Relationship between membrane permeability and specificity of human secretory phospholipase A2 isoforms during cell death

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 7, 2011, Pages 1913-1920

  Nelson, Jennifer ^a   Gibbons, Elizabeth ^a   Pickett, Katalyn R ^a   Streeter, Michael ^a   Warcup, Ashley O ^a   Yeung, Celestine H Y ^a   Judd, Allan M ^a   Bell, John D ^a  

^a BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

Apoptosis; Fluorescence spectroscopy; Membrane biophysics; Merocyanine 540; Propidium iodide

Indexed keywords

CALCIUM IONOPHORE; DEXAMETHASONE; ISOENZYME; MEROCYANINE; PHOSPHOLIPASE V; PHOSPHOLIPASE X; PROPIDIUM IODIDE; SECRETORY PHOSPHOLIPASE A2; SNAKE VENOM; THAPSIGARGIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME SPECIFICITY; FLOW CYTOMETRY; HYDROLYSIS; LYMPHOMA CELL; MACROPHAGE MIGRATION; MAMMAL CELL; MEMBRANE PERMEABILITY; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CELL DEATH; CELL LINE, TUMOR; CELL MEMBRANE PERMEABILITY; FLOW CYTOMETRY; HUMANS; HYDROLYSIS; ISOENZYMES; MICE; PHOSPHOLIPASES A2; PROPIDIUM; SUBSTRATE SPECIFICITY;

MAMMALIA;

EID: 79955841019     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.04.003     Document Type: Article

References (70)

