Effects of apolipoprotein E on the human immunodeficiency virus protein Tat in neuronal cultures and synaptosomes

Journal of Neuroscience Research

Volumn 77, Issue 4, 2004, Pages 532-539

  Pocernich, Chava B ^a   Sultana, Rukhsana ^a   Hone, Eugene ^b   Turchan, Jadwiga ^c   Martins, Ralph N ^b   Calabrese, Vittorio ^d   Nath, Avindra ^c   Butterfield, D Allan ^a,e  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CATANIA   (Italy)

^e UNIVERSITY OF KENTUCKY   (United States)

Author keywords

ApoE3; ApoE4; HIV dementia; LRP receptor; Oxidative stress; Tat

Indexed keywords

APOLIPOPROTEIN E; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; REACTIVE OXYGEN METABOLITE; TRANSACTIVATOR PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEMENTIA; HUMAN IMMUNODEFICIENCY VIRUS 1; KNOCKOUT MOUSE; LIPID OXIDATION; MITOCHONDRION; MOUSE; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SYNAPTOSOME; WILD TYPE;

AIDS DEMENTIA COMPLEX; ANIMALS; ANTIOXIDANTS; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; APOLIPOPROTEINS E; CELL MEMBRANE; CELLS, CULTURED; GENE PRODUCTS, TAT; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LIPID PEROXIDATION; METABOLIC CLEARANCE RATE; MICE; MICE, KNOCKOUT; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SYNAPTOSOMES;

EID: 3442882468     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20182     Document Type: Article

References (62)

