Protecting the synapse: Evidence for a rational strategy to treat HIV-1 associated neurologic disease

Journal of Neuroimmune Pharmacology

Volumn 1, Issue 1, 2006, Pages 20-31

  Bellizzi, Matthew J ^a   Lu, Shao Ming ^a   Gelbard, Harris A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Alzheimer's disease; Excitotoxicity; HIV 1; HIV associated dementia; Memantine; Neuroinflammation; Neuroprotection; Synapse

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ALZHEIMER DISEASE; ANIMAL; HUMAN; IMMUNOLOGY; INFLAMMATION; NERVE DEGENERATION; PATHOLOGY; REVIEW; SYNAPSE;

AIDS DEMENTIA COMPLEX; ALZHEIMER DISEASE; ANIMALS; HUMANS; INFLAMMATION; NERVE DEGENERATION; SYNAPSES;

EID: 33747476112     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-005-9006-y     Document Type: Review

References (137)

1. Adle-Biassette H, Chretien F, Wingertsmann L, Hery C, Ereau T, Scaravilli F, Tardieu M, Gray F (1999) Neuronal apoptosis does not correlate with dementia in HIV infection but is related to microglial activation and axonal damage. Neuropathol Appl Neurobiol 25:123-133
2. Aisen PS, Davis KL, Berg JD, Schafer K, Campbell K, Thomas RG, Weiner MF, Farlow MR, Sano M, Grundman M, Thal LJ (2000) A randomized controlled trial of prednisone in Alzheimer's disease. Alzheimer's disease cooperative study. Neurology 54:588-593
3. Aisen PS, Schafer KA, Grundman M, Pfeiffer E, Sano M, Davis KL, Farlow MR, Jin S, Thomas RG, Thal LJ (2003) Effects of rofecoxib or naproxen vs placebo on Alzheimer disease progression: a randomized controlled trial. JAMA 289:2819-2826
4. Al-Noori S, Swann JW (2000) A role for sodium and chloride in kainic acid-induced beading of inhibitory interneuron dendrites. Neuroscience 101:337-348
5. Anderson ER, Boyle J, Zink WE, Persidsky Y, Gendelman HE, Xiong H (2003) Hippocampal synaptic dysfunction in a murine model of human immunodeficiency virus type 1 encephalitis. Neuroscience 118:359-369
6. Anderson ER, Gendelman HE, Xiong H (2004) Memantine protects hippocampal neuronal function in murine human immunodeficiency virus type 1 encephalitis. J Neurosci 24:7194-7198
7. Araujo DM, Cotman CW (1992) Beta-amyloid stimulates glial cells in vitro to produce growth factors that accumulate in senile plaques in Alzheimer's disease. Brain Res 569:141-145
8. Areosa SA, Sherriff F, McShane R. Memantine for dementia. Cochrane Database Syst. Rev. CD003154, 2005
9. Beal MF (1992) Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann Neurol 31:119-130
10. Bellizzi MJ, Lu S-M, Masliah E, Gelbard HA (2005) Synaptic activity becomes excitotoxic in neurons exposed to elevated platelet-activating factor. J Clin Invest 115:3185-3192
11. Bernardino L, Xapelli S, Silva AP, Jakobsen B, Poulsen FR, Oliveira CR, Vezzani A, Malva JO, Zimmer J (2005) Modulator effects of interleukin-1beta and tumor necrosis factor-alpha on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J Neurosci 25:6734-6744
12. Billings LM, Oddo S, Green KN, McGaugh JL, Laferla FM (2005) Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45:675-688
13. Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA, Mazziotta JC, Small GW (2000) Patterns of brain activation in people at risk for Alzheimer's disease. N Engl J Med 343:450-456
14. 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
15. Brendza RP, Bacskai BJ, Cirrito JR, Simmons KA, Skoch JM, Klunk WE, Mathis CA, Bales KR, Paul SM, Hyman BT, Holtzman DM (2005) Anti-Abeta antibody treatment promotes the rapid recovery of amyloid-associated neuritic dystrophy in PDAPP transgenic mice. J Clin Invest 115:428-433
16. Brown DF, Risser RC, Bigio EH, Tripp P, Stiegler A, Welch E, Eagan KP, Hladik CL, White CL 3rd (1998) Neocortical synapse density and Braak stage in the Lewy body variant of Alzheimer disease: a comparison with classic Alzheimer disease and normal aging. J Neuropathol Exp Neurol 57:955-960
