Amyloid-β peptide induces temporal membrane biphasic changes in astrocytes through cytosolic phospholipase A2

Biochimica et Biophysica Acta - Biomembranes

Volumn 1778, Issue 11, 2008, Pages 2512-2519

  Hicks, Jacob B ^a   Lai, Yinzhi ^a   Sheng, Wenwen ^b   Yang, Xiaoguang ^a   Zhu, Donghui ^a   Sun, Grace Y ^b   Lee, James C M ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

Alzheimer; Amyloid beta peptide; Astrocytes; NADPH oxidase; Phospholipase

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; APOCYNIN; CELL ENZYME; LYSOPHOSPHATIDYLCHOLINE; PHOSPHOLIPASE A2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ANIMAL CELL; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CYTOSOL; MEMBRANE BIOLOGY; MEMBRANE STRUCTURE; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

AMYLOID BETA-PROTEIN; ANIMALS; ASTROCYTES; CELL MEMBRANE; ENZYME INHIBITORS; HYDROLYSIS; MEMBRANES, ARTIFICIAL; NADPH OXIDASE; PHASE TRANSITION; PHOSPHOLIPASES A2, CYTOSOLIC; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; RATS; SUPEROXIDES; TISSUE EXTRACTS;

RATTUS;

EID: 54049089921     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2008.07.027     Document Type: Article

References (67)

1. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 298 (2002) 789-791
2. Ashley R.H., Harroun T.A., Hauss T., Breen K.C., and Bradshaw J.P. Autoinsertion of soluble oligomers of Alzheimer's Abeta(1-42) peptide into cholesterol-containing membranes is accompanied by relocation of the sterol towards the bilayer surface. BMC Struct. Biol. 6 (2006) 21
3. Arispe N., Rojas E., and Pollard H.B. Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 567-571
4. Hartmann H., Eckert A., and Muller W.E. Apolipoprotein E and cholesterol affect neuronal calcium signalling: the possible relationship to beta-amyloid neurotoxicity. Biochem. Biophys. Res. Commun. 200 (1994) 1185-1192
5. McLaurin J., and Chakrabartty A. Membrane disruption by Alzheimer beta-amyloid peptides mediated through specific binding to either phospholipids or gangliosides. Implications for neurotoxicity. J. Biol. Chem. 271 (1996) 26482-26489
6. Sultana R., and Butterfield D.A. Alterations of some membrane transport proteins in Alzheimer's disease: role of amyloid beta-peptide. Mol. Biosyst. 4 (2008) 36-41
7. Hashimoto M., Hossain S., Shimada T., and Shido O. Docosahexaenoic acid-induced protective effect against impaired learning in amyloid beta-infused rats is associated with increased synaptosomal membrane fluidity. Clin. Exp. Pharmacol. Physiol. 33 (2006) 934-939
8. Dennis E.A. Diversity of group types, regulation, and function of phospholipase A2. J. Biol. Chem. 269 (1994) 13057-13060
9. Balsinde J., Balboa M.A., Insel P.A., and Dennis E.A. Regulation and inhibition of phospholipase A2. Annu. Rev. Pharmacol. Toxicol. 39 (1999) 175-189
10. Murakami M., and Kudo I. Phospholipase A2. J. Biochem. (Tokyo) 131 (2002) 285-292
11. Farooqui A.A., and Horrocks L.A. Phospholipase A2-generated lipid mediators in the brain: the good, the bad, and the ugly. Neuroscientist 12 (2006) 245-260
12. Forlenza O.V., Schaeffer E.L., and Gattaz W.F. The role of phospholipase A2 in neuronal homeostasis and memory formation: implications for the pathogenesis of Alzheimer's disease. J. Neural. Transm. 114 (2007) 231-238
13. Stephenson D., Rash K., Smalstig B., Roberts E., Johnstone E., Sharp J., Panetta J., Little S., Kramer R., and Clemens J. Cytosolic phospholipase A2 is induced in reactive glia following different forms of neurodegeneration. Glia 27 (1999) 110-128
14. Farooqui A.A., Ong W.Y., and Horrocks L.A. Plasmalogens, docosahexaenoic acid, and neurological disorders. In: Roels F., Baes M., and de Bies S. (Eds). Peroxisomal disorders and regulation of genes (2003), Kluwer Academic/Plenum, London 335-354
15. Farooqui A.A., Ong W.Y., and Horrocks L.A. Stimulation of lipases and phospholipases in Alzheimer disease. In: Szuhaj B., and van Nieuwenhuyzen W. (Eds). Nutrition and biochemistry of phospholipids (2003), AOCS, Champaign, IL 14-29
16. Hibbeln J.R., Palmer J.W., and Davis J.M. Are disturbances in lipid-protein interactions by phospholipase-A2 a predisposing factor in affective illness?. Biol. Psychiatry. 25 (1989) 945-961
17. Zhu D., Lai Y., Shelat P.B., Hu C., Sun G.Y., and Lee J.C. Phospholipases A2 mediate amyloid-beta peptide-induced mitochondrial dysfunction. J. Neurosci. 26 (2006) 11111-11119
18. Dahlgren K.N., Manelli A.M., Stine Jr. W.B., Baker L.K., Krafft G.A., and LaDu M.J. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 277 (2002) 32046-32053
19. Zhang J.P., and Sun G.Y. Free fatty acids, neutral glycerides, and phosphoglycerides in transient focal cerebral ischemia. J. Neurochem. 64 (1995) 1688-1695
20. Lee J.C., Bermudez H., Discher B.M., Sheehan M.A., Won Y.Y., Bates F.S., and Discher D.E. Preparation, stability, and in vitro performance of vesicles made with diblock copolymers. Biotechnol. Bioeng. 73 (2001) 135-145
21. Parasassi T., Gratton E., Yu W.M., Wilson P., and Levi M. Two-photon fluorescence microscopy of laurdan generalized polarization domains in model and natural membranes. Biophys. J. 72 (1997) 2413-2429
22. Parasassi T., Di Stefano M., Ravagnan G., Sapora O., and Gratton E. Membrane aging during cell growth ascertained by Laurdan generalized polarization. Exp. Cell Res. 202 (1992) 432-439
23. Lee J.C.-M., Law R.J., and Discher D.E. Bending contributions hydration of phospholipid and block copolymer membranes: Unifying correlations between probe fluorescence and vesicle thermoelasticity. Langmuir 17 (2001) 3592-3597
24. Zhu D., Tan K.S., Zhang X., Sun A.Y., Sun G.Y., and Lee J.C. Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. J. Cell. Sci. 118 (2005) 3695-3703
25. Chapman K.E., Sinclair S.E., Zhuang D., Hassid A., Desai L.P., and Waters C.M. Cyclic mechanical strain increases reactive oxygen species production in pulmonary epithelial cells. Am. J. Physiol. Lung. Cell Mol. Physiol. 289 (2005) L834-841
26. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
27. Parasassi T., De Stasio G., d'Ubaldo A., and Gratton E. Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys. J. 57 (1990) 1179-1186
28. Parasassi T., Giusti A.M., Gratton E., Monaco E., Raimondi M., Ravagnan G., and Sapora O. Evidence for an increase in water concentration in bilayers after oxidative damage of phospholipids induced by ionizing radiation. Int. J. Radiat. Biol. 65 (1994) 329-334
29. Parasassi T., Ravagnan G., Rusch R.M., and Gratton E. Modulation and dynamics of phase properties in phospholipid mixtures detected by Laurdan fluorescence. Photochem. Photobiol. 57 (1993) 403-410
30. Waschuk S.A., Elton E.A., Darabie A.A., Fraser P.E., and McLaurin J.A. Cellular membrane composition defines A beta-lipid interactions. J. Biol. Chem. 276 (2001) 33561-33568
31. Stolk J., Hiltermann T.J., Dijkman J.H., and Verhoeven A.J. Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol. Am. J. Respir. Cell Mol. Biol. 11 (1994) 95-102
32. Eckert G.P., Cairns N.J., Maras A., Gattaz W.F., and Muller W.E. Cholesterol modulates the membrane-disordering effects of beta-amyloid peptides in the hippocampus: specific changes in Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 11 (2000) 181-186