1. Z. Darzynkiewicz, G. Juan, X. Li, W. Gorczyca, T. Murakami, and F. Traganos Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death necrosis Cytometry 27 1997 1 20 (Pubitemid 27059777)
2. M. Vitale, L. Zamai, G. Mazzotti, A. Cataldi, and E. Falcieri Differential kinetics of propidium iodide uptake in apoptotic and necrotic thymocytes Histochemistry 100 1993 223 229 (Pubitemid 23285678)
3. L. Zamai, E. Falcieri, G. Marhefka, and M. Vitale Supravital exposure to propidium iodide identifies apoptotic cells in the absence of nucleosomal DNA fragmentation Cytometry 23 1996 303 311
4. G. Atsumi, M. Murakami, M. Tajima, S. Shimbara, N. Hara, and I. Kudo The perturbed membrane of cells undergoing apoptosis is susceptible to type II secretory phospholipase A2 to liberate arachidonic acid Biochim. Biophys. Acta 1349 1997 43 54 (Pubitemid 27517522)
5. K.H. Nielson, C.A. Olsen, D.V. Allred, K.L. O'Neill, G.F. Burton, and J.D. Bell Susceptibility of S49 lymphoma cell membranes to hydrolysis by secretory phospholipase A(2) during early phase of apoptosis Biochim. Biophys. Acta 1484 2000 163 174 (Pubitemid 30175966)
6. R.W. Bailey, E.D. Olson, M.P. Vu, T.J. Brueseke, L. Robertson, R.E. Christensen, K.H. Parker, A.M. Judd, and J.D. Bell Relationship between membrane physical properties and secretory phospholipase A2 hydrolysis kinetics in S49 cells during ionophore-induced apoptosis Biophys. J. 93 2007 2350 2362 (Pubitemid 47511135)
7. R.W. Bailey, T. Nguyen, L. Robertson, E. Gibbons, J. Nelson, R.E. Christensen, J.P. Bell, A.M. Judd, and J.D. Bell Sequence of physical changes to the cell membrane during glucocorticoid-induced apoptosis in S49 lymphoma cells Biophys. J. 96 2009 2709 2718
8. E.D. Olson, J. Nelson, K. Griffith, T. Nguyen, M. Streeter, H.A. Wilson-Ashworth, M.H. Gelb, A.M. Judd, and J.D. Bell Kinetic evaluation of cell membrane hydrolysis during apoptosis by human isoforms of secretory phospholipase A2 J. Biol. Chem. 285 2010 10993 11002
9. L.B. Jensen, 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 Mechanisms governing the level of susceptibility of erythrocyte membranes to secretory phospholipase A2 Biophys. J. 88 2005 2692 2705 (Pubitemid 40976136)
10. H.A. Wilson, J.B. Waldrip, K.H. Nielson, A.M. Judd, S.K. Han, W. Cho, P.J. Sims, and J.D. Bell Mechanisms by which elevated intracellular calcium induces S49 cell membranes to become susceptible to the action of secretory phospholipase A2 J. Biol. Chem. 274 1999 11494 11504
11. K.B. Best, A.J. Ohran, A.C. Hawes, T.L. Hazlett, E. Gratton, A.M. Judd, and J.D. Bell Relationship between erythrocyte membrane phase properties and susceptibility to secretory phospholipase A2 Biochemistry 41 2002 13982 13988 (Pubitemid 35364870)
12. S. Bezzine, J.G. Bollinger, A.G. Singer, S.L. Veatch, S.L. Keller, and M.H. Gelb On the binding preference of human groups IIA and X phospholipases A2 for membranes with anionic phospholipids J. Biol. Chem. 277 2002 48523 48534 (Pubitemid 35470813)
13. A.G. Singer, F. Ghomashchi, C. Le Calvez, J. Bollinger, S. Bezzine, M. Rouault, M. Sadilek, M. Lazdunski, G. Lambeau, and M.H. Gelb 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 2002 48535 48549 (Pubitemid 35470814)
14. F.M. Harris, S.K. Smith, and J.D. Bell Physical properties of erythrocyte ghosts that determine susceptibility to secretory phospholipase A2 J. Biol. Chem. 276 2001 22722 22731
15. S.K. Smith, A.R. Farnbach, F.M. Harris, A.C. Hawes, L.R. Jackson, A.M. Judd, R.S. Vest, S. Sanchez, and J.D. Bell Mechanisms by which intracellular calcium induces susceptibility to secretory phospholipase A2 in human erythrocytes J. Biol. Chem. 276 2001 22732 22741
16. X. Bian, F.M. Hughes Jr., Y. Huang, J.A. Cidlowski, and J.W. Putney Jr. Roles of cytoplasmic Ca2+ and intracellular Ca2+ stores in induction and suppression of apoptosis in S49 cells Am. J. Physiol. 272 1997 C1241 C1249