17. Castilho RF, Ward MW, Nicholls DG (1999) Oxidative stress, mitochondrial function, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem 72:1394-1401
18. Chang L, Speck O, Miller EN, Braun J, Jovicich J, Koch C, Itti L, Ernst T (2001) Neural correlates of attention and working memory deficits in HIV patients. Neurology 57:1001-1007
19. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2:271-276
20. Chen HS, Pellegrini JW, Aggarwal SK, Lei SZ, Warach S, Jensen FE, Lipton SA (1992) Open-channel block of N-methyl-D-aspartate (NMDA) responses by memantine: therapeutic advantage against NMDA receptor-mediated neurotoxicity. J Neurosci 12:4427-4436
21. Clark GD, Happel LT, Zorumski CF, Bazan NG (1992) Enhancement of hippocampal excitatory synaptic transmission by platelet-activating factor. Neuron 9:1211-1216
22. Coleman PD, Yao PJ (2003) Synaptic slaughter in Alzheimer's disease. Neurobiol Aging 24:1023-1027
23. Combs CK, Karlo JC, Kao SC, Landreth GE (2001) beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J Neurosci 21:1179-1188
24. Cowan CM, Thai J, Krajewski S, Reed JC, Nicholson DW, Kaufmann SH, Roskams AJ (2001) Caspases 3 and 9 send a pro-apoptotic signal from synapse to cell body in olfactory receptor neurons. J Neurosci 21:7099-7109
25. Cunningham C, Deacon R, Wells H, Boche D, Waters S, Diniz CP, Scott H, Rawlins JN, Perry VH (2003) Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur J Neurosci 17:2147-2155
26. Cysique LA, Maruff P, Brew BJ (2004) Prevalence and pattern of neuropsychological impairment in human immunodeficiency virus-infected/acquired immunodeficiency syndrome (HIV/AIDS) patients across pre- and post-highly active antiretroviral therapy eras: a combined study of two cohorts. J Neurovirology 10:350-357
27. d'Aldin CG, Ruel J, Assie R, Pujol R, Puel JL (1997) Implication of NMDA type glutamate receptors in neural regeneration and neoformation of synapses after excitotoxic injury in the guinea pig cochlea. Int J Dev Neurosci 15:619-629
28. Davies CA, Mann DM, Sumpter PQ, Yates PO (1987) A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease. J Neurol Sci 78:151-164
29. Davis KL, Mohs RC, Marin D, Purohit DP, Perl DP, Lantz M, Austin G, Haroutunian V (1999) Cholinergic markers in elderly patients with early signs of Alzheimer disease. JAMA 281:1401-1406
30. Dawson VL, Dawson TM, Uhl GR, Snyder SH (1993) Human immunodeficiency virus type 1 coat protein neurotoxicity mediated by nitric oxide in primary cortical cultures. Proc Natl Acad Sci U S A 90:3256-3259
31. DeKosky ST, Scheff SW (1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 27:457-464
32. Ernst T, Chang L, Jovicich J, Ames N, Arnold S (2002) Abnormal brain activation on functional MRI in cognitively asymptomatic HIV patients. Neurology 59:1343-1349
33. Everall IP, Luthert PJ, Lantos PL (1991) Neuronal loss in the frontal cortex in HIV infection. Lancet 337:1119-1121
34. Everall IP, Luthert PJ, Lantos PL (1993) Neuronal number and volume alterations in the neocortex of HIV infected individuals. J Neurol Neurosurg Psychiatry 56:481-486
35. Everall IP, Glass JD, McArthur J, Spargo E, Lantos P (1994) Neuronal density in the superior frontal and temporal gyri does not correlate with the degree of human immunodeficiency virus-associated dementia. Acta Neuropathol (Berl) 88:538-544
36. Everall IP, Heaton RK, Marcotte TD, Ellis RJ, McCutchan JA, Atkinson JH, Grant I, Mallory M, Masliah E (1999) Cortical synaptic density is reduced in mild to moderate human immunodeficiency virus neurocognitive disorder. HNRC Group. HIV Neurobehavioral Research Center. Brain Pathol 9:209-217
37. Fein G, Biggins CA, MacKay S (1995) Delayed latency of the event-related brain potential P3A component in HIV disease. Progressive effects with increasing cognitive impairment. Arch Neurol 52:1109-1118
