The human immunodeficiency virus coat protein gp120 promotes forward trafficking and surface clustering of NMDA receptors in membrane microdomains

Journal of Neuroscience

Volumn 31, Issue 47, 2011, Pages 17074-17090

  Xu, Hangxiu ^a   Bae, Mihyun ^a   Tovar y Romo, Luis B ^a   Patel, Neha ^a   Bandaru, Veera Venkata Ratnam ^a   Pomerantz, Daniel ^a   Steiner, Joseph P ^a   Haughey, Norman J ^a,b  

^a Departments of Neurology   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLYCOPROTEIN GP 120; LIPID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NEUTRAL SPHINGOMYELINASE 2; PROTEIN KINASE C; SERINE; SPHINGOMYELIN PHOSPHODIESTERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; CELL DISRUPTION; CELL MEMBRANE TRANSPORT; CELL SURFACE; CLUSTER ANALYSIS; CONTROLLED STUDY; DENDRITE; EMBRYO; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; LIPID RAFT; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; RAT; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; CELLS, CULTURED; HIPPOCAMPUS; HIV ENVELOPE PROTEIN GP120; HUMANS; MEMBRANE MICRODOMAINS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR AGGREGATION; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 81855224923     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4072-11.2011     Document Type: Article

References (114)

1. Achim CL, (2009) Increased accumulation of intraneuronal amyloid beta in HIV-infected patients. J Neuroimmune Pharmacol 4:190-199.
2. Ances BM, Vaida F, Yeh MJ, Liang CL, Buxton RB, Letendre S, McCutchan JA, Ellis RJ (2010) HIV infection and aging independently affect brain function as measured by functional magnetic resonance imaging. J Infect Dis 201:336-340.
3. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Cinque P, Epstein LG, Goodkin K, Gisslen M, Grant I, Heaton RK, Joseph J, Marder K, Marra CM, McArthur JC, Nunn M, Price RW, Pulliam L, Robertson KR, Sacktor N, Valcour V, Wojna VE (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789-1799.
4. Aubin I, Adams CP, Opsahl S, Septier D, Bishop CE, Auge N, Salvayre R, Negre-Salvayre A, Goldberg M, Guénet JL, Poirier C (2005) A deletion in the gene encoding sphingomyelin phosphodiesterase 3 (Smpd3) results in osteogenesis and dentinogenesis imperfecta in the mouse. Nat Genet 37:803-805.
5. Bagetta V, Ghiglieri V, Sgobio C, Calabresi P, Picconi B (2010) Synaptic dysfunction in Parkinson's disease. Biochem Soc Trans 38:493-497.
6. Bandaru VV, McArthur JC, Sacktor N, Cutler RG, Knapp EL, Mattson MP, Haughey NJ (2007) Associative and predictive biomarkers of dementia in HIV-1-infected patients. Neurology 68:1481-1487.
7. Bandaru VV, Troncoso J, Wheeler D, Pletnikova O, Wang J, Conant K, Haughey NJ (2009) ApoE4 disrupts sterol and sphingolipid metabolism in Alzheimer's but not normal brain. Neurobiol Aging 30:591-599.
8. Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35:345-353.
9. Bécart S, Setterblad N, Ostrand-Rosenberg S, Ono SJ, Charron D, Mooney N (2003) Intracytoplasmic domains ofMHCclass II molecules are essential for lipid-raft-dependent signaling. J Cell Sci 116:2565-2575.
10. Ben-David O, Futerman AH (2010) The role of the ceramide acyl chain length in neurodegeneration: involvement of ceramide synthases. Neuromolecular Med 12:341-350.
11. Besshoh S, Bawa D, Teves L, Wallace MC, Gurd JW (2005) Increased phosphorylation and redistribution of NMDA receptors between synaptic lipid rafts and post-synaptic densities following transient global ischemia in the rat brain. J Neurochem 93:186-194.
12. Bi K, Tanaka Y, Coudronniere N, Sugie K, Hong S, van Stipdonk MJ, Altman A (2001) Antigen-induced translocation of PKC-theta to membrane rafts is required for T cell activation. Nat Immunol 2:556-563.