17. G.E. Kass, and S. Orrenius Calcium signaling and cytotoxicity Environ. Health Perspect. 107 Suppl 1 1999 25 35 (Pubitemid 29164197)
18. I. Yoshida, A. Monji, K. Tashiro, K. Nakamura, R. Inoue, and S. Kanba Depletion of intracellular Ca2+ store itself may be a major factor in thapsigargin-induced ER stress and apoptosis in PC12 cells Neurochem. Int. 48 2006 696 702
19. D.A. Mower Jr., D.W. Peckham, V.A. Illera, J.K. Fishbaugh, L.L. Stunz, and R.F. Ashman Decreased membrane phospholipid packing and decreased cell size precede DNA cleavage in mature mouse B cell apoptosis J. Immunol. 152 1994 4832 4842 (Pubitemid 24139076)
20. R.F. Ashman, D. Peckham, S. Alhasan, and L.L. Stunz Membrane unpacking and the rapid disposal of apoptotic cells Immunol. Lett. 48 1995 159 166 (Pubitemid 26074227)
21. W. Stillwell, S.R. Wassall, A.C. Dumaual, W.D. Ehringer, C.W. Browning, and L.J. Jenski Use of merocyanine (MC540) in quantifying lipid domains and packing in phospholipid vesicles and tumor cells Biochim. Biophys. Acta 1146 1993 136 144 (Pubitemid 23067052)
22. S.J. Martin, C.P. Reutelingsperger, A.J. McGahon, J.A. Rader, R.C. van Schie, D.M. LaFace, and D.R. Green Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl J. Exp. Med. 182 1995 1545 1556
23. C. Diaz, A.T. Lee, D.J. McConkey, and A.J. Schroit Phosphatidylserine externalization during differentiation-triggered apoptosis of erythroleukemic cells Cell Death Differ. 6 1999 218 226 (Pubitemid 29145825)
24. A.J. Mazur, D. Nowak, H.G. Mannherz, and M. Malicka-Blaszkiewicz Methotrexate induces apoptosis in CaSki and NRK cells and influences the organization of their actin cytoskeleton Eur. J. Pharmacol. 613 2009 24 33
25. H.J. Ahn, Y.S. Kim, J.U. Kim, S.M. Han, J.W. Shin, and H.O. Yang Mechanism of taxol-induced apoptosis in human SKOV3 ovarian carcinoma cells J. Cell. Biochem. 91 2004 1043 1052
26. J.M. Maraganore, G. Merutka, W. Cho, W. Welches, F.J. Kezdy, and R.L. Heinrikson A new class of phospholipases A2 with lysine in place of aspartate 49. Functional consequences for calcium and substrate binding J. Biol. Chem. 259 1984 13839 13843 (Pubitemid 15222813)
27. S.F. Baker, R. Othman, and D.C. Wilton Tryptophan-containing mutant of human (group IIa) secreted phospholipase A2 has a dramatically increased ability to hydrolyze phosphatidylcholine vesicles and cell membranes Biochemistry 37 1998 13203 13211 (Pubitemid 28449564)
28. M. Markova, R.A. Koratkar, K.A. Silverman, V.E. Sollars, M. MacPhee-Pellini, R. Walters, J.P. Palazzo, A.M. Buchberg, L.D. Siracusa, and S.A. Farber Diversity in secreted PLA2-IIA activity among inbred mouse strains that are resistant or susceptible to Apc Min/+ tumorigenesis Oncogene 24 2005 6450 6458 (Pubitemid 41486478)
29. W. Cho, S.K. Han, B.I. Lee, Y. Snitko, and R. Dua Purification and assay of mammalian group I and group IIa secretory phospholipase A2 Methods Mol. Biol. 109 1999 31 38
30. Y.H. Pan, B.Z. Yu, A.G. Singer, F. Ghomashchi, G. Lambeau, M.H. Gelb, M.K. Jain, and B.J. Bahnson Crystal structure of human group X secreted phospholipase A2. Electrostatically neutral interfacial surface targets zwitterionic membranes J. Biol. Chem. 277 2002 29086 29093
31. B.M. Stott, M.P. Vu, C.O. McLemore, M.S. Lund, E. Gibbons, T.J. Brueseke, H.A. Wilson-Ashworth, and J.D. Bell Use of fluorescence to determine the effects of cholesterol on lipid behavior in sphingomyelin liposomes and erythrocyte membranes J. Lipid Res. 49 2008 1202 1215
32. H.A. Wilson, W. Huang, J.B. Waldrip, A.M. Judd, L.P. Vernon, and J.D. Bell Mechanisms by which thionin induces susceptibility of S49 cell membranes to extracellular phospholipase A2 Biochim. Biophys. Acta 1349 1997 142 156 (Pubitemid 27519556)
33. C. Riccardi, and I. Nicoletti Analysis of apoptosis by propidium iodide staining and flow cytometry Nat. Protoc. 1 2006 1458 1461
34. J.D. Bell, and R.L. Biltonen 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 1989 12194 12200