38. Ferrando SJ, Rabkin JG, Gorp Wvan, Lin SH, McElhiney M (2003) Longitudinal improvement in psychomotor processing speed is associated with potent combination antiretroviral therapy in HIV-1 infection. J Neuropsychiatry Clin Neurosci 15:208-214
39. Fine SM, Angel RA, Perry SW, Epstein LG, Rothstein JD, Dewhurst S, Gelbard HA (1996) Tumor necrosis factor alpha inhibits glutamate uptake by primary human astrocytes. Implications for pathogenesis of HIV-1 dementia. J Biol Chem 271:15303-15306
40. Floden AM, Li S, Combs CK (2005) Beta-amyloid-stimulated microglia induce neuron death via synergistic stimulation of tumor necrosis factor alpha and NMDA receptors. J Neurosci 25:2566-2575
41. Fonseca MI, Zhou J, Botto M, Tenner AJ (2004) Absence of C1q leads to less neuropathology in transgenic mouse models of Alzheimer's disease. J Neurosci 24:6457-6465
42. Gelbard HA, Dzenko KA, DiLoreto D, del Cerro C, del Cerro M, Epstein LG (1993) Neurotoxic effects of tumor necrosis factor alpha in primary human neuronal cultures are mediated by activation of the glutamate AMPA receptor subtype: implications for AIDS neuropathogenesis. Dev Neurosci 15:417-422
43. Gelbard HA, Nottet HS, Swindells S, Jett M, Dzenko KA, Genis P, White R, Wang L, Choi YB, Zhang D (1994) Platelet-activating factor: a candidate human immunodeficiency virus type 1-induced neurotoxin. J Virol 68:4628-4635
44. Gendelman HE, Zheng J, Coulter CL, Ghorpade A, Che M, Thylin M, Rubocki R, Persidsky Y, Hahn F, Reinhard J Jr, Swindells S (1998) Suppression of inflammatory neurotoxins by highly active antiretroviral therapy in human immunodeficiency virus-associated dementia. J Infect Dis 178:1000-1007
45. Genis P, Jett M, Bernton EW, Boyle T, Gelbard HA, Dzenko K, Keane RW, Resnick L, Mizrachi Y, Volsky DJ (1992) Cytokines and arachidonic metabolites produced during human immunodeficiency virus (HIV)-infected macrophage-astroglia interactions: implications for the neuropathogenesis of HIV disease. J Exp Med 176:1703-1718
46. Giulian D, Vaca K, Noonan CA (1990) Secretion of neurotoxins by mononuclear phagocytes infected with HIV-1. Science 250:1593-1596
47. Glass JD, Wesselingh SL, Selnes OA, McArthur JC (1993) Clinical-neuropathologic correlation in HIV-associated dementia. Neurology 43:2230-2237
48. Glass JD, Fedor H, Wesselingh SL, McArthur JC (1995) Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 38:755-762
49. Griffin WS, Stanley LC, Ling C, White L, MacLeod V, Perrot LJ, White CL, 3rd, Araoz C (1989) Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc Natl Acad Sci USA 86:7611-7615
50. Gylys KH, Fein JA, Yang F, Wiley DJ, Miller CA, Cole GM (2004) Synaptic changes in Alzheimer's disease: increased amyloid-beta and gliosis in surviving terminals is accompanied by decreased PSD-95 fluorescence. Am J Pathol 165:1809-1817
51. Harigaya Y, Shoji M, Shirao T, Hirai S (1996) Disappearance of actin-binding protein, drebrin, from hippocampal synapses in Alzheimer's disease. J Neurosci Res 43:87-92
52. Harkany T, Abraham I, Timmerman W, Laskay G, Toth B, Sasvari M, Konya C, Sebens JB, Korf J, Nyakas C, Zarandi M, Soos K, Penke B, Luiten PG (2000) Beta-amyloid neurotoxicity is mediated by a glutamate-triggered excitotoxic cascade in rat nucleus basalis. Eur J Neurosci 12:2735-2745
53. Hasbani MJ, Hyrc KL, Faddis BT, Romano C, Goldberg MP (1998) Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp Neurol 154:241-258
54. Hasbani MJ, Schlief ML, Fisher DA, Goldberg MP (2001) Dendritic spines lost during glutamate receptor activation reemerge at original sites of synaptic contact. J Neurosci 21:2393-2403
55. Hermann GE, Rogers RC, Bresnahan JC, Beattie MS (2001) Tumor necrosis factor-alpha induces cFOS and strongly potentiates glutamate-mediated cell death in the rat spinal cord. Neurobiol Dis 8:590-599
