLE; CELL CULTURE; CHEMISTRY; DRUG EFFECT; ERYTHROCYTE MEMBRANE; HUMAN; HYDROLYSIS; MEMBRANE FLUIDITY; METABOLISM; PHASE TRANSITION; PHYSIOLOGY;

CELLS, CULTURED; CHOLESTEROL; ERYTHROCYTE MEMBRANE; HUMANS; HYDROLYSIS; MEMBRANE FLUIDITY; PHASE TRANSITION; PHOSPHOLIPASES A2, SECRETORY;

EID: 43149124850     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.118356     Document Type: Article

References (69)

1. Yethiraj, A., and J. C. Weisshaar. 2007. Why are lipid rafts not observed in vivo? Biophys. J. 93:3113-3119.
2. Gelb, M. H., M. K. Jain, A. M. Hanel, and O. G. Berg. 1995. Interfacial enzymology of glycerolipid hydrolases: lessons from secreted phospholipases A2. Annu. Rev. Biochem. 64:653-688.
3. Winget, J. M., Y. H. Pan, and B. J. Bahnson. 2006. The interfacial binding surface of phospholipase A2s. Biochim. Biophys. Acta. 1761:1260-1269.
4. Lichtenberg, D., G. Romero, M. Menashe, and R. L. Biltonen. 1986. Hydrolysis of dipalmitoylphosphatidylcholine large unilamellar vesicles by porcine pancreatic phospholipase A2. J. Biol. Chem. 261:5334-5340.
5. Bell, J. D., and R. L. Biltonen. 1989. The temporal sequence of events in the activation of phospholipase A2 by lipid vesicles. Studies with the monomeric enzyme from Agkistrodon piscivorus piscivorus. J. Biol. Chem. 264:12194-12200.
6. Bell, J. D., and R. L. Biltonen. 1992. Molecular details of the activation of soluble phospholipase A2 on lipid bilayers. Comparison of computer simulations with experimental results. J. Biol. Chem. 267:11046-11056.
7. Bell, J. D., M. L. Baker, E. D. Bent, R. W. Ashton, D. J. Hemming, and L. D. Hansen. 1995. Effects of temperature and glycerides on the enhancement of Agkistrodon piscivorus piscivorus phospholipase A2 activity by lysolecithin and palmitic acid. Biochemistry. 34:11551-11560.
8. Henshaw, J. B., C. A. Olsen, A. R. Farnbach, K. H. Nielson, and J. D. Bell. 1998. Definition of the specific roles of lysolecithin and palmitic acid in altering the susceptibility of dipalmitoylphosphatidylcholine bilayers to phospholipase A2. Biochemistry. 37:10709-10721.
9. Jain, M. K., and G. H. de Haas. 1983. Activation of phospholipase A2 by freshly added lysophospholipids. Biochim. Biophys. Acta. 736:157-162.
10. Menashe, M., G. Romero, R. L. Biltonen, and D. Lichtenberg. 1986. Hydrolysis of dipalmitoylphosphatidylcholine small unilamellar vesicles by porcine pancreatic phospholipase A2. J. Biol. Chem. 261:5328-5333.
11. Gheriani-Gruszka, N., S. Almog, R. L. Biltonen, and D. Lichtenberg. 1988. Hydrolysis of phosphatidylcholine in phosphatidylcholine-cholate mixtures by porcine pancreatic phospholipase A2. J. Biol. Chem. 263:11808-11813.
12. Jain, M. K., B. Z. Yu, and A. Kozubek. 1989. Binding of phospholipase A2 to zwitterionic bilayers is promoted by lateral segregation of anionic amphiphiles. Biochim. Biophys. Acta. 980:23-32.
13. Bent, E. D., and J. D. Bell. 1995. Quantification of the interactions among fatty acid, lysophosphatidylcholine, calcium, dimyristoylphosphatidylcholine vesicles, and phospholipase A2. Biochim. Biophys. Acta. 1254:349-360.
14. Bell, J. D., M. Burnside, J. A. Owen, M. L. Royall, and M. L. Baker. 1996. Relationships between bilayer structure and phospholipase A2 activity: interactions among temperature, diacylglycerol, lysolecithin, palmitic acid, and dipalmitoylphosphatidylcholine. Biochemistry. 35:4945-4955.
