Loss of phospholipid asymmetry and elevated brain apoptotic protein levels in subjects with amnestic mild cognitive impairment and Alzheimer disease

Neurobiology of Disease

Volumn 29, Issue 3, 2008, Pages 456-464

  Bader Lange, Miranda L ^a   Cenini, Giovanna ^a,b   Piroddi, Marta ^a,c   Mohmmad Abdul, Hafiz ^a   Sultana, Rukhsana ^a   Galli, Francesco ^c   Memo, Maurizio ^b   Butterfield, D Allan ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF BRESCIA   (Italy)

^c UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Alzheimer disease (AD); Apoptosis; Bax; Bcl 2; Caspase 3; Mild cognitive impairment (MCI); Oxidative stress; Phosphatidylserine (PtdSer); Phospholipid asymmetry

Indexed keywords

CASPASE 3; PHOSPHATIDYLSERINE; PHOSPHOLIPID; PROTEIN BAX; PROTEIN BCL 2;

AGED; ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; FLUORESCENCE; HUMAN; HUMAN TISSUE; LIPID BILAYER; LIPID PEROXIDATION; MALE; MEMBRANE LEAFLET; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTOSOME; WESTERN BLOTTING;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMNESIA; ANIMALS; APOPTOSIS; BRAIN; COGNITION DISORDERS; FEMALE; HUMANS; LONGITUDINAL STUDIES; MALE; MICE; OXIDATIVE STRESS; PHOSPHATIDYLSERINES; PHOSPHOLIPIDS;

EID: 39249083317     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2007.11.004     Document Type: Article

References (75)