13. Botto L, Masserini M, Palestini P (2007) Changes in the composition of detergent-resistant membrane domains of cultured neurons following protein kinase C activation. J Neurosci Res 85:443-450.
14. Brann AB, Scott R, Neuberger Y, Abulafia D, Boldin S, Fainzilber M, Futerman AH (1999) Ceramide signaling downstream of the p75 neurotrophin receptor mediates the effects of nerve growth factor on outgrowth of cultured hippocampal neurons. J Neurosci 19:8199-8206.
15. Brann AB, Tcherpakov M, Williams IM, Futerman AH, Fainzilber M (2002) Nerve growth factor-induced p75-mediated death of cultured hippocampal neurons is age-dependent and transduced through ceramide generated by neutral sphingomyelinase. J Biol Chem 277:9812-9818.
16. Brew BJ, Crowe SM, Landay A, Cysique LA, Guillemin G (2009) Neurodegeneration and ageing in the HAART era. J Neuroimmune Pharmacol 4:163-174.
17. 2+ release by cAMP-dependent protein kinase. A mechanism for agonist-specific calcium signaling? Cell Calcium 25:219-226.
18. Cardenas VA, Meyerhoff DJ, Studholme C, Kornak J, Rothlind J, Lampiris H, Neuhaus J, Grant RM, Chao LL, Truran D, Weiner MW (2009) Evidence for ongoing brain injury in human immunodeficiency viruspositive patients treated with antiretroviral therapy. J Neurovirol 15:324-333.
19. Catani MV, Corasaniti MT, Navarra M, Nisticò G, Finazzi-Agrò A, Melino G (2000) gp120 induces cell death in human neuroblastoma cells through the CXCR4 and CCR5 chemokine receptors. J Neurochem 74:2373-2379.
20. Chang L, Wong V, Nakama H, Watters M, Ramones D, Miller EN, Cloak C, Ernst T (2008) Greater than age-related changes in brain diffusion of HIV patients after 1 year. J Neuroimmune Pharmacol 3:265-274.
21. Choi WT, Tian S, Dong CZ, Kumar S, Liu D, Madani N, An J, Sodroski JG, Huang Z (2005) Unique ligand binding sites on CXCR4 probed by a chemical biology approach: implications for the design of selective human immunodeficiency virus type 1 inhibitors. J Virol 79:15398-15404.
22. Cohen RA, Harezlak J, Gongvatana A, Buchthal S, Schifitto G, Clark U, Paul R, Taylor M, Thompson P, Tate D, Alger J, Brown M, Zhong J, Campbell T, Singer E, Daar E, McMahon D, Tso Y, Yiannoutsos CT, Navia B; HIV Neuroimaging Consortium (2010) Cerebral metabolite abnormalities in human immunodeficiency virus are associated with cortical and subcortical volumes. J Neurovirol 16:435-444.
23. Coogan AN, O'Neill LA, O'Connor JJ (1999) The P38 mitogen-activated protein kinase inhibitor SB203580 antagonizes the inhibitory effects of interleukin-1beta on long-term potentiation in the rat dentate gyrus in vitro. Neuroscience 93:57-69.
24. Corasaniti MT, Melino G, Navarra M, Garaci E, Finazzi-Agrò A, Nisticò G (1995) Death of cultured human neuroblastoma cells induced by HIV-1 gp120 is prevented byNMDAreceptor antagonists and inhibitors of nitric oxide and cyclooxygenase. Neurodegeneration 4:315-321.
25. Corasaniti MT, Strongoli MC, Piccirilli S, Nisticò R, Costa A, Bilotta A, Turano P, Finazzi-Agrò A, Bagetta G (2000) Apoptosis induced by gp120 in the neocortex of rat involves enhanced expression of cyclooxygenase type 2 and is prevented by NMDA receptor antagonists and by the 21-aminosteroid U-74389G. Biochem Biophys Res Commun 274:664-669.
26. Davis CN, Tabarean I, Gaidarova S, Behrens MM, Bartfai T (2006) IL-1beta induces a MyD88-dependent and ceramide-mediated activation of Src in anterior hypothalamic neurons. J Neurochem 98:1379-1389.