56. Hull M, Strauss S, Berger M, Volk B, Bauer J (1996) Inflammatory mechanisms in Alzheimer's disease. Eur Arch Psychiatry Clin Neurosci 246:124-128
57. Ikegaya Y, Kim JA, Baba M, Iwatsubo T, Nishiyama N, Matsuki N (2001) Rapid and reversible changes in dendrite morphology and synaptic efficacy following NMDA receptor activation: implication for a cellular defense against excitotoxicity. J Cell Sci 114:4083-4093
58. Ivins KJ, Bui ET, Cotman CW (1998) Beta-amyloid induces local neurite degeneration in cultured hippocampal neurons: evidence for neuritic apoptosis. Neurobiol Dis 5:365-378
59. Janus C, Pearson J, McLaurin J, Mathews PM, Jiang Y, Schmidt SD, Chishti MA, Horne P, Heslin D, French J, Mount HT, Nixon RA, Mercken M, Bergeron C, Fraser PE, St George-Hyslop P, Westaway D (2000) A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408:979-982
60. Keelan J, Vergun O, Duchen MR (1999) Excitotoxic mitochondrial depolarisation requires both calcium and nitric oxide in rat hippocampal neurons. J Physiol 520(Pt 3):797-813
61. Klegeris A, Walker DG, McGeer PL (1994) Activation of macrophages by Alzheimer beta amyloid peptide. Biochem Biophys Res Commun 199:984-991
62. Koenig S, Gendelman HE, Orenstein JM, Canto MCDal, Pezeshkpour GH, Yungbluth M, Janotta F, Aksamit A, Martin MA, Fauci AS (1986) Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233:1089-1093
63. Koh JY, Yang LL, Cotman CW (1990) Beta-amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage. Brain Res 533:315-320
64. Kustova Y, Ha JH, Espey MG, Sei Y, Morse D, Basile AS (1998) The pattern of neurotransmitter alterations in LPBM5 infected mice is consistent with glutamatergic hyperactivation. Brain Res 793:119-126
65. Larson J, Lynch G, Games D, Seubert P (1999) Alterations in synaptic transmission and long-term potentiation in hippocampal slices from young and aged PDAPP mice. Brain Res 840:23-35
66. Lawrence CB, Allan SM, Rothwell NJ (1998) Interleukin-1beta and the interleukin-1 receptor antagonist act in the striatum to modify excitotoxic brain damage in the rat. Eur J Neurosci 10:1188-1195
67. Li ST, Matsushita M, Moriwaki A, Saheki Y, Lu YF, Tomizawa K, Wu HY, Terada H, Matsui H (2004) HIV-1 Tat inhibits long-term potentiation and attenuates spatial learning [corrected]. Ann Neurol 55:362-371
68. Lippa CF (2004) Synaptophysin immunoreactivity in Pick's disease: comparison with Alzheimer's disease and dementia with Lewy bodies. Am J Alzheimer's Dis Other Dement 19:341-344
69. Lipton AM, Cullum CM, Satumtira S, Sontag E, Hynan LS, White CL 3rd, Bigio EH (2001) Contribution of asymmetric synapse loss to lateralizing clinical deficits in frontotemporal dementias. Arch Neurol 58:1233-1239
70. Lipton SA (2004) Failures and successes of NMDA receptor antagonists: molecular basis for the use of open-channel blockers like memantine in the treatment of acute and chronic neurologic insults. NeuroRx 1:101-110
71. Lipton SA, Rosenberg PA (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330:613-622
72. Lue LF, Brachova L, Civin WH, Rogers J (1996) Inflammation, A beta deposition, and neurofibrillary tangle formation as correlates of Alzheimer's disease neurodegeneration. J Neuropathol Exp Neurol 55:1083-1088
73. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, Wang N, Caspersen C, Chen X, Pollak S, Chaney M, Trinchese F, Liu S, Gunn-Moore F, Lue LF, Walker DG, Kuppusamy P, Zewier ZL, Arancio O, Stern D, Yan SS, Wu H (2004) ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 304:448-452
74. Ma XC, Gottschall PE, Chen LT, Wiranowska M, Phelps CP (2002) Role and mechanisms of interleukin-1 in the modulation of neurotoxicity. Neuroimmunomodulation 10:199-207
75. Masliah E, Ge N, Morey M, DeTeresa R, Terry RD, Wiley CA (1992a) Cortical dendritic pathology in human immunodeficiency virus encephalitis. Lab Invest 66:285-291