1. Albrecht S., Bourdeau M., Bennett D., Mufson E.J., Bhattacharjee M., and LeBlanc A.C. Activation of caspase-6 in aging and mild cognitive impairment. Am. J. Pathol. 170 (2007) 1200-1209
2. Auland M.E., Roufogalis B.D., Devaux P.F., and Zachowski A. Reconstitution of ATP-dependent aminophospholipid translocation in proteoliposomes. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 10938-10942
3. Balasubramanian K., and Schroit A.J. Aminophospholipid asymmetry: a matter of life and death. Annu. Rev. Physiol. 65 (2003) 701-734
4. Bitbol M., Fellmann P., Zachowski A., and Devaux P.F. Ion regulation of phosphatidylserine and phosphatidylethanolamine outside-inside translocation in human erythrocytes. Biochim. Biophys. Acta 904 (1987) 268-282
5. Bruce-Keller A.J., Begley J.G., Fu W., Butterfield D.A., Bredesen D.E., Hutchins J.B., Hensley K., and Mattson M.P. Bcl-2 protects isolated plasma and mitochondrial membranes against lipid peroxidation induced by hydrogen peroxide and amyloid beta-peptide. J. Neurochem. 70 (1998) 31-39
6. Butterfield D.A., and Lauderback C.M. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid b-peptide-associated free radical oxidative stress. Free Radic. Biol. Med. 32 (2002) 1050-1060
7. Butterfield D.A., Drake J., Pocernich C., and Castegna A. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid b-peptide. Trends Mol. Med. 7 (2001) 548-554
8. Butterfield D.A., Castegna A., Lauderback C.M., and Drake J. Evidence that amyloid β-peptide-induced lipid peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death. Neurobiol. Aging 23 (2002) 655-664
9. Butterfield D.A., Reed T., Perluigi M., De Marco C., Coccia R., Cini C., and Sultana R. Elevated protein-bound levels of the lipid peroxidation product, 4-hydroxy-2-nonenal, in brain from persons with mild cognitive impairment. Neurosci. Lett. 397 (2006) 170-173
10. Butterfield D.A., Poon H.F., St Clair D., Keller J.N., Pierce W.M., Klein J.B., and Markesbery W.R. Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer's disease. Neurobiol. Dis. 22 (2006) 223-232
11. Butterfield D.A., Reed T.T., Perluigi M., De Marco C., Coccia R., Keller J.N., Markesbery W.R., and Sultana R. Elevated levels of 3-nitrotyrosine in brain from subjects with amnestic mild cognitive impairment: implications for the role of nitration in the progression of Alzheimer's disease. Brain Res. 1148 (2007) 243-248
12. Castegna A., Lauderback C.M., Mohmmad-Abdul H., and Butterfield D.A. Modulation of phospholipid asymmetry in synaptosomal membranes by the lipid peroxidation products, 4-hydroxynonenal and acrolein: implications for Alzheimer's disease. Brain Res. 1004 (2004) 193-197
13. Castren E., Ohga Y., Berzaghi M.P., Tzimagiorgis G., Thoenen H., and Lindholm D. Bcl-2 messenger RNA is localized in neurons of the developing and adult rat brain. Neuroscience 61 (1994) 165-177
14. Comfurius P., Williamson P., Smeets E.F., Schlegel R.A., Bevers E.M., and Zwaal R.F. Reconstitution of phospholipid scramblase activity from human blood platelets. Biochemistry 35 (1996) 7631-7634
15. Cotman C.W., and Anderson A.J. A potential role for apoptosis in neurodegeneration and Alzheimer's disease. Mol. Neurobiol. 10 (1995) 19-45
16. Cras P., Smith M.A., Richey P.L., Siedlak S.L., Mulvihill P., and Perry G. Extracellular neurofibrillary tangles reflect neuronal loss and provide further evidence of extensive protein cross-linking in Alzheimer disease. Acta Neuropathol. (Berl.) 89 (1995) 291-295
17. Daleke D.L. Regulation of transbilayer plasma membrane phospholipid asymmetry. J. Lipid Res. 44 (2003) 233-242
18. Daleke D.L., and Lyles J.V. Identification and purification of aminophospholipid flippases. Biochim. Biophys. Acta 1486 (2000) 108-127
19. Drake J., Link C.D., and Butterfield D.A. Oxidative stress precedes fibrillar deposition of Alzheimer's disease amyloid β-peptide (1-42) in a transgenic Caenorhabditis elegans model. Neurobiol. Aging 24 (2003) 415-420
20. Eckert G.P., Kirsch C., Leutz S., Wood W.G., and Muller W.E. Cholesterol modulates amyloid b-peptide's membrane interactions. Pharmacopsychiatry 36 Suppl 2 (2003) S136-S143
21. Engidawork E., Gulesserian T., Seidl R., Cairns N., and Lubec G. Expression of apoptosis related proteins in brains of patients with Alzheimer's disease. Neurosci. Lett. 303 (2001) 79-82
22. Fabisiak J.P., Kagan V.E., Ritov V.B., Johnson D.E., and Lazo J.S. Bcl-2 inhibits selective oxidation and externalization of phosphatidylserine during paraquat-induced apoptosis. Am. J. Physiol. 272 (1997) C675-C684
23. Fadok V.A., Voelker D.R., Campbell P.A., Cohen J.J., Bratton D.L., and Henson P.M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148 (1992) 2207-2216
24. Fadok V.A., de Cathelineau A., Daleke D.L., Henson P.M., and Bratton D.L. Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. J. Biol. Chem. 276 (2001) 1071-1077