1. Bagasra O, Bachman SE, Jew L, Tawadros R, Cater J, Boden G, Ryan I, Pomerantz RJ. 1996. Increased human immunodeficiency virus type 1 replication in human peripheral blood mononuclear cells induced by ethanol: potential immunopathogenic mechanisms. J Infect Dis 173:550-558.
2. Beffert U, Aumont N, Dea D, Lussier-Cacan S, Davignon J, Poirier J. 1999. Apolipoprotein E isoform-specific reduction of extracellular amyloid in neuronal cultures. Brain Res Mol Brain Res 68:181-185.
3. Bohnet K, Pillot T, Visvikis S, Sabolovic N, Siest G. 1996. Apolipoprotein (apo) E genotype and apoE concentration determine binding of normal very low density lipoproteins to HepG2 cell surface receptors. J Lipid Res 37:1316-1324.
4. Borgatti P, Zauli G, Cantley LC, Capitani S. 1998. Extracellular HIV-1 Tat protein induces a rapid and selective activation of protein kinase C (PKC)-alpha, and -epsilon and -zeta isoforms in PC12 cells. Biochem Biophys Res Commun 242:332-337.
5. Boven LA, Gomes L, Hery C, Gray F, Verhoef J, Portegies P, Tardieu M, Nottet HS. 1999. Increased peroxynitrite activity in AIDS dementia complex: implications for the neuropathogenesis of HIV-1 infection. J Immunol 162:4319-4327.
6. Bowler A, Redgrave TG, Mamo JC. 1991. Chylomicron-remnant clearance in homozygote and heterozygote Watanabe-heritable-hyperlipidaemic rabbits is defective. Lack of evidence for an independent chylomicron-remnant receptor. Biochem J 276:381-386.
7. Butterfield DA, Stadtman ER. 1997. Protein oxidation processes in aging brain. Adv Cell Aging Gerontol 2:161-191.
8. Butterfield DA, Yatin SM, Varadarajan S, Koppal T. 1999. Amyloid β-peptide-induced oxidative pathways of cell death. Meth Enzymol 309:746-768.
9. Butterfield DA, Drake J, Pocernich C, Castegna A. 2001. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol Med 7:548-554.
10. Butterfield DA, Castegna A, Lauderback CM, Drake J. 2002. Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death. Neurobiol Aging 23:655-664.
11. Chang HC, Samaniego F, Nair BC, Buonaguro L, Ensoli B. 1997. HIV-1 Tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrix-associated heparan sulfate proteoglycans through its basic region. AIDS 11:1421-1431.
12. Chauhan A, Turchan J, Pocernich C, Bruce-Keller A, Roth S, Butterfield DA, Major EO, Nath A. 2003. Intracellular human immunodeficiency virus Tat expression in astrocytes promotes astrocyte survival but induces potent neurotoxicity at distant sites via axonal transport. J Biol Chem 278:13512-13519.
13. Chen P, Mayne M, Power C, Nath A. 1997. The Tat protein of HIV-1 induces tumor necrosis factor-alpha production. Implications for HIV-1-associated neurological diseases. J Biol Chem 272:22385-22388.
14. Cheng J, Nath A, Knudsen B, Hochman S, Geiger JD, Ma M, Magnuson DS. 1998. Neuronal excitatory properties of human immunodeficiency virus type 1 Tat protein. Neuroscience 82:97-106.
15. Conant K, Ma M, Nath A, Major EO. 1996. Extracellular human immunodeficiency virus type 1 Tat protein is associated with an increase in both NF-kappa B binding and protein kinase C activity in primary human astrocytes. J Virol 70:1384-1389.
16. Corder EH, Robertson K, Lannfelt L, Bogdanovic N, Eggertsen G, Wilkins J, Hall C. 1998. HIV-infected subjects with the E4 allele for APOE have excess dementia and peripheral neuropathy. Nat Med 4:1182-1184.
17. Dunlop O, Goplen AK, Liestol K, Myrvang B, Rootwelt H, Christophersen B, Kvittingen EA, Maehlen J. 1997. HIV dementia and apolipoprotein E. Acta Neurol Scand 95:315-318.
18. Ensoli B, Buonaguro L, Barillari G, Fiorelli V, Gendelman R, Morgan RA, Wingfield P, Gallo RC. 1993. Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J Virol 67:277-287.
19. Esterbauer H, Schaur RJ, Zollner H. 1991. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11:81-128.
20. Fagan AM, Watson M, Parsadanian M, Bales KR, Paul SM, Holtzman DM. 2002. Human and murine ApoE markedly alters A beta metabolism before and after plaque formation in a mouse model of Alzheimer's disease. Neurobiol Dis 9:305-318.
21. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, et al. 1995. Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 373:523-527.
