HIV-1 gp120Bal down-Regulates Phosphorylated NMDA Receptor Subunit 1 in Cortical Neurons via Activation of Glutamate and Chemokine Receptors

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• 作者：Wenjuan Ru ; Shao-Jun Tang
• 关键词：HIV ; 1 ; gp120 ; Synapse ; NMDA receptor ; Phosphorylation
• 刊名：Journal of Neuroimmune Pharmacology
• 出版年：2016
• 出版时间：March 2016
• 年：2016
• 卷：11
• 期：1
• 页码：182-191
• 全文大小：1,692 KB
• 参考文献：Alirezaei M, Watry DD, Flynn CF, Kiosses WB, Masliah E, Williams BR, Kaul M, Lipton SA, Fox HS (2007) Human immunodeficiency virus-1/surface glycoprotein 120 induces apoptosis through RNA-activated protein kinase signaling in neurons. J Neurosci 27:11047–11055CrossRef PubMed
  Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE, Murphy PM, Berger EA (1996) CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272:1955–1958CrossRef PubMed
  Bachis A, Mocchetti I (2005) Brain-derived neurotrophic factor is neuroprotective against human immunodeficiency virus-1 envelope proteins. Neuroprotective Agents 1053:247–257
  Bachis A, Biggio F, Major EO, Mocchetti I (2009) M- and T-tropic HIVs promote apoptosis in rat neurons. J NeuroImmune Pharmacol 4:150–160PubMedCentral CrossRef PubMed
  Bachis A, Cruz MI, Mocchetti I (2010) M-tropic HIV envelope protein gp120 exhibits a different neuropathological profile than T-tropic gp120 in rat striatum. Eur J Neurosci 32:570–578PubMedCentral CrossRef PubMed
  Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A (2001) CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat Neurosci 4:702–710CrossRef PubMed
  Bliss TVP, Collingridge GL (1993) A synaptic model of memory - long-term potentiation in the hippocampus. Nature 361:31–39CrossRef PubMed
  Catani MV, Corasaniti MT, Navarra M, Nistico G, Finazzi-Agro A, Melino G (2000) gp120 induces cell death in human neuroblastoma cells through the CXCR4 and CCR5 chemokine receptors. J Neurochem 74:2373–2379CrossRef PubMed
  Chen BS, Roche KW (2007) Regulation of NMDA receptors by phosphorylation. Neuropharmacology 53:362–368PubMedCentral CrossRef PubMed
  Choe H, Farzan M, Sun Y, Sullivan N, Rollins B, Ponath PD, Wu L, Mackay CR, LaRosa G, Newman W, Gerard N, Gerard C, Sodroski J (1996) The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85:1135–1148CrossRef PubMed
  Collman R, Balliet JW, Gregory SA, Friedman H, Kolson DL, Nathanson N, Srinivasan A (1992) An infectious molecular clone of an unusual macrophage-tropic and highly cytopathic strain of human immunodeficiency virus type 1. J Virol 66:7517–7521PubMedCentral PubMed
  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 Neurovirol 10:350–357CrossRef PubMed
  Davis CB, Dikic I, Unutmaz D, Hill CM, Arthos J, Siani MA, Thompson DA, Schlessinger J, Littman DR (1997) Signal transduction due to HIV-1 envelope interactions with chemokine receptors CXCR4 or CCR5. J Exp Med 186:1793–1798PubMedCentral CrossRef PubMed
  Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, Cayanan C, Maddon PJ, Koup RA, Moore JP, Paxton WA (1996) HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667–673CrossRef PubMed
  Dreyer EB, Kaiser PK, Offermann JT, Lipton SA (1990) HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists. Science 248:364–367CrossRef PubMed
  Ellis R, Langford D, Masliah E (2007) HIV and antiretroviral therapy in the brain: neuronal injury and repair. Nat Rev Neurosci 8:33–44CrossRef PubMed
  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 9:209–217CrossRef PubMed
  Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872–877CrossRef PubMed