15. Hoyrup, P., T. H. Callisen, M. O. Jensen, A. Halperin, and O. G. Mouritsen. 2004. Lipid protrusions, membrane softness, and enzymatic activity. Phys. Chem. Chem. Phys. 6:1608-1615.
16. Honger, T., K. Jorgensen, R. L. Biltonen, and O. G. Mouritsen. 1996. Systematic relationship between phospholipase A2 activity and dynamic lipid bilayer microheterogeneity. Biochemistry. 35:9003-9006.
17. Salomon, Y., C. Londos, and M. Rodbell. 1974. A highly sensitive adenylate cyclase assay. Anal. Biochem. 58:541-548.
18. Brueseke, T. J., and J. D. Bell. 2006. A new hat for an old enzyme: Waste management. Biochim. Biophys. Acta. 1761:1270-1279.
19. Wilson, H. A., J. B. Waldrip, K. H. Nielson, A. M. Judd, S. K. Han, W. Cho, P. J. Sims, and J. D. Bell. 1999. Mechanisms by which elevated intracellular calcium induces S49 cell membranes to become susceptible to the action of secretory phospholipase A2. J. Biol. Chem. 274:11494-11504.
20. Nielson, K. H., C. A. Olsen, D. V. Allred, K. L. O'Neill, G. F. Burton, and J. D. Bell. 2000. Susceptibility of S49 lymphoma cell membranes to hydrolysis by secretory phospholipase A(2) during early phase of apoptosis. Biochim. Biophys. Acta. 1484:163-174.
21. Smith, S. K., A. R. Farnbach, F. M. Harris, A. C. Hawes, L. R. Jackson, A. M. Judd, R. S. Vest, S. Sanchez, and J. D. Bell. 2001. Mechanisms by which intracellular calcium induces susceptibility to secretory phospholipase A2 in human erythrocytes. J. Biol. Chem. 276:22732-22741.
22. Best, K. B., A. J. Ohran, A. C. Hawes, T. L. Hazlett, E. Gratton, A. M. Judd, and J. D. Bell. 2002. Relationship between erythrocyte membrane phase properties and susceptibility to secretory phospholipase A2. Biochemistry. 41:13982-13988.
23. Jensen, L. B., N. K. Burgess, D. D. Gonda, E. Spencer, H. A. Wilson-Ashworth, E. Driscoll, M. P. Vu, J. L. Fairbourn, A. M. Judd, and J. D. Bell. 2005. Mechanisms governing the level of susceptibility of erythrocyte membranes to secretory phospholipase A2. Biophys. J. 88:2692-2705.
24. Bailey, R. W., E. D. Olson, M. P. Vu, T. J. Brueseke, L. Robertson, R. E. Christensen, K. H. Parker, A. M. Judd, and J. D. Bell. 2007. Relationship between membrane physical properties and secretory phospholipase A2 hydrolysis kinetics in S49 cells during ionophore-induced apoptosis. Biophys. J. 93:2350-2362.
25. Parasassi, T., M. Di Stefano, M. Loiero, G. Ravagnan, and E. Gratton. 1994. Cholesterol modifies water concentration and dynamics in phospholipid bilayers: a fluorescence study using Laurdan probe. Biophys. J. 66:763-768.
26. Wang, M. M., M. Olsher, I. P. Sugar, and P. L. Chong. 2004. Cholesterol superlattice modulates the activity of cholesterol oxidase in lipid membranes. Biochemistry. 43:2159-2166.
27. Veatch, S. L., and S. L. Keller. 2005. Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta. 1746:172-185.
28. Barenholz, Y. 2004. Sphingomyelin and cholesterol: from membrane biophysics and rafts to potential medical applications. Subcell. Biochem. 37:167-215.
29. Wilson-Ashworth, H. A., Q. Bahm, J. Erickson, A. Shinkle, M. P. Vu, D. Woodbury, and J. D. Bell. 2006. Differential detection of phospholipid fluidity, order, and spacing by fluorescence spectroscopy of bis-pyrene, prodan, nystatin, and merocyanine 540. Biophys. J. 91:4091-4101.
30. McConnell, H., and A. Radhakrishnan. 2006. Theory of the deuterium NMR of sterol-phospholipid membranes. Proc. Natl. Acad. Sci. USA. 103:1184-1189.