27. Day CA, Kenworthy AK (2009) Tracking microdomain dynamics in cell membranes. Biochim Biophys Acta 1788:245-253.
28. Delint-Ramirez I, Fernández E, Bayés A, Kicsi E, Komiyama NH, Grant SG (2010) In vivo composition of NMDA receptor signaling complexes differs between membrane subdomains and is modulated by PSD-95 and PSD-93. J Neurosci 30:8162-8170.
29. Dhillon NK, Peng F, Bokhari S, Callen S, Shin SH, Zhu X, Kim KJ, Buch SJ (2008) Cocaine-mediated alteration in tight junction protein expression and modulation of CCL2/CCR2 axis across the blood-brain barrier: implications for HIV-dementia. J Neuroimmune Pharmacol 3:52-56.
30. Dreyer EB, Lipton SA (1995) The coat protein gp120 of HIV-1 inhibits astrocyte uptake of excitatory amino acids via macrophage arachidonic acid. Eur J Neurosci 7:2502-2507.
31. Dreyer EB, Kaiser PK, Offermann JT, Lipton SA (1990) HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists. Science 248:364-367.
32. El-Hage N, Wu G, Wang J, Ambati J, Knapp PE, Reed JL, Bruce-Keller AJ, Hauser KF (2006) HIV-1 Tat and opiate-induced changes in astrocytes promote chemotaxis of microglia through the expression of MCP-1 and alternative chemokines. Glia 53:132-146.
33. Fasano C, Miolan JP, Niel JP (2003) Modulation by C2 ceramide of the nicotinic transmission within the coeliac ganglion in the rabbit. Neuroscience 116:753-759.
34. Fischer-Smith T, Bell C, Croul S, Lewis M, Rappaport J (2008) Monocyte/ macrophage trafficking in acquired immunodeficiency syndrome encephalitis: lessons from human and nonhuman primate studies. J Neurovirol 14:318-326.
35. Füllekrug J, Simons K (2004) Lipid rafts and apical membrane traffic. Ann N Y Acad Sci 1014:164-169.
36. Furukawa K, Mattson MP (1998) The transcription factor NF-kappaB mediates increases in calcium currents and decreases in NMDA-and AMPA/ kainate-induced currents induced by tumor necrosis factor-alpha in hippocampal neurons. J Neurochem 70:1876-1886.
37. Furuya S, Mitoma J, Makino A, Hirabayashi Y (1998) Ceramide and its interconvertible metabolite sphingosine function as indispensable lipid factors involved in survival and dendritic differentiation of cerebellar Purkinje cells. J Neurochem 71:366-377.
38. Geeraerts T, Deiva K, M'sika I, Salim H, Héry C, Tardieu M (2006) Effects of SDF-1alpha and gp120IIIB on apoptotic pathways in SK-N-SH neuroblastoma cells. Neurosci Lett 399:115-120.
39. Gelman BB (2007) The neuropathology of HIV. Handb Clin Neurol 85:301-317.
40. Gongvatana A, Schweinsburg BC, Taylor MJ, Theilmann RJ, Letendre SL, Alhassoon OM, Jacobus J, Woods SP, Jernigan TL, Ellis RJ, Frank LR, Grant I; Charter Group (2009) White matter tract injury and cognitive impairment in human immunodeficiency virus-infected individuals. J Neurovirol 15:187-195.
41. Gorry PR, Bristol G, Zack JA, Ritola K, Swanstrom R, Birch CJ, Bell JE, Bannert N, Crawford K, Wang H, Schols D, De Clercq E, Kunstman K, Wolinsky SM, Gabuzda D (2001) Macrophage tropism of human immunodeficiency virus type 1 isolates from brain and lymphoid tissues predicts neurotropism independent of coreceptor specificity. J Virol 75: 10073-10089.
42. Gray F, Bazille C, Adle-Biassette H, Mikol J, Moulignier A, Scaravilli F (2005) Central nervous system immune reconstitution disease in acquired immunodeficiency syndrome patients receiving highly active antiretroviral treatment. J Neurovirol 11 [Suppl 3]:16-22.