25. Geddes J.W., Chang-Chui H., Cooper S.M., Lott I.T., and Cotman C.W. Density and distribution of NMDA receptors in the human hippocampus in Alzheimer's disease. Brain Res. 399 (1986) 156-161
26. Giannakopoulos P., Kovari E., Savioz A., de Bilbao F., Dubois-Dauphin M., Hof P.R., and Bouras C. Differential distribution of presenilin-1, Bax, and Bcl-X(L) in Alzheimer's disease and frontotemporal dementia. Acta Neuropathol. (Berl.). 98 (1999) 141-149
27. Herrmann A., and Devaux P.F. Alteration of the aminophospholipid translocase activity during in vivo and artificial aging of human erythrocytes. Biochim. Biophys. Acta 1027 (1990) 41-46
28. Honig L.S., and Rosenberg R.N. Apoptosis and neurologic disease. Am. J. Med. 108 (2000) 317-330
29. Kagan V.E., Fabisiak J.P., Shvedova A.A., Tyurina Y.Y., Tyurin V.A., Schor N.F., and Kawai K. Oxidative signaling pathway for externalization of plasma membrane phosphatidylserine during apoptosis. FEBS Lett. 477 (2000) 1-7
30. Kagan V.E., Gleiss B., Tyurina Y.Y., Tyurin V.A., Elenstrom-Magnusson C., Liu S.X., Serinkan F.B., Arroyo A., Chandra J., Orrenius S., and Fadeel B. A role for oxidative stress in apoptosis: oxidation and externalization of phosphatidylserine is required for macrophage clearance of cells undergoing Fas-mediated apoptosis. J. Immunol. 169 (2002) 487-499
31. Kagan V.E., Borisenko G.G., Serinkan B.F., Tyurina Y.Y., Tyurin V.A., Jiang J., Liu S.X., Shvedova A.A., Fabisiak J.P., Uthaisang W., and Fadeel B. Appetizing rancidity of apoptotic cells for macrophages: oxidation, externalization, and recognition of phosphatidylserine. Am. J. Physiol., Lung Cell. Mol. Physiol. 285 (2003) L1-L17
32. Keller J.N., Hanni K.B., and Markesbery W.R. Impaired proteasome function in Alzheimer's disease. J. Neurochem. 75 (2000) 436-439
33. Keller J.N., Schmitt F.A., Scheff S.W., Ding Q., Chen Q., Butterfield D.A., and Markesbery W.R. Evidence of increased oxidative damage in subjects with mild cognitive impairment. Neurology 64 (2005) 1152-1156
34. Kitamura Y., Shimohama S., Kamoshima W., Ota T., Matsuoka Y., Nomura Y., Smith M.A., Perry G., Whitehouse P.J., and Taniguchi T. Alteration of proteins regulating apoptosis, Bcl-2, Bcl-x, Bax, Bak, Bad, ICH-1 and CPP32, in Alzheimer's disease. Brain Res. 780 (1998) 260-269
35. Klein W.L. Synaptic targeting by Aβ oligomers (ADDLS) as a basis for memory loss in early Alzheimer's disease. Alzheimer's & Dementia 2 (2006) 43-55
36. Lopez-Revuelta A., Sanchez-Gallego J.I., Garcia-Montero A.C., Hernandez-Hernandez A., Sanchez-Yague J., and Llanillo M. Membrane cholesterol in the regulation of aminophospholipid asymmetry and phagocytosis in oxidized erythrocytes. Free Radic. Biol. Med. 42 (2007) 1106-1118
37. Lovell M.A., Xie C., and Markesbery W.R. Acrolein is increased in Alzheimer's disease brain and is toxic to primary hippocampal cultures. Neurobiol. Aging 22 (2001) 187-194
38. MacGibbon G.A., Lawlor P.A., Sirimanne E.S., Walton M.R., Connor B., Young D., Williams C., Gluckman P., Faull R.L., Hughes P., and Dragunow M. Bax expression in mammalian neurons undergoing apoptosis, and in Alzheimer's disease hippocampus. Brain Res. 750 (1997) 223-234
39. Mandal D., Moitra P.K., Saha S., and Basu J. Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes. FEBS Lett. 513 (2002) 184-188
40. Mandal D., Mazumder A., Das P., Kundu M., and Basu J. Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J. Biol. Chem. 280 (2005) 39460-39467
41. Markesbery W.R., and Lovell M.A. 4-Hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol. Aging 19 (1998) 33-36
42. Markesbery W.R., Kryscio R.J., Lovell M.A., and Morrow J.D. Lipid peroxidation is an early event in the brain in amnestic mild cognitive impairment. Ann. Neurol. 58 (2005) 730-735
43. Martin S.J., Finucane D.M., Amarante-Mendes G.P., O'Brien G.A., and Green D.R. Phosphatidylserine externalization during CD95-induced apoptosis of cells and cytoplasts requires ICE/CED-3 protease activity. J. Biol. Chem. 271 (1996) 28753-28756
44. McKhann G., Drachman D., Folstein M., Katzman R., Price D., and Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34 (1984) 939-944
45. Mohmmad Abdul H., and Butterfield D.A. Protection against amyloid b-peptide (1-42)-induced loss of phospholipid asymmetry in synaptosomal membranes by tricyclodecan-9-xanthogenate (D609) and ferulic acid ethyl ester (FAEE): implications for Alzheimer's disease. Biochim. Biophys. Acta 1741 (2005) 140-148
46. 2 and kainic acid: implications for Alzheimer's disease. J. Neurochem. 96 (2006) 1322-1335
47. Nagy Z.S., and Esiri M.M. Apoptosis-related protein expression in the hippocampus in Alzheimer's disease. Neurobiol. Aging 18 (1997) 565-571
48. Nicholson D.W. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ. 6 (1999) 1028-1042
49. Nicholson D.W., Ali A., Thornberry N.A., Vaillancourt J.P., Ding C.K., Gallant M., Gareau Y., Griffin P.R., Labelle M., Lazebnik Y.A., et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376 (1995) 37-43