76. Masliah E, Achim CL, Ge N, DeTeresa R, Terry RD, Wiley CA (1992b) Spectrum of human immunodeficiency virus-associated neocortical damage. Ann Neurol 32:321-329
77. Masliah E, Mallory M, Hansen L, DeTeresa R, Alford M, Terry R (1994) Synaptic and neuritic alterations during the progression of Alzheimer's disease. Neurosci Lett 174:67-72
78. Masliah E, Heaton RK, Marcotte TD, Ellis RJ, Wiley CA, Mallory M, Achim CL, McCutchan JA, Nelson JA, Atkinson JH, Grant I (1997) Dendritic injury is a pathological substrate for human immunodeficiency virus-related cognitive disorders. HNRC Group. The HIV Neurobehavioral Research Center. Ann Neurol 42:963-972
79. Masliah E, Mallory M, Alford M, DeTeresa R, Hansen LA, McKeel DW Jr, Morris JC (2001) Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology 56:127-129
80. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE (1992) beta-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12:376-389
81. Mattson MP, Keller JN, Begley JG (1998a) Evidence for synaptic apoptosis. Exp Neurol 153:35-48
82. Mattson MP, Partin J, Begley JG (1998b) Amyloid beta-peptide induces apoptosis-related events in synapses and dendrites. Brain Res 807:167-176
83. McArthur JC (2004) HIV dementia: an evolving disease. J Neuroimmunol 157:3-10
84. Meda L, Cassatella MA, Szendrei GI, Otvos L Jr, Baron P, Villalba M, Ferrari D, Rossi F (1995) Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374:647-650
85. Meeker RB, Robertson K, Barry T, Hall C (1999) Neurotoxicity of CSF from HIV-infected humans. J Neurovirology 5:507-518
86. Meeker RB, Boles JC, Robertson KR, Hall CD (2005) Cerebrospinal fluid from human immunodeficiency virus-infected individuals facilitates neurotoxicity by suppressing intracellular calcium recovery. J Neurovirology 11:144-156
87. Minkeviciene R, Banerjee P, Tanila H (2004) Memantine improves spatial learning in a transgenic mouse model of Alzheimer's disease. J Pharmacol Exp Ther 311:677-682
88. Missonnier P, Gold G, Fazi-Costa L, Michel JP, Mulligan R, Michon A, Ibanez V, Giannakopoulos P (2005) Early event-related potential changes during working memory activation predict rapid decline in mild cognitive impairment. J Gerontol, Ser A, Biol Sci Med Sci 60:660-666
89. Morgan D, Diamond DM, Gottschall PE, Ugen KE, Dickey C, Hardy J, Duff K, Jantzen P, DiCarlo G, Wilcock D, Connor K, Hatcher J, Hope C, Gordon M, Arendash GW (2000) A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408:982-985
90. Murphy GM Jr, Yang L, Cordell B (1998) Macrophage colony-stimulating factor augments beta-amyloid-induced interleukin-1, interleukin-6, and nitric oxide production by microglial cells. J Biol Chem 273:20967-20971
91. Mutisya EM, Bowling AC, Beal MF (1994) Cortical cytochrome oxidase activity is reduced in Alzheimer's disease. J Neurochem 63:2179-2184
92. Nath A, Conant K, Chen P, Scott C, Major EO (1999) Transient exposure to HIV-1 Tat protein results in cytokine production in macrophages and astrocytes. A hit and run phenomenon. J Biol Chem 274:17098-17102
93. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39:409-421
94. Orgogozo JM, Gilman S, Dartigues JF, Laurent B, Puel M, Kirby LC, Jouanny P, Dubois B, Eisner L, Flitman S, Michel BF, Boada M, Frank A, Hock C (2003) Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 61:46-54
95. Park JS, Bateman MC, Goldberg MP (1996) Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation. Neurobiol Dis 3:215-227
96. Parpura-Gill A, Beitz D, Uemura E (1997) The inhibitory effects of beta-amyloid on glutamate and glucose uptakes by cultured astrocytes. Brain Res 754:65-71
97. Perry SW, Dewhurst S, Bellizzi MJ, Gelbard HA (2002) Tumor necrosis factor-alpha in normal and diseased brain: Conflicting effects via intraneuronal receptor crosstalk? J Neurovirology 8:611-624