43. Gupta RG, Kelly KM, Helke KL, Queen SE, Karper JM, Dorsey JL, Brice AK, Adams RJ, Tarwater PM, Kolson DL, Mankowski JL (2010) HIV and SIV induce alterations in CNS CaMKII expression and activation: a potential mechanism for cognitive impairment. Am J Pathol 176:2776-2784.
44. Gupta S, Aggarwal S, Kim C, Gollapudi S (1994) Human immunodeficiency virus-1 recombinant gp120 induces changes in protein kinaseCisozymes: a preliminary report. Int J Immunopharmacol 16:197-204.
45. Haughey NJ (2010) Sphingolipids in neurodegeneration. Neuromolecular Med 12:301-305.
46. Haughey NJ, Cutler RG, Tamara A, McArthur JC, Vargas DL, Pardo CA, Turchan J, Nath A, Mattson MP (2004) Perturbation of sphingolipid metabolism and ceramide production in HIV-dementia. Ann Neurol 55:257-267.
47. Hesselgesser J, Taub D, Baskar P, Greenberg M, Hoxie J, Kolson DL, Horuk R (1998) Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1 alpha is mediated by the chemokine receptor CXCR4. Curr Biol 8:595-598.
48. 2+-dependent neutral sphingomyelinase. Proc Natl Acad Sci USA 97:5895-5900.
49. Höke A, Morris M, Haughey NJ (2009) GPI-1046 protects dorsal root ganglia from gp120-induced axonal injury by modulating store-operated calcium entry. J Peripher Nerv Syst 14:27-35.
50. Horak M, Wenthold RJ (2009) Different roles of C-terminal cassettes in the trafficking of full-length NR1 subunits to the cell surface. J Biol Chem 284:9683-9691.
51. Inokuchi J, Mizutani A, Jimbo M, Usuki S, Yamagishi K, Mochizuki H, Muramoto K, Kobayashi K, Kuroda Y, Iwasaki K, Ohgami Y, Fujiwara M (1998) A synthetic ceramide analog (L-PDMP) up-regulates neuronal function. Ann N Y Acad Sci 845:219-224.
52. Irish BP, Khan ZK, Jain P, Nonnemacher MR, Pirrone V, Rahman S, Rajagopalan N, Suchitra JB, Mostoller K, Wigdahl B (2009) Molecular mechanisms of neurodegenerative diseases induced by human retroviruses: a review. Am J Infect Dis 5:231-258.
53. Ito A, Horigome K (1995) Ceramide prevents neuronal programmed cell death induced by nerve growth factor deprivation. J Neurochem 65:463-466.
54. Jana A, Pahan K (2004) Human immunodeficiency virus type 1 gp120 induces apoptosis in human primary neurons through redox-regulated activation of neutral sphingomyelinase. J Neurosci 24:9531-9540.
55. Jana A, Hogan EL, Pahan K (2009) Ceramide and neurodegeneration: susceptibility of neurons and oligodendrocytes to cell damage and death. J Neurol Sci 278:5-15.
56. Kaul M, Lipton SA (1999) Chemokines and activated macrophages in HIV gp120-induced neuronal apoptosis. Proc Natl Acad Sci USA. 96:8212-8216.
57. Khan MZ, Brandimarti R, Patel JP, Huynh N, Wang J, Huang Z, Fatatis A, Meucci O (2004) Apoptotic and antiapoptotic effects of CXCR4: is it a matter of intrinsic efficacy? Implications for HIV neuropathogenesis. AIDS Res Hum Retroviruses 20:1063-1071.
58. Khan MZ, Brandimarti R, Shimizu S, Nicolai J, Crowe E, Meucci O (2008) The chemokine CXCL12 promotes survival of postmitotic neurons by regulating Rb protein. Cell Death Differ 15:1663-1672.
59. Khanlou N, Moore DJ, Chana G, Cherner M, Lazzaretto D, Dawes S, Grant I, Masliah E, Everall IP; HNRC Group (2009) Increased frequency of alpha-synuclein in the substantia nigra in human immunodeficiency virus infection. J Neurovirol 15:131-138.