31. Mannock, D. A., R. N. Lewis, and R. N. McElhaney. 2006. Comparative calorimetric and spectroscopic studies of the effects of lanosterol and cholesterol on the thermotropic phase behavior and organization of dipalmitoylphosphatidylcholine bilayer membranes. Biophys. J. 91:3327-3340.
32. Pandit, S. A., G. Khelashvili, E. Jakobsson, A. Grama, and H. L. Scott. 2007. Lateral organization in lipid-cholesterol mixed bilayers. Biophys. J. 92:440-447.
33. Op den Kamp, J. A., M. T. Kauerz, and L. L. Van Deenen. 1975. Action of pancreatic phospholipase A2 on phosphatidylcholine bilayers in different physical states. Biochim. Biophys. Acta. 406:169-177.
34. Liu, F., and P. L. Chong. 1999. Evidence for a regulatory role of cholesterol superlattices in the hydrolytic activity of secretory phospholipase A2 in lipid membranes. Biochemistry. 38:3867-3873.
35. Kannagi, R., and K. Koizumi. 1979. Effect of different physical states of phospholipid substrates on partially purified platelet phospholipase A2 activity. Biochim. Biophys. Acta. 556:423-433.
36. Richieri, G. V., and A. M. Kleinfeld. 1995. Continuous measurement of phospholipase A2 activity using the fluorescent probe ADIFAB. Anal. Biochem. 229:256-263.
37. Koumanov, K. S., P. J. Quinn, G. Bereziat, and C. Wolf. 1998. Cholesterol relieves the inhibitory effect of sphingomyelin on type II secretory phospholipase A2. Biochem. J. 336:625-630.
38. Gottfried, E. L. 1967. Lipids of human leukocytes: relation to cell type. J. Lipid Res. 8:321-327.
39. Parmahamsa, M., K. R. Reddy, and N. Varadacharyulu. 2004. Changes in composition and properties of erythrocyte membrane in chronic alcoholics. Alcohol Alcohol. 39:110-112.
40. Ashworth, L. A., and C. Green. 1966. Plasma membranes: phospholipid and sterol content. Science. 151:210-211.
41. Marcus, A. J., H. L. Ullman, and L. B. Safier. 1969. Lipid composition of subcellular particles of human blood platelets. J. Lipid Res. 10:108-114.
42. Johnson, S. M., and R. Robinson. 1979. The composition and fluidity of normal and leukaemic or lymphomatous lymphocyte plasma membranes in mouse and man. Biochim. Biophys. Acta. 558:282-295.
43. Rigaud, J. L., and G. Leblanc. 1980. Effect of membrane cholesterol on action of phospholipase A2 in Mycoplasma mycoides var. Capri. Evidence for lysophospholipase activity. Eur. J. Biochem. 110:77-84.
44. + exchange within human platelets. FEBS Lett. 299:19-22.
45. Klein, U., G. Gimpl, and F. Fahrenholz. 1995. Alteration of the myometrial plasma membrane cholesterol content with beta-cyclodextrin modulates the binding affinity of the oxytocin receptor. Biochemistry. 34:13784-13793.
46. Ohtani, Y., T. Irie, K. Uekama, K. Fukunaga, and J. Pitha. 1989. Differential effects of alpha-, beta- and gamma-cyclodextrins on human erythrocytes. Eur. J. Biochem. 186:17-22.
47. Wolkers, W. F., L. M. Crowe, N. M. Tsvetkova, F. Tablin, and J. H. Crowe. 2002. In situ assessment of erythrocyte membrane properties during cold storage. Mol. Membr. Biol. 19:59-65.
48. Yancey, P. G., W. V. Rodrigueza, E. P. Kilsdonk, G. W. Stoudt, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1996. Cellular cholesterol efflux mediated by cyclodextrins. Demonstration of kinetic pools and mechanism of efflux. J. Biol. Chem. 271:16026-16034.
49. Pitha, J., T. Irie, P. B. Sklar, and J. S. Nye. 1988. Drug solubilizers to aid pharmacologists: amorphous cyclodextrin derivatives. Life Sci. 43:493-502.
50. Maraganore, J. M., G. Merutka, W. Cho, W. Welches, F. J. Kezdy, and R. L. Heinrikson. 1984. A new class of phospholipases A2 with lysine in place of aspartate 49. Functional consequences for calcium and substrate binding. J. Biol. Chem. 259:13839-13843.
51. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
52. Parasassi, T., G. De Stasio, G. Ravagnan, R. M. Rusch, and E. Gratton. 1991. Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence. Biophys. J. 60:179-189.
53. Harris, F. M., S. K. Smith, and J. D. Bell. 2001. Physical properties of erythrocyte ghosts that determine susceptibility to secretory phospholipase A2. J. Biol. Chem. 276:22722-22731.
54. Richieri, G. V., R. T. Ogata, and A. M. Kleinfeld. 1992. A fluorescently labeled intestinal fatty acid binding protein. Interactions with fatty acids and its use in monitoring free fatty acids. J. Biol. Chem. 267:23495-23501.
55. Yu, W., P. T. So, T. French, and E. Gratton. 1996. Fluorescence generalized polarization of cell membranes: a two-photon scanning microscopy approach. Biophys. J. 70:626-636.
56. Harris, F. M., K. B. Best, and J. D. Bell. 2002. Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order. Biochim. Biophys. Acta. 1565:123-128.
57. Vest, R. S., L. J. Gonzales, S. A. Permann, E. Spencer, L. D. Hansen, A. M. Judd, and J. D. Bell. 2004. Divalent cations increase lipid order in erythrocytes and susceptibility to secretory phospholipase A2. Biophys. J. 86:2251-2260.
58. Jain, M. K., and D. V. Jahagirdar. 1985. Action of phospholipase A2 on bilayers. Effect of fatty acid and lysophospholipid additives on the kinetic parameters. Biochim. Biophys. Acta. 814:313-318.
59. Burack, W. R., Q. Yuan, and R. L. Biltonen. 1993. Role of lateral phase separation in the modulation of phospholipase A2 activity. Biochemistry. 32:583-589.
60. Brown, S. D., B. L. Baker, and J. D. Bell. 1993. Quantification of the interaction of lysolecithin with phosphatidylcholine vesicles using bovine serum albumin: relevance to the activation of phospholipase A2. Biochim. Biophys. Acta. 1168:13-22.
61. Honger, T., K. Jorgensen, D. Stokes, R. L. Biltonen, and O. G. Mouritsen. 1997. Phospholipase A2 activity and physical properties of lipid-bilayer substrates. Methods Enzymol. 286:168-190.
62. Burack, W. R., A. R. Dibble, M. M. Allietta, and R. L. Biltonen. 1997. Changes in vesicle morphology induced by lateral phase separation modulate phospholipase A2 activity. Biochemistry. 36:10551-10557.
63. Menashe, M., D. Lichtenberg, C. Gutierrez-Merino, and R. L. Biltonen. 1981. Relationship between the activity of pancreatic phospholipase A2 and the physical state of the phospholipid substrate. J. Biol. Chem. 256:4541-4543.
64. Sheffield, M. J., B. L. Baker, D. Li, N. L. Owen, M. L. Baker, and J. D. Bell. 1995. Enhancement of Agkistrodon piscivorus piscivorus venom phospholipase A2 activity toward phosphatidylcholine vesicles by lysolecithin and palmitic acid: studies with fluorescent probes of membrane structure. Biochemistry. 34:7796-7806.
65. Parasassi, T., A. M. Giusti, M. Raimondi, and E. Gratton. 1995. Abrupt modifications of phospholipid bilayer properties at critical cholesterol concentrations. Biophys. J. 68:1895-1902.
66. Zidovetzki, R., and I. Levitan. 2007. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim. Biophys. Acta. 1768:1311-1324.
67. Kilsdonk, E. P., P. G. Yancey, G. W. Stoudt, F. W. Bangerter, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1995. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 270:17250-17256.
68. Lange, Y., H. B. Cutler, and T. L. Steck. 1980. The effect of cholesterol and other intercalated amphipaths on the contour and stability of the isolated red cell membrane. J. Biol. Chem. 255:9331-9337.
69. Kim, K. P., J. D. Rafter, L. Bittova, S. K. Han, Y. Snitko, N. M. Munoz, A. R. Leff, and W. Cho. 2001. Mechanism of human group V phospholipase A2 (PLA2)-induced leukotriene biosynthesis in human neutrophils. A potential role of heparan sulfate binding in PLA2 internalization and degradation. J. Biol. Chem. 276:11126-11134.