98. Perry SW, Norman JP, Litzburg A, Zhang D, Dewhurst S, Gelbard HA (2005) HIV-1 transactivator of transcription protein induces mitochondrial hyperpolarization and synaptic stress leading to apoptosis. J Immunol 174:4333-4344
99. Polazzi E, Levi G, Minghetti L (1999) Human immunodeficiency virus type 1 Tat protein stimulates inducible nitric oxide synthase expression and nitric oxide production in microglial cultures. J Neuropathol Exp Neurol 58:825-831
100. Puel JL, Saffiedine S, Gervais d'Aldin C, Eybalin M, Pujol R (1995) Synaptic regeneration and functional recovery after excitotoxic injury in the guinea pig cochlea. C R Acad Sci III 318:67-75
101. Pujol R, Puel JL (1999) Excitotoxicity, synaptic repair, and functional recovery in the mammalian cochlea: a review of recent findings. Ann NY Acad Sci 884:249-254
102. Pulliam L, Herndier BG, Tang NM, McGrath MS (1991) Human immunodeficiency virus-infected macrophages produce soluble factors that cause histological and neurochemical alterations in cultured human brains. J Clin Invest 87:503-512
103. Rintoul GL, Filiano AJ, Brocard JB, Kress GJ, Reynolds IJ (2003) Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J Neurosci 23:7881-7888
104. Rogers J, Cooper NR, Webster S, Schultz J, McGeer PL, Styren SD, Civin WH, Brachova L, Bradt B, Ward P(1992) Complement activation by beta-amyloid in Alzheimer disease. Proc Natl Acad Sci U S A 89:10016-10020
105. Sacktor N, McDermott MP, Marder K, Schifitto G, Selnes OA, McArthur JC, Stern Y, Albert S, Palumbo D, Kieburtz K, De Marcaida JA, Cohen B, Epstein L (2002) HIV-associated cognitive impairment before and after the advent of combination therapy. J Neurovirology 8:136-142
106. Smith MA, Richey Harris PL, Sayre LM, Beckman JS, Perry G (1997) Widespread peroxynitrite-mediated damage in Alzheimer's disease. J Neurosci 17:2653-2657
107. Speth C, Stockl G, Mohsenipour I, Wurzner R, Stoiber H, Lass-Florl C, Dierich MP (2001) Human immunodeficiency virus type 1 induces expression of complement factors in human astrocytes. J Virol 75:2604-2615
108. Stellwagen D, Beattie EC, Seo JY, Malenka RC (2005) Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J Neurosci 25:3219-3228
109. Stout AK, Raphael HM, Kanterewicz BI, Klann E, Reynolds IJ (1998) Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat Neurosci 1:366-373
110. Strauss S, Bauer J, Ganter U, Jonas U, Berger M, Volk B (1992) Detection of interleukin-6 and alpha 2-macroglobulin immunoreactivity in cortex and hippocampus of Alzheimer's disease patients. Lab Invest 66:223-230
111. Szekely CA, Thorne JE, Zandi PP, Ek M, Messias E, Breitner JC, Goodman SN (2004) Nonsteroidal anti-inflammatory drugs for the prevention of Alzheimer's disease: a systematic review. Neuroepidemiology 23:159-169
112. Tabet N, Feldman H. Indomethacin for the treatment of Alzheimer's disease patients. Cochrane Database Syst. Rev. CD003673, 2002
113. Tarkowski E, Blennow K, Wallin A, Tarkowski A (1999) Intracerebral production of tumor necrosis factor-alpha, a local neuroprotective agent, in Alzheimer disease and vascular dementia. J Clin Immunol 19:223-230
114. Tarkowski E, Andreasen N, Tarkowski A, Blennow K (2003) Intrathecal inflammation precedes development of Alzheimer's disease. J Neurol Neurosurg Psychiatry 74:1200-1205
115. Tepper VJ, Farley JJ, Rothman MI, Houck DL, Davis KF, Collins-Jones TL, Wachtel RC (1998) Neurodevelopmental/neuroradiologic recovery of a child infected with HIV after treatment with combination antiretroviral therapy using the HIV-specific protease inhibitor ritonavir. Pediatrics 101:E7,
116. Terry RD (2000) Cell death or synaptic loss in Alzheimer disease. J Neuropathol Exp Neurol 59:1118-1119
117. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572-580