  Geeraerts T, Deiva K, M'Sika I, Salim H, Hery C, Tardieu M (2006) Effects of SDF-1alpha and gp120IIIB on apoptotic pathways in SK-N-SH neuroblastoma cells. Neurosci Lett 399:115–120CrossRef PubMed
  Gemignani A, Paudice P, Pittaluga A, Raiteri M (2000) The HIV-1 coat protein gp120 and some of its fragments potently activate native cerebral NMDA receptors mediating neuropeptide release. Eur J Neurosci 12:2839–2846CrossRef PubMed
  Glass JD, Wesselingh SL, Selnes OA, Mcarthur JC (1993) Clinical-neuropathologic correlation in Hiv-associated dementia. Neurology 43:2230–2237CrossRef PubMed
  Glass JD, Fedor H, Wesselingh SL, McArthur JC (1995) Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 38:755–762CrossRef PubMed
  Gonzalez-Perez MP, O'Connell O, Lin R, Sullivan WM, Bell J, Simmonds P, Clapham PR (2012) Independent evolution of macrophage-tropism and increased charge between HIV-1 R5 envelopes present in brain and immune tissue. Retrovirology 9:20PubMedCentral CrossRef PubMed
  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 75:10073–10089PubMedCentral CrossRef PubMed
  Gray L, Roche M, Churchill MJ, Sterjovski J, Ellett A, Poumbourios P, Sherieff S, Wang B, Saksena N, Purcell DF, Wesselingh S, Cunningham AL, Brew BJ, Gabuzda D, Gorry PR (2009) Tissue-specific sequence alterations in the human immunodeficiency virus type 1 envelope favoring CCR5 usage contribute to persistence of dual-tropic virus in the brain. J Virol 83:5430–5441PubMedCentral CrossRef PubMed
  Haughey NJ, Mattson MP (2002) Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J Acquir Immune Defic Syndr 31(Suppl 2):S55–S61CrossRef PubMed
  Hayward P (2004) Viral proteins cause cell death in HIV-associated dementia. Lancet Neurol 3:325CrossRef PubMed
  Heaton RK, Clifford DB, Franklin DR, Woods SP, Ake C, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Rivera-Mindt M, Vigil OR, Taylor MJ, Collier AC, Marra CM, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I, Grp C (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy CHARTER study. Neurology 75:2087–2096PubMedCentral CrossRef PubMed
  Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL, LeBlanc S, Corkran SH, Duarte NA, Clifford DB, Woods SP, Collier AC, Marra CM, Morgello S, Mindt MR, Taylor MJ, Marcotte TD, Atkinson JH, Wolfson T, Gelman BB, McArthur JC, Simpson DM, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I, Grp CH (2011) HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol 17:3–16PubMedCentral CrossRef PubMed
  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 8:595–598CrossRef PubMed
  Honore T, Davies SN, Drejer J, Fletcher EJ, Jacobsen P, Lodge D, Nielsen FE (1988) Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists. Science 241:701–703CrossRef PubMed
  Hylden JL, Wilcox GL (1980) Intrathecal morphine in mice: a new technique. Eur J Pharmacol 67:313–316CrossRef PubMed
  Igarashi T, Donau OK, Imamichi H, Dumaurier MJ, Sadjadpour R, Plishka RJ, Buckler-White A, Buckler C, Suffredini AF, Lane HC, Moore JP, Martin MA (2003) Macrophage-tropic simian/human immunodeficiency virus chimeras use CXCR4, not CCR5, for infections of rhesus macaque peripheral blood mononuclear cells and alveolar macrophages. J Virol 77:13042–13052PubMedCentral CrossRef PubMed
  Iskander S, Walsh KA, Hammond RR (2004) Human CNS cultures exposed to HIV-1 gp120 reproduce dendritic injuries of HIV-1-associated dementia. J Neuroinflammation 1:7PubMedCentral CrossRef PubMed