33. Abramov A.Y., Jacobson J., Wientjes F., Hothersall J., Canevari L., and Duchen M.R. Expression and modulation of an NADPH oxidase in mammalian astrocytes. J. Neurosci. 25 (2005) 9176-9184
34. Gaus K., Gratton E., Kable E.P., Jones A.S., Gelissen I., Kritharides L., and Jessup W. Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15554-15559
35. Dietrich C., Bagatolli L.A., Volovyk Z.N., Thompson N.L., Levi M., Jacobson K., and Gratton E. Lipid rafts reconstituted in model membranes. Biophys. J. 80 (2001) 1417-1428
36. Bagatolli L.A., and Gratton E. Two-photon fluorescence microscopy observation of shape changes at the phase transition in phospholipid giant unilamellar vesicles. Biophys. J. 77 (1999) 2090-2101
37. Bagatolli L.A., and Gratton E. A correlation between lipid domain shape and binary phospholipid mixture composition in free standing bilayers: A two-photon fluorescence microscopy study. Biophys. J. 79 (2000) 434-447
38. Dinnes D.L., Santerre J.P., and Labow R.S. Intracellular phospholipase A2 expression and location in human macrophages: influence of synthetic material surface chemistry. J. Cell. Physiol. 214 (2008) 136-144
39. Harris F.M., Smith S.K., and Bell J.D. Physical properties of erythrocyte ghosts that determine susceptibility to secretory phospholipase A2. J. Biol. Chem. 276 (2001) 22722-22731
40. Dave J.R., Knazek R.A., and Liu S.C. Arachidonic acid, bradykinin and phospholipase A2 modify both prolactin binding capacity and fluidity of mouse hepatic membranes. Biochem. Biophys. Res. Commun. 103 (1981) 727-738
41. Schaeffer E.L., Bassi Jr. F., and Gattaz W.F. Inhibition of phospholipase A2 activity reduces membrane fluidity in rat hippocampus. J. Neural. Transm. 112 (2005) 641-647
42. Kameyama Y., Kudo S., Ohki K., and Nozawa Y. Differential inhibitory effects by phospholipase A2 on guanylate and adenylate cyclases of Tetrahymena plasma membranes. Jpn. J. Exp. Med. 52 (1982) 183-192
43. Selkoe D.J. The ups and downs of Abeta. Nat. Med. 12 (2006) 758-759 discussion 759
44. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., and Klein W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 6448-6453
45. Mattson M.P., Cheng B., Davis D., Bryant K., Lieberburg I., and Rydel R.E. beta-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 12 (1992) 376-389
46. Demuro A., Mina E., Kayed R., Milton S.C., Parker I., and Glabe C.G. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 280 (2005) 17294-17300
47. Gibson Wood W., Eckert G.P., Igbavboa U., and Muller W.E. Amyloid beta-protein interactions with membranes and cholesterol: causes or casualties of Alzheimer's disease. Biochim. Biophys. Acta. 1610 (2003) 281-290
48. Muller W.E., Eckert G.P., Scheuer K., Cairns N.J., Maras A., and Gattaz W.F. Effects of beta-amyloid peptides on the fluidity of membranes from frontal and parietal lobes of human brain. High potencies of A beta 1-42 and A beta 1-43. Amyloid 5 (1998) 10-15
49. Yip C.M., Elton E.A., Darabie A.A., Morrison M.R., and McLaurin J. Cholesterol, a modulator of membrane-associated Abeta-fibrillogenesis and neurotoxicity. J. Mol. Biol. 311 (2001) 723-734
50. Avdulov N.A., Chochina S.V., Igbavboa U., O'Hare E.O., Schroeder F., Cleary J.P., and Wood W.G. Amyloid beta-peptides increase annular and bulk fluidity and induce lipid peroxidation in brain synaptic plasma membranes. J. Neurochem. 68 (1997) 2086-2091
51. Chochina S.V., Avdulov N.A., Igbavboa U., Cleary J.P., O'Hare E.O., and Wood W.G. Amyloid beta-peptide1-40 increases neuronal membrane fluidity: role of cholesterol and brain region. J. Lipid. Res. 42 (2001) 1292-1297
52. Kremer J.J., Pallitto M.M., Sklansky D.J., and Murphy R.M. Correlation of beta-amyloid aggregate size and hydrophobicity with decreased bilayer fluidity of model membranes. Biochemistry 39 (2000) 10309-10318
53. Mason R.P., Jacob R.F., Walter M.F., Mason P.E., Avdulov N.A., Chochina S.V., Igbavboa U., and Wood W.G. Distribution and fluidizing action of soluble and aggregated amyloid beta-peptide in rat synaptic plasma membranes. J. Biol. Chem. 274 (1999) 18801-18807
54. Nunomura A., Perry G., Aliev G., Hirai K., Takeda A., Balraj E.K., Jones P.K., Ghanbari H., Wataya T., Shimohama S., Chiba S., Atwood C.S., Petersen R.B., and Smith M.A. Oxidative damage is the earliest event in Alzheimer disease. J. Neuropathol. Exp. Neurol. 60 (2001) 759-767
55. Abramov A.Y., Canevari L., and Duchen M.R. Beta-amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J. Neurosci. 24 (2004) 565-575
56. 2 to plasma membranes mediated by the NADPH oxidase in phagocytes. J. Cell. Biol. 162 (2003) 683-692
57. 2. J. Hypertens. 23 (2005) 1183-1190
58. 2 for stimulation of NADPH oxidase-associated diaphorase activity in granulocyte-like cells. J. Biol. Chem. 276 (2001) 33495-33503
59. 2 for activation of the phagocyte NADPH oxidase. J. Biol. Chem. 273 (1998) 441-445
60. +channel in phagocyte-like cells. Adv. Exp. Med. Biol. 479 (2000) 125-135
61. phox. J. Biol. Chem. 277 (2002) 25385-25392
62. Levy R. The role of cytosolic phospholipase A2-alfa in regulation of phagocytic functions. Biochim. Biophys. Acta. 1761 (2006) 1323-1334
63. Radany E.H., Brenner M., Besnard F., Bigornia V., Bishop J.M., and Deschepper C.F. Directed establishment of rat brain cell lines with the phenotypic characteristics of type 1 astrocytes. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 6467-6471
64. Yip C.M., Darabie A.A., and McLaurin J. Abeta42-peptide assembly on lipid bilayers. J. Mol. Biol. 318 (2002) 97-107
65. Wilson H.A., Huang W., Waldrip J.B., Judd A.M., Vernon L.P., and Bell J.D. Mechanisms by which thionin induces susceptibility of S49 cell membranes to extracellular phospholipase A2. Biochim. Biophys. Acta. 1349 (1997) 142-156
66. Janson J., Ashley R.H., Harrison D., McIntyre S., and Butler P.C. The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes 48 (1999) 491-498
67. Janciauskiene S., and Ahren B. Fibrillar islet amyloid polypeptide differentially affects oxidative mechanisms and lipoprotein uptake in correlation with cytotoxicity in two insulin-producing cell lines. Biochem. Biophys. Res. Commun. 267 (2000) 619-625