118. Thurnher MM, Schindler EG, Thurnher SA, Pernerstorfer-Schon H, Kleibl-Popov C, Rieger A (2000) Highly active antiretroviral therapy for patients with AIDS dementia complex: effect on MR imaging findings and clinical course. AJNR Am J Neuroradiol 21:670-678
119. Tiraboschi P, Hansen LA, Alford M, Masliah E, Thal LJ, Corey-Bloom J (2000) The decline in synapses and cholinergic activity is asynchronous in Alzheimer's disease. Neurology 55:1278-1283
120. 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
121. Van Dam D, De Deyn PP (2006) Cognitive evaluation of disease-modifying efficacy of galantamine and memantine in the APP23 model. Eur Neuropsychopharmacol 16:59-69
122. Van Gool WA, Weinstein HC, Scheltens P, Walstra GJ (2001) Effect of hydroxychloroquine on progression of dementia in early Alzheimer's disease: an 18-month randomised, double-blind, placebo-controlled study. Lancet 358:455-460
123. Vehmas AK, Kawas CH, Stewart WF, Troncoso JC (2003) Immune reactive cells in senile plaques and cognitive decline in Alzheimer's disease. Neurobiol Aging 24:321-331
124. Vergun O, Keelan J, Khodorov BI, Duchen MR (1999) Glutamate-induced mitochondrial depolarisation and perturbation of calcium homeostasis in cultured rat hippocampal neurones. J Physiol 519(Pt 2):451-466
125. Vergun O, Sobolevsky AI, Yelshansky MV, Keelan J, Khodorov BI, Duchen MR (2001) Exploration of the role of reactive oxygen species in glutamate neurotoxicity in rat hippocampal neurones in culture. J Physiol 531:147-163
126. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Luca MDi, Galli CL, Marinovich M (2003) Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23:8692-8700
127. Wang P, Barks JD, Silverstein FS (1999) Tat, a human immunodeficiency virus-1-derived protein, augments excitotoxic hippocampal injury in neonatal rats. Neuroscience 88:585-597
128. Wang Z, Pekarskaya O, Bencheikh M, Chao W, Gelbard HA, Ghorpade A, Rothstein JD, Volsky DJ (2003) Reduced expression of glutamate transporter EAAT2 and impaired glutamate transport in human primary astrocytes exposed to HIV-1 or gp120. Virology 312:60-73
129. White RJ, Reynolds IJ (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J Neurosci 16:5688-5697
130. White AR, Guirguis R, Brazier MW, Jobling MF, Hill AF, Beyreuther K, Barrow CJ, Masters CL, Collins SJ, Cappai R (2001) Sublethal concentrations of prion peptide PrP106-126 or the amyloid beta peptide of Alzheimer's disease activates expression of proapoptotic markers in primary cortical neurons. Neurobiol Dis 8:299-316
131. Wiley CA, Schrier RD, Nelson JA, Lampert PW, Oldstone MB (1986) Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc Natl Acad Sci U S A 83:7089-7093
132. Xu Y, Tao YX (2004) Involvement of the NMDA receptor/nitric oxide signal pathway in platelet-activating factor-induced neurotoxicity. NeuroReport 15:263-266
133. Xu Y, Zhang B, Hua Z, Johns RA, Bredt DS, Tao YX (2004) Targeted disruption of PSD-93 gene reduces platelet-activating factor-induced neurotoxicity in cultured cortical neurons. Exp Neurol 189:16-24
134. Yao PJ, Zhu M, Pyun EI, Brooks AI, Therianos S, Meyers VE, Coleman PD (2003) Defects in expression of genes related to synaptic vesicle trafficking in frontal cortex of Alzheimer's disease. Neurobiol Dis 12:97-109
135. Zanjani H, Finch CE, Kemper C, Atkinson J, McKeel D, Morris JC, Price JL (2005) Complement activation in very early Alzheimer disease. Alzheimer Dis Assoc Disord 19:55-66
136. Zhu B, Luo L, Moore GR, Paty DW, Cynader MS (2003) Dendritic and synaptic pathology in experimental autoimmune encephalomyelitis. Am J Pathol 162:1639-1650
137. Zink WE, Anderson E, Boyle J, Hock L, Rodriguez-Sierra J, Xiong H, Gendelman HE, Persidsky Y (2002) Impaired spatial cognition and synaptic potentiation in a murine model of human immunodeficiency virus type 1 encephalitis. J Neurosci 22:2096-2105