  Kasyanov A, Tamamura H, Fujii N, Xiong H (2006) HIV-1 gp120 enhances giant depolarizing potentials via chemokine receptor CXCR4 in neonatal rat hippocampus. Eur J Neurosci 23:1120–1128CrossRef PubMed
  Kaul M, Lipton SA (1999) Chemokines and activated macrophages in HIV gp120-induced neuronal apoptosis. Proc Natl Acad Sci U S A 96:8212–8216PubMedCentral CrossRef PubMed
  Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988–994CrossRef PubMed
  Kaul M, Ma Q, Medders KE, Desai MK, Lipton SA (2007) HIV-1 coreceptors CCR5 and CXCR4 both mediate neuronal cell death but CCR5 paradoxically can also contribute to protection. Cell Death Differ 14:296–305CrossRef PubMed
  Kim HJ, Shin AH, Thayer SA (2011) Activation of cannabinoid type 2 receptors inhibits HIV-1 envelope glycoprotein gp120-induced synapse loss. Mol Pharmacol 80:357–366PubMedCentral CrossRef PubMed
  Krogh KA, Wydeven N, Wickman K, Thayer SA (2014) HIV-1 protein Tat produces biphasic changes in NMDA-evoked increases in intracellular Ca2+ concentration via activation of Src kinase and nitric oxide signaling pathways. J Neurochem 130:642–656PubMedCentral CrossRef PubMed
  Lannuzel A, Lledo PM, Lamghitnia HO, Vincent JD, Tardieu M (1995) HIV-1 envelope proteins gp120 and gp160 potentiate NMDA-induced [Ca2+]i increase, alter [Ca2+]i homeostasis and induce neurotoxicity in human embryonic neurons. Eur J Neurosci 7:2285–2293CrossRef PubMed
  Li B, Shi Y, Shu J, Gao J, Wu P, Tang SJ (2013) Wingless-type mammary tumor virus integration site family, member 5A (Wnt5a) regulates human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein 120 (gp120)-induced expression of pro-inflammatory cytokines via the Ca2+/calmodulin-dependent protein kinase II (CaMKII) and c-Jun N-terminal kinase (JNK) signaling pathways. J Biol Chem 288:13610–13619PubMedCentral CrossRef PubMed
  Lipton SA (1992) Memantine prevents HIV coat protein-induced neuronal injury in vitro. Neurology 42:1403–1405CrossRef PubMed
  Lipton SA, Sucher NJ, Kaiser PK, Dreyer EB (1991) Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron 7:111–118CrossRef PubMed
  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 42:963–972CrossRef PubMed
  Mattson MP, Haughey NJ, Nath A (2005) Cell death in HIV dementia. Cell Death Differ 12(Suppl 1):893–904CrossRef PubMed
  McArthur JC, Brew BJ, Nath A (2005) Neurological complications of HIV infection. Lancet Neurol 4:543–555CrossRef PubMed
  Medina I, Ghose S, Ben-Ari Y (1999) Mobilization of intracellular calcium stores participates in the rise of [Ca2+]i and the toxic actions of the HIV coat protein GP120. Eur J Neurosci 11:1167–1178CrossRef PubMed
  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 95:14500–14505PubMedCentral CrossRef PubMed
  Morris RG (1989) Synaptic plasticity and learning: selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J Neurosci 9:3040–3057PubMed
  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 70:1475–1480PubMedCentral PubMed
  Pattarini R, Pittaluga A, Raiteri M (1998) The human immunodeficiency virus-1 envelope protein gp120 binds through its V3 sequence to the glycine site of N-methyl-D-aspartate receptors mediating noradrenaline release in the hippocampus. Neuroscience 87:147–157CrossRef PubMed
  Peters PJ, Bhattacharya J, Hibbitts S, Dittmar MT, Simmons G, Bell J, Simmonds P, Clapham PR (2004) Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J Virol 78:6915–6926PubMedCentral CrossRef PubMed