22. Haughey NJ, Holden CP, Nath A, Geiger JD. 1999. Involvement of inositol 1,4,5-trisphosphate-regulated stores of intracellular calcium in calcium dysregulation and neuron cell death caused by HIV-1 protein tat. J Neurochem 73:1363-1374.
23. Haughey NJ, Nath A, Mattson MP, Slevin JT, Geiger JD. 2001. HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J Neurochem 78:457-467.
24. Hayman M, Arbuthnott G, Harkiss G, Brace H, Filippi P, Philippon V, Thomson D, Vigne R, Wright A. 1993. Neurotoxicity of peptide analogues of the transactivating protein tat from Maedi-Visna virus and human immunodeficiency virus. Neuroscience 53:1-6.
25. Herz J, Strickland DK. 2001. LRP: a multifunctional scavenger and signaling receptor. J Clin Invest 108:779-784.
26. Hudson L, Liu J, Nath A, Jones M, Raghavan R, Narayan O, Male D, Everall I. 2000. Detection of the human immunodeficiency virus regulatory protein tat in CNS tissues. J Neurovirol 6:145-155.
27. Jones M, Olafson K, Del Bigio MR, Peeling J, Nath A. 1998. Intraventricular injection of human immunodeficiency virus type 1 (HIV-1) tat protein causes inflammation, gliosis, apoptosis, and ventricular enlargement. J Neuropathol Exp Neurol 57:563-570.
28. Kang DE, Pietrzik CU, Baum L, Chevallier N, Merriam DE, Kounnas MZ, Wagner SL, Troncoso JC, Kawas CH, Katzman R, Koo EH. 2000. Modulation of amyloid beta-protein clearance and Alzheimer's disease susceptibility by the LDL receptor-related protein pathway. J Clin Invest 106:1159-1166.
29. Kanski J, Lauderback C, Butterfield DA. 2001. 5-Aminosalicylic acid protection against oxidative damage to synaptosomal membranes by alkoxyl radicals in vitro. Neurochem Res 26:23-29.
30. Keller JN, Lauderback CM, Butterfield DA, Kindy MS, Markesbery WR. 2000. Potential role for apolipoprotein E in maintaining synaptic homeostasis. J Neurochem 74:1579-1586.
31. Kolson DL, Gonzalez-Scarano F. 2000. HIV and HIV dementia. J Clin Invest 106:11-13.
32. Kruman II, Nath A, Mattson MP. 1998. HIV-1 protein Tat induces apoptosis of hippocampal neurons by a mechanism involving caspase activation, calcium overload, and oxidative stress. Exp Neurol 154:276-288.
33. LaDu MJ, Falduto MT, Manelli AM, Reardon CA, Getz GS, Frail DE. 1994. Isoform-specific binding of apolipoprotein E to beta-amyloid. J Biol Chem 269:23403-23406.
34. Laskowitz DT, Horsburgh K, Roses AD. 1998. Apolipoprotein E and the CNS response to injury. J Cereb Blood Flow Metab 18:465-471.
35. Lauderback CM, Hackett JM, Keller JN, Varadarajan S, Szweda L, Kindy M, Markesbery WR, Butterfield DA. 2001. Vulnerability of synaptosomes from apoE knock-out mice to structural and oxidative modifications induced by A beta(1-40): implications for Alzheimer's disease. Biochemistry 40:2548-2554.
36. Lauderback CM, Kanski J, Hackett JM, Maeda N, Kindy MS, Butterfield DA. 2002. Apolipoprotein E modulates Alzheimer's Abeta(1-42)-induced oxidative damage to synaptosomes in an allele-specific manner. Brain Res 924:90-97.
37. Lee SC, Hatch WC, Liu W, Brosnan CF, Dickson DW. 1993. Productive infection of human fetal microglia in vitro by HIV-1. Ann N Y Acad Sci 693:314-316.
38. Liu Y, Jones M, Hingtgen CM, Bu G, Laribee N, Tanzi RE, Moir RD, Nath A, He JJ. 2000. Uptake of HIV-1 tat protein mediated by low-density lipoprotein receptor-related protein disrupts the neuronal metabolic balance of the receptor ligands. Nat Med 6:1380-1387.
39. Magnuson DS, Knudsen BE, Geiger JD, Brownstone RM, Nath A. 1995. Human immunodeficiency virus type 1 tat activates non-N-methyl-D-aspartate excitatory amino acid receptors and causes neurotoxicity. Ann Neurol 37:373-380.
40. Mahley RW, Rall SC Jr. 2000. Apolipoprotein E: far more than a lipid transport protein. Annu Rev Genom Hum Genet 1:507-537.
41. Mamo JC, Bowler A, Elsegood CL, Redgrave TG. 1991. Defective plasma clearance of chylomicron-like lipid emulsions in Watanabe heritable hyperlipidemic rabbits. Biochim Biophys Acta 1081:241-245.
42. Mamotte CD, Sturm M, Foo JI, van Bockxmeer FM, Taylor RR. 1999. Comparison of the LDL-receptor binding of VLDL and LDL from apoE4 and apoE3 homozygotes. Am J Physiol 276:E553-E557.