50. Oltvai Z.N., Milliman C.L., and Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog Bax, that accelerates programmed cell death. Cell 74 (1993) 609-619
51. Ott M., Gogvadze V., Orrenius S., and Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis 12 (2007) 913-922
52. Paulusma C.C., and Oude Elferink R.P. The type 4 subfamily of P-type ATPases, putative aminophospholipid translocases with a role in human disease. Biochim. Biophys. Acta 1741 (2005) 11-24
53. Pellegrini M., and Strasser A. A portrait of the Bcl-2 protein family: life, death, and the whole picture. J. Clin. Immunol. 19 (1999) 365-377
54. Petersen R.C., Smith G.E., Waring S.C., Ivnik R.J., Tangalos E.G., and Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Arch. Neurol. 56 (1999) 303-308
55. Prasad M.R., Lovell M.A., Yatin M., Dhillon H., and Markesbery W.R. Regional membrane phospholipid alterations in Alzheimer's disease. Neurochem. Res. 23 (1998) 81-88
56. Sadrzadeh S.M., Vincenzi F.F., and Hinds T.R. Simultaneous measurement of multiple membrane ATPases in microtiter plates. J. Pharmacol. Toxicol. Methods 30 (1993) 103-110
57. Satou T., Cummings B.J., and Cotman C.W. Immunoreactivity for Bcl-2 protein within neurons in the Alzheimer's disease brain increases with disease severity. Brain Res. 697 (1995) 35-43
58. Schwab C., Bondada V., Sparks D.L., Cahan L.D., and Geddes J.W. Postmortem changes in the levels and localization of microtubule-associated proteins (tau, MAP2 and MAP1B) in the rat and human hippocampus. Hippocampus 4 (1994) 210-225
59. Shimohama S. Apoptosis in Alzheimer's disease-an update. Apoptosis 5 (2000) 9-16
60. Smale G., Nichols N.R., Brady D.R., Finch C.E., and Horton Jr. W.E. Evidence for apoptotic cell death in Alzheimer's disease. Exp. Neurol. 133 (1995) 225-230
61. Su J.H., Anderson A.J., Cummings B.J., and Cotman C.W. Immunohistochemical evidence for apoptosis in Alzheimer's disease. NeuroReport 5 (1994) 2529-2533
62. Su J.H., Satou T., Anderson A.J., and Cotman C.W. Up-regulation of Bcl-2 is associated with neuronal DNA damage in Alzheimer's disease. NeuroReport 7 (1996) 437-440
63. Su J.H., Nichol K.E., Sitch T., Sheu P., Chubb C., Miller B.L., Tomaselli K.J., Kim R.C., and Cotman C.W. DNA damage and activated caspase-3 expression in neurons and astrocytes: evidence for apoptosis in frontotemporal dementia. Exp. Neurol. 163 (2000) 9-19
64. Su J.H., Zhao M., Anderson A.J., Srinivasan A., and Cotman C.W. Activated caspase-3 expression in Alzheimer's and aged control brain: correlation with Alzheimer pathology. Brain Res. 898 (2001) 350-357
65. Sultana R., Boyd-Kimball D., Poon H.F., Cai J., Pierce W.M., Klein J.B., Merchant M., Markesbery W.R., and Butterfield D.A. Redox proteomics identification of oxidized proteins in Alzheimer's disease hippocampus and cerebellum: an approach to understand pathological and biochemical alterations in AD. Neurobiol. Aging 27 (2006) 1564-1576
66. Tang X., Halleck M.S., Schlegel R.A., and Williamson P. A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 272 (1996) 1495-1497
67. Tortosa A., Lopez E., and Ferrer I. Bcl-2 and Bax protein expression in Alzheimer's disease. Acta Neuropathol. (Berl.). 95 (1998) 407-412
68. Tyurina Y.Y., Serinkan F.B., Tyurin V.A., Kini V., Yalowich J.C., Schroit A.J., Fadeel B., and Kagan V.E. Lipid antioxidant, etoposide, inhibits phosphatidylserine externalization and macrophage clearance of apoptotic cells by preventing phosphatidylserine oxidation. J. Biol. Chem. 279 (2004) 6056-6064
69. Tyurina Y.Y., Tyurin V.A., Zhao Q., Djukic M., Quinn P.J., Pitt B.R., and Kagan V.E. Oxidation of phosphatidylserine: a mechanism for plasma membrane phospholipid scrambling during apoptosis?. Biochem. Biophys. Res. Commun. 324 (2004) 1059-1064
70. Vanags D.M., Porn-Ares M.I., Coppola S., Burgess D.H., and Orrenius S. Protease involvement in fodrin cleavage and phosphatidylserine exposure in apoptosis. J. Biol. Chem. 271 (1996) 31075-31085
71. Verkleij A.J., and Post J.A. Membrane phospholipid asymmetry and signal transduction. J. Membr. Biol. 178 (2000) 1-10
72. Winblad B., Palmer K., Kivipelto M., Jelic V., Fratiglioni L., Wahlund L.O., Nordberg A., Backman L., Albert M., Almkvist O., Arai H., Basun H., Blennow K., de Leon M., DeCarli C., Erkinjuntti T., Giacobini E., Graff C., Hardy J., Jack C., Jorm A., Ritchie K., van Duijn C., Visser P., and Petersen R.C. Mild cognitive impairment-beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J. Intern. Med. 256 (2004) 240-246
73. Wolf B.B., and Green D.R. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J. Biol. Chem. 274 (1999) 20049-20052
74. Wood W.G., Schroeder F., Igbavboa U., Avdulov N.A., and Chochina S.V. Brain membrane cholesterol domains, aging and amyloid b-peptides. Neurobiol. Aging 23 (2002) 685-694
75. Wood W.G., Eckert G.P., Igbavboa U., and Muller W.E. Amyloid b-protein interactions with membranes and cholesterol: causes or casualties of Alzheimer's disease. Biochim. Biophys. Acta 1610 (2003) 281-290