60. Kristiansen LV, Patel SA, Haroutunian V, Meador-Woodruff JH (2010) Expression of the NR2B-NMDA receptor subunit and its Tbr-1/CINAP regulatory proteins in postmortem brain suggest altered receptor processing in schizophrenia. Synapse 64:495-502.
61. Lan JY, Skeberdis VA, Jover T, Grooms SY, Lin Y, Araneda RC, Zheng X, Bennett MV, Zukin RS (2001) Protein kinase C modulates NMDA receptor trafficking and gating. Nat Neurosci 4:382-390.
62. Lavezzari G, McCallum J, Dewey CM, Roche KW (2004) Subunit-specific regulation of NMDA receptor endocytosis. J Neurosci 24:6383-6391.
63. Levy M, Castillo SS, Goldkorn T (2006) nSMase2 activation and trafficking are modulated by oxidative stress to induce apoptosis. Biochem Biophys Res Commun 344:900-905.
64. Lipton SA (1992) Memantine prevents HIV coat protein-induced neuronal injury in vitro. Neurology 42:1403-1405.
65. Lipton SA, Sucher NJ, Kaiser PK, Dreyer EB (1991) Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron 7:111-118.
66. Liu Y, Tang XP, McArthur JC, Scott J, Gartner S (2000) Analysis of human immunodeficiency virus type 1 gp160 sequences from a patient with HIV dementia: evidence for monocyte trafficking into brain. J Neurovirol 6 [Suppl 1]:S70-S81.
67. Masci AM, Galgani M, Cassano S, De Simone S, Gallo A, De Rosa V, Zappacosta S, Racioppi L (2003) HIV-1 gp120 induces anergy in naive T lymphocytes through CD4-independent protein kinase-A-mediated signaling. J Leukoc Biol 74:1117-1124.
68. Mattson MP, Haughey NJ, Nath A (2005) Cell death in HIV dementia. Cell Death Differ 12 [Suppl 1]:893-904.
69. McArthur JC, Steiner J, Sacktor N, Nath A (2010) Human immunodeficiency virus-associated neurocognitive disorders: mind the gap. Ann Neurol 67:699-714.
70. McMurtray A, Nakamoto B, Shikuma C, Valcour V (2008) Cortical atrophy and white matter hyperintensities in HIV: the Hawaii Aging with HIV Cohort Study. J Stroke Cerebrovasc Dis 17:212-217.
71. 2+]i and the toxic actions of the HIV coat protein GP120. Eur J Neurosci 11:1167-1178.
72. Meucci O, Miller RJ (1996) gp120-induced neurotoxicity in hippocampal pyramidal neuron cultures: protective action of TGF-β1. J Neurosci 16:4080-4088.
73. Meucci O, Fatatis A, Simen AA, Bushell TJ, Gray PW, Miller RJ (1998) Chemokines regulate hippocampal neuronal signaling and gp120 neurotoxicity. Proc Natl Acad Sci U S A 95:14500-14505.
74. 8+ lymphocytosis in HIV-1 infected patients with immune restoration induced by HAART. Acta Neuropathol 108:17-23.
75. Nicolai J, Burbassi S, Rubin J, Meucci O (2010) CXCL12 inhibits expression of the NMDA receptor's NR2B subunit through a histone deacetylasedependent pathway contributing to neuronal survival. Cell Death Dis 1:e33.
76. Nong Y, Huang YQ, Ju W, Kalia LV, Ahmadian G, Wang YT, Salter MW (2003) Glycine binding primes NMDA receptor internalization. Nature 422:302-307.
77. Norman E, Cutler RG, Flannery R, Wang Y, Mattson MP (2010) Plasma membrane sphingomyelin hydrolysis increases hippocampal neuron excitability by sphingosine-1-phosphate mediated mechanisms. J Neurochem 114:430-439.
78. O'Connell AD, Leng Q, Dong K, MacGregor GG, Giebisch G, Hebert SC (2005) Phosphorylation-regulated endoplasmic reticulum retention signal in the renal outer-medullary K_ channel (ROMK). Proc Natl Acad Sci USA. 102:9954-9959.