35. D. Lichtenberg, G. Romero, M. Menashe, and R.L. Biltonen Hydrolysis of dipalmitoylphosphatidylcholine large unilamellar vesicles by porcine pancreatic phospholipase A2 J. Biol. Chem. 261 1986 5334 5340 (Pubitemid 17204341)
36. T. Honger, K. Jorgensen, R.L. Biltonen, and O.G. Mouritsen Systematic relationship between phospholipase A2 activity and dynamic lipid bilayer microheterogeneity Biochemistry 35 1996 9003 9006 (Pubitemid 26249845)
37. S.A. Beers, A.G. Buckland, R.S. Koduri, W. Cho, M.H. Gelb, and D.C. Wilton 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 2002 1788 1793 (Pubitemid 34968750)
38. B.B. Boyanovsky, and N.R. Webb Biology of secretory phospholipase A2 Cardiovasc. Drugs Ther. 23 2009 61 72
39. C.N. Birts, C.H. Barton, and D.C. Wilton Catalytic and non-catalytic functions of human IIA phospholipase A2 Trends Biochem. Sci. 35 2010 28 35
40. S.A. Beers, A.G. Buckland, N. Giles, M.H. Gelb, and D.C. Wilton Effect of tryptophan insertions on the properties of the human group IIA phospholipase A2: mutagenesis produces an enzyme with characteristics similar to those of the human group V phospholipase A2 Biochemistry 42 2003 7326 7338 (Pubitemid 36735811)
41. Y.Y. Tyurina, A.A. Shvedova, K. Kawai, V.A. Tyurin, C. Kommineni, P.J. Quinn, N.F. Schor, J.P. Fabisiak, and V.E. Kagan Phospholipid signaling in apoptosis: peroxidation and externalization of phosphatidylserine Toxicology 148 2000 93 101 (Pubitemid 30621348)
42. M.E. Greenberg, X.M. Li, B.G. Gugiu, X. Gu, J. Qin, R.G. Salomon, and S.L. Hazen The lipid whisker model of the structure of oxidized cell membranes J. Biol. Chem. 283 2008 2385 2396
43. V.A. Tyurin, Y.Y. Tyurina, M.Y. Jung, M.A. Tungekar, K.J. Wasserloos, H. Bayir, J.S. Greenberger, P.M. Kochanek, A.A. Shvedova, B. Pitt, and V.E. Kagan Mass-spectrometric analysis of hydroperoxy- and hydroxy-derivatives of cardiolipin and phosphatidylserine in cells and tissues induced by pro-apoptotic and pro-inflammatory stimuli J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 877 2009 2863 2872
44. V.A. Tyurin, Y.Y. Tyurina, P.M. Kochanek, R. Hamilton, S.T. DeKosky, J.S. Greenberger, H. Bayir, and V.E. Kagan Oxidative lipidomics of programmed cell death Methods Enzymol. 442 2008 375 393
45. D. Yajima, H. Motani, M. Hayakawa, Y. Sato, K. Sato, and H. Iwase The relationship between cell membrane damage and lipid peroxidation under the condition of hypoxia-reoxygenation: analysis of the mechanism using antioxidants and electron transport inhibitors Cell Biochem. Funct. 27 2009 338 343
46. M.C. Howland, and A.N. Parikh Model studies of membrane disruption by photogenerated oxidative assault J. Phys. Chem. B 114 2010 6377 6385
47. H.L. Smith, M.C. Howland, A.W. Szmodis, Q. Li, L.L. Daemen, A.N. Parikh, and J. Majewski Early stages of oxidative stress-induced membrane permeabilization: a neutron reflectometry study J. Am. Chem. Soc. 131 2009 3631 3638
48. S. Akiba, R. Nagatomo, M. Hayama, and T. Sato Lipid peroxide overcomes the inability of platelet secretory phospholipase A2 to hydrolyze membrane phospholipids in rabbit platelets J. Biochem. Tokyo 122 1997 859 864 (Pubitemid 27474958)
49. A.A. Korotaeva, E.V. Samoilova, A.A. Pirkova, and N.V. Prokazova The effect of LDL on the activity of proinflammatory secretory phospholipase A2 (IIA) depends on the degree of their oxidation Ross. Fiziol. Zh. Im. I. M. Sechenova 95 2009 476 483
50. A.A. Korotaeva, E.V. Samoilova, A.A. Pirkova, V.A. Ameliushkina, N.V. Prokazova, V.A. Tkachuk, and E.I. Chazov Opposite effects of native and oxidized lipoproteins on the activity of secretory phospholipase A(2) group IIA Prostaglandins Other Lipid Mediat. 90 2009 37 41
51. A.A. Korotaeva, E.V. Samoilova, G.F. Piksina, and N.V. Prokazova Oxidized phosphatidylcholine stimulates activity of secretory phospholipase A2 group IIA and abolishes sphingomyelin-induced inhibition of the enzyme Prostaglandins Other Lipid Mediat. 91 2010 38 41