43. Martins IJ, Vilcheze C, Mortimer BC, Bittman R, Redgrave TG. 1998. Sterol side chain length and structure affect the clearance of chylomicron-like lipid emulsions in rats and mice. J Lipid Res 39:302-312.
44. Martins RN, Clamette R, Fisher C, Broe GA, Brooks WS, Montgomery P, Gandy SE. 1995. ApoE genotypes in Australia: roles in early and late onset Alzheimer's disease and Down's syndrome. Neuroreport 6:1513-1516.
45. Milani D, Mazzoni M, Borgatti P, Zauli G, Cantley L, Capitani S. 1996. Extracellular human immunodeficiency virus type-1 Tat protein activates phosphatidylinositol 3-kinase in PC12 neuronal cells. J Biol Chem 271:22961-22964.
46. Miyata M, Smith JD. 1996. Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and beta-amyloid peptides. Nat Genet 14:55-61.
47. Nath A. 1999. Pathobiology of human immunodeficiency virus dementia. Semin Neurol 19:113-127.
48. Nath A, Psooy K, Martin C, Knudsen B, Magnuson DS, Haughey N, Geiger JD. 1996. Identification of a human immunodeficiency virus type 1 Tat epitope that is neuroexcitatory and neurotoxic. J Virol 70:1475-1480.
49. New DR, Maggirwar SB, Epstein LG, Dewhurst S, Gelbard HA. 1998. HIV-1 Tat induces neuronal death via tumor necrosis factor-alpha and activation of non-N-methyl-D-aspartate receptors by a NFkappaB- independent mechanism. J Biol Chem 273:17852-17858.
50. Poirier J, Baccichet A, Dea D, Gauthier S. 1993. Cholesterol synthesis and lipoprotein reuptake during synaptic remodelling in hippocampus in adult rats. Neuroscience 55:81-90.
51. Rajavashisth TB, Kaptein JS, Reue KL, Lusis AJ. 1985. Evolution of apolipoprotein E: mouse sequence and evidence for an 11-nucleotide ancestral unit. Proc Natl Acad Sci USA 82:8085-8089.
52. Rappaport J, Joseph J, Croul S, Alexander G, Del Valle L, Amini S, Khalili K. 1999. Molecular pathway involved in HIV-1-induced CNS pathology: role of viral regulatory protein, Tat. J Leukoc Biol 65:458-465.
53. Redgrave TG, Ly HL, Quintao EC, Ramberg CF, Boston RC. 1993. Clearance from plasma of triacylglycerol and cholesteryl ester after intravenous injection of chylomicron-like lipid emulsions in rats and man. Biochem J 290:843-847.
54. Sabatier JM, Vives E, Mabrouk K, Benjouad A, Rochat H, Duval A, Hue B, Bahraoui E. 1991. Evidence for neurotoxic activity of tat from human immunodeficiency virus type 1. J Virol 65:961-967.
55. Sheng H, Laskowitz DT, Bennett E, Schmechel DE, Bart RD, Saunders AM, Pearlstein RD, Roses AD, Warner DS. 1998. Apolipoprotein E isoform-specific differences in outcome from focal ischemia in transgenic mice. J Cereb Blood Flow Metab 18:361-366.
56. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD. 1993. Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 90:1977-1981.
57. Tardieu M, Hery C, Peudenier S, Boespflug O, Montagnier L. 1992. Human immunodeficiency virus type 1-infected monocytic cells can destroy human neural cells after cell-to-cell adhesion. Ann Neurol 32:11-17.
58. Turchan J, Pocernich CB, Gairola C, Chauhan A, Schifitto G, Butterfield DA, Buch S, Narayan O, Sinai A, Geiger J, Berger JR, Elford H, Nath A. 2003. Oxidative stress in HIV demented patients and protection ex vivo with novel antioxidants. Neurology 60:307-314.
59. Varadarajan S, Yatin S, Aksenova M, Butterfield DA. 2000. Review: Alzheimer's amyloid beta-peptide-associated free radical oxidative stress and neurotoxicity. J Struct Biol 130:184-208.
60. Yang DS, Smith JD, Zhou Z, Gandy SE, Martins RN. 1997. Characterization of the binding of amyloid-beta peptide to cell culture-derived native apolipoprotein E2, E3, and E4 isoforms and to isoforms from human plasma. J Neurochem 68:721-725.
61. Yang DS, Small DH, Seydel U, Smith JD, Hallmayer J, Gandy SE, Martins RN. 1999. Apolipoprotein E promotes the binding and uptake of beta-amyloid into Chinese hamster ovary cells in an isoform-specific manner. Neuroscience 90:1217-1226.
62. Ziegler A, Seelig J. 2004. Interaction of the protein transduction domain of HIV-1 TAT with heparan sulfate: binding mechanism and thermodynamic parameters. Biophys J 86:254-263.