79. Owen DM, Williamson D, Rentero C, Gaus K (2009) Quantitative microscopy: protein dynamics and membrane organisation. Traffic 10:962-971.
80. Pandey V, Bolsover SR (2000) Immediate and neurotoxic effects of HIV protein gp120 act through CXCR4 receptor. Biochem Biophys Res Commun 274:212-215.
81. Pelle MT, Bazille C, Gray F (2008) Neuropathology and HIV dementia. Handb Clin Neurol 89:807-818.
82. Phipps DJ, Read SE, Piovesan JP, Mills GB, Branch DR (1996) HIV infection in vitro enhances the activity of src-family protein tyrosine kinases. AIDS 10:1191-1198.
83. Ping SE, Barrett GL (1998) Ceramide can induce cell death in sensory neurons, whereas ceramide analogues and sphingosine promote survival. J Neurosci Res 54:206-213.
84. Procino G, Carmosino M, Marin O, Brunati AM, Contri A, Pinna LA, Mannucci R, Nielsen S, Kwon TH, Svelto M, Valenti G (2003) Ser-256 phosphorylation dynamics of Aquaporin 2 during maturation from the ER to the vesicular compartment in renal cells. FASEB J 17:1886-1888.
85. Quinlan EM, Philpot BD, Huganir RL, Bear MF (1999) Rapid, experiencedependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci 2:352-357.
86. Ramirez SH, Potula R, Fan S, Eidem T, Papugani A, Reichenbach N, Dykstra H, Weksler BB, Romero IA, Couraud PO, Persidsky Y (2009) Methamphetamine disrupts blood-brain barrier function by induction of oxidative stress in brain endothelial cells. J Cereb Blood Flow Metab 29:1933-1945.
87. Rao A, Craig AM (1997) Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19:801-812.
88. Riboni L, Prinetti A, Bassi R, Caminiti A, Tettamanti G (1995) A mediator role of ceramide in the regulation of neuroblastoma Neuro2a cell differentiation. J Biol Chem 270:26868-26875.
89. Roche KW, Standley S, McCallum J, Dune Ly C, Ehlers MD, Wenthold RJ (2001) Molecular determinants of NMDA receptor internalization. Nat Neurosci 4:794-802.
90. Ronaldson PT, Bendayan R (2006) HIV-1 viral envelope glycoprotein gp120 triggers an inflammatory response in cultured rat astrocytes and regulates the functional expression of P-glycoprotein. Mol Pharmacol 70:1087-1098.
91. Scott DB, Blanpied TA, Swanson GT, Zhang C, Ehlers MD (2001) An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. J Neurosci 21:3063-3072.
92. Scott DB, Blanpied TA, Ehlers MD (2003) Coordinated PKA and PKC phosphorylation suppresses RXR-mediated ER retention and regulates the surface delivery of NMDA receptors. Neuropharmacology 45:755-767.
93. Scott DB, Michailidis I, Mu Y, Logothetis D, Ehlers MD (2004) Endocytosis and degradative sorting of NMDA receptors by conserved membraneproximal signals. J Neurosci 24:7096-7109.
94. Simioni S, Cavassini M, Annoni JM, Rimbault Abraham A, Bourquin I, Schiffer V, Calmy A, Chave JP, Giacobini E, Hirschel B, Du Pasquier RA (2010) Cognitive dysfunction in HIV patients despite long-standing suppression of viremia. AIDS 24:1243-1250.
95. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11:688-699.
96. Stahelin RV (2009) Lipid binding domains: more than simple lipid effectors. J Lipid Res [Suppl] 50:S299-S304.
97. Swartz KJ (2008) Sensing voltage across lipid membranes. Nature 456:891-897.
98. Tabarean IV, Korn H, Bartfai T (2006) Interleukin-1beta induces hyperpolarization and modulates synaptic inhibition in preoptic and anterior hypothalamic neurons. Neuroscience 141:1685-1695.