52. L.R. McLean, K.A. Hagaman, and W.S. Davidson Role of lipid structure in the activation of phospholipase A2 by peroxidized phospholipids Lipids 28 1993 505 509 (Pubitemid 23177647)
53. D. Marsh, A. Watts, and P.F. Knowles Evidence for phase boundary lipid. Permeability of tempo-choline into dimyristoylphosphatidylcholine vesicles at the phase transition Biochemistry 15 1976 3570 3578
54. E. Freire, and R. Biltonen Estimation of molecular averages and equilibrium fluctuations in lipid bilayer systems from the excess heat capacity function Biochim. Biophys. Acta 514 1978 54 68 (Pubitemid 9061071)
55. H.A. Wilson-Ashworth, A.M. Judd, R.M. Law, B.D. Freestone, S. Taylor, M.K. Mizukawa, K.R. Cromar, S. Sudweeks, and J.D. Bell Formation of transient non-protein calcium pores by lysophospholipids in S49 Lymphoma cells J. Membr. Biol. 200 2004 25 33 (Pubitemid 39180535)
56. D.W. Deamer, and J. Bramhall Permeability of lipid bilayers to water and ionic solutes Chem. Phys. Lipids 40 2006 167 188
57. B. Apellaniz, J.L. Nieva, P. Schwille, and A.J. Garcia-Saez All-or-none versus graded: single-vesicle analysis reveals lipid composition effects on membrane permeabilization Biophys. J. 99 2010 3619 3628
58. H.A. Wilson-Ashworth, Q. Bahm, J. Erickson, A. Shinkle, M.P. Vu, D. Woodbury, and J.D. Bell Differential detection of phospholipid fluidity, order, and spacing by fluorescence spectroscopy of bis-pyrene, prodan, nystatin, and merocyanine 540 Biophys. J. 91 2006 4091 4101 (Pubitemid 44887269)
59. F.B. Chekeni, M.R. Elliott, J.K. Sandilos, S.F. Walk, J.M. Kinchen, E.R. Lazarowski, A.J. Armstrong, S. Penuela, D.W. Laird, G.S. Salvesen, B.E. Isakson, D.A. Bayliss, and K.S. Ravichandran Pannexin 1 channels mediate "find-me" signal release and membrane permeability during apoptosis Nature 467 2010 863 867
60. F.B. Chekeni, and K.S. Ravichandran The role of nucleotides in apoptotic cell clearance: implications for disease pathogenesis J. Mol. Med. 89 2011 13 22
61. C. Peter, S. Wesselborg, and K. Lauber Apoptosis: opening PANdora's BoX Curr. Biol. 20 2010 R940 R942
62. C. Peter, S. Wesselborg, M. Herrmann, and K. Lauber Dangerous attraction: phagocyte recruitment and danger signals of apoptotic and necrotic cells Apoptosis 15 2010 1007 1028
63. C. Peter, S. Wesselborg, and K. Lauber Molecular suicide notes: last call from apoptosing cells J. Mol. Cell Biol. 2 2010 78 80
64. M.K. Callahan, P. Williamson, and R.A. Schlegel Surface expression of phosphatidylserine on macrophages is required for phagocytosis of apoptotic thymocytes Cell Death Differ. 7 2000 645 653 (Pubitemid 30456170)
65. B. Fadeel Plasma membrane alterations during apoptosis: role in corpse clearance Antioxid. Redox Signal. 6 2004 269 275 (Pubitemid 38332584)
66. S. Krahling, M.K. Callahan, P. Williamson, and R.A. Schlegel Exposure of phosphatidylserine is a general feature in the phagocytosis of apoptotic lymphocytes by macrophages Cell Death Differ. 6 1999 183 189 (Pubitemid 29082307)
67. B. Verhoven, R.A. Schlegel, and P. Williamson Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes J. Exp. Med. 182 1995 1597 1601
68. R.B. Mueller, A. Sheriff, U.S. Gaipl, S. Wesselborg, and K. Lauber Attraction of phagocytes by apoptotic cells is mediated by lysophosphatidylcholine Autoimmunity 40 2007 342 344 (Pubitemid 46845536)
69. K. Lauber, E. Bohn, S.M. Krober, Y.J. Xiao, S.G. Blumenthal, R.K. Lindemann, P. Marini, C. Wiedig, A. Zobywalski, S. Baksh, Y. Xu, I.B. Autenrieth, K. Schulze-Osthoff, C. Belka, G. Stuhler, and S. Wesselborg Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal Cell 113 2003 717 730 (Pubitemid 36724936)
70. C. Peter, M. Waibel, C.G. Radu, L.V. Yang, O.N. Witte, K. Schulze-Osthoff, S. Wesselborg, and K. Lauber Migration to apoptotic "find-me" signals is mediated via the phagocyte receptor G2A J. Biol. Chem. 283 2008 5296 5305