99. Tabatadze N, Savonenko A, Song H, Bandaru VV, Chu M, Haughey NJ (2010) Inhibition of neutral sphingomyelinase-2 perturbs brain sphingolipid balance and spatial memory in mice. J Neurosci Res 88:2940-2951.
100. Tingley WG, Ehlers MD, Kameyama K, Doherty C, Ptak JB, Riley CT, Huganir RL (1997) Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J Biol Chem 272:5157-5166.
101. Toggas SM, Masliah E, Mucke L (1996) Prevention of HIV-1 gp120- induced neuronal damage in the central nervous system of transgenic mice by the NMDA receptor antagonist memantine. Brain Res 706:303-307.
102. Toth PT, Ren D, Miller RJ (2004) Regulation of CXCR4 receptor dimerization by the chemokine SDF-1alpha and the HIV-1 coat protein gp120: a fluorescence resonance energy transfer (FRET) study. J Pharmacol Exp Ther 310:8-17.
103. Tozzi V, Balestra P, Bellagamba R, Corpolongo A, Salvatori MF, Visco- Comandini U, Vlassi C, Giulianelli M, Galgani S, Antinori A, Narciso P (2007) Persistence of neuropsychologic deficits despite long-term highly active antiretroviral therapy in patients with HIV-related neurocognitive impairment: prevalence and risk factors. J Acquir Immune Defic Syndr 45:174-182.
104. Ushijima H, Ando S, Kunisada T, Schröder HC, Klöcking HP, Kijjoa A, Müller WE (1993) HIV-1 gp120 and NMDA induce protein kinase C translocation differentially in rat primary neuronal cultures. J Acquir Immune Defic Syndr 6:339-343.
105. Valcour V, Watters MR, Williams AE, Sacktor N, McMurtray A, Shikuma C (2008) Aging exacerbates extrapyramidal motor signs in the era of highly active antiretroviral therapy. J Neurovirol 14:362-367.
106. Waldron E, Heilig C, Schweitzer A, Nadella N, Jaeger S, Martin AM, Weggen S, Brix K, Pietrzik CU (2008) LRP1 modulates APP trafficking along early compartments of the secretory pathway. Neurobiol Dis 31:188-197.
107. Washbourne P, Liu XB, Jones EG, McAllister AK (2004) Cycling of NMDA receptors during trafficking in neurons before synapse formation. J Neurosci 24:8253-8264.
108. Watt AJ, van Rossum MC, MacLeod KM, Nelson SB, Turrigiano GG (2000) Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron 26:659-670.
109. Wheeler D, Knapp E, Bandaru VV, Wang Y, Knorr D, Poirier C, Mattson MP, Geiger JD, Haughey NJ (2009) Tumor necrosis factor_ induced neutral sphingomyelinase-2 modulates synaptic plasticity by controlling the membrane insertion of NMDA receptors. J Neurochem 109:1237-1249.
110. Wu P, Price P, Du B, Hatch WC, Terwilliger EF (1996) Direct cytotoxicity of HIV-1 envelope protein gp120 on human NT neurons. Neuroreport 7:1045-1049.
111. Yang SN (2000) Ceramide-induced sustained depression of synaptic currents mediated by ionotropic glutamate receptors in the hippocampus: an essential role of postsynaptic protein phosphatases. Neuroscience 96:253-258.
112. Yao H, Duan M, Buch S (2011) Cocaine-mediated induction of plateletderived growth factor: implication for increased vascular permeability. Blood 117:2538-2547.
113. Zheng J, Thylin MR, Ghorpade A, Xiong H, Persidsky Y, Cotter R, Niemann D, Che M, Zeng YC, Gelbard HA, Shepard RB, Swartz JM, Gendelman HE (1999) Intracellular CXCR4 signaling, neuronal apoptosis and neuropathogenic mechanisms of HIV-1-associated dementia. J Neuroimmunol 98:185-200.
114. Zhou J, Shin HG, Yi J, Shen W, Williams CP, Murray KT (2002) Phosphorylation and putative ER retention signals are required for protein kinase A-mediated potentiation of cardiac sodium current. Circ Res 91:540-546.