  Potter MC, Figuera-Losada M, Rojas C, Slusher BS (2013) Targeting the glutamatergic system for the treatment of HIV-associated neurocognitive disorders. J NeuroImmune Pharmacol 8:594–607PubMedCentral CrossRef PubMed
  Rao JS, Kim HW, Kellom M, Greenstein D, Chen M, Kraft AD, Harry GJ, Rapoport SI, Basselin M (2011) Increased neuroinflammatory and arachidonic acid cascade markers, and reduced synaptic proteins, in brain of HIV-1 transgenic rats. J Neuroinflammation 8:101PubMedCentral CrossRef PubMed
  Ru W, Peng Y, Zhong L, Tang SJ (2012) A role of the mammalian target of rapamycin (mTOR) in glutamate-induced down-regulation of tuberous sclerosis complex proteins 2 (TSC2). J Mol Neurosci 47:340–345CrossRef PubMed
  Sa MJ, Madeira MD, Ruela C, Volk B, Mota-Miranda A, Paula-Barbosa MM (2004) Dendritic changes in the hippocampal formation of AIDS patients: a quantitative golgi study. Acta Neuropathol 107:97–110CrossRef PubMed
  Sanchez-Perez AM, Felipo V (2005) Serines 890 and 896 of the NMDA receptor subunit NR1 are differentially phosphorylated by protein kinase C isoforms. Neurochem Int 47:84–91CrossRef PubMed
  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 21:3063–3072PubMed
  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 45:755–767CrossRef PubMed
  Shepherd AJ, Loo L, Gupte RP, Mickle AD, Mohapatra DP (2012) Distinct modifications in Kv2.1 channel via chemokine receptor CXCR4 regulate neuronal survival-death dynamics. J Neurosci 32:17725–17739PubMedCentral CrossRef PubMed
  Shepherd AJ, Loo L, Mohapatra DP (2013) Chemokine co-receptor CCR5/CXCR4-dependent modulation of Kv2.1 channel confers acute neuroprotection to HIV-1 glycoprotein gp120 exposure. PLoS One 8:e76698PubMedCentral CrossRef PubMed
  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 272:5157–5166CrossRef PubMed
  Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367:188–193CrossRef PubMed
  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 706:303–307CrossRef PubMed
  Tong G, Shepherd D, Jahr CE (1995) Synaptic desensitization of NMDA receptors by calcineurin. Science 267:1510–1512CrossRef PubMed
  Tovar YRLB, Kolson DL, Bandaru VV, Drewes JL, Graham DR, Haughey NJ (2013) Adenosine triphosphate released from HIV-infected macrophages regulates glutamatergic tone and dendritic spine density on neurons. J NeuroImmune Pharmacol 8:998–1009CrossRef
  Viviani B, Gardoni F, Bartesaghi S, Corsini E, Facchi A, Galli CL, Di Luca M, Marinovich M (2006) Interleukin-1 beta released by gp120 drives neural death through tyrosine phosphorylation and trafficking of NMDA receptors. J Biol Chem 281:30212–30222CrossRef PubMed
  Wang LY, Orser BA, Brautigan DL, MacDonald JF (1994) Regulation of NMDA receptors in cultured hippocampal neurons by protein phosphatases 1 and 2A. Nature 369:230–232CrossRef PubMed
  Westphal RS, Tavalin SJ, Lin JW, Alto NM, Fraser ID, Langeberg LK, Sheng M, Scott JD (1999) Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex. Science 285:93–96CrossRef PubMed
  Xu H, Bae M, Tovar-y-Romo LB, Patel N, Bandaru VV, Pomerantz D, Steiner JP, Haughey NJ (2011) The human immunodeficiency virus coat protein gp120 promotes forward trafficking and surface clustering of NMDA receptors in membrane microdomains. J Neurosci 31:17074–17090PubMedCentral CrossRef PubMed
  Yang J, Hu D, Xia J, Liu J, Zhang G, Gendelman HE, Boukli NM, Xiong H (2013) Enhancement of NMDA receptor-mediated excitatory postsynaptic currents by gp120-treated macrophages: implications for HIV-1-associated neuropathology. J NeuroImmune Pharmacol 8:921–933PubMedCentral CrossRef PubMed
  Yi Y, Isaacs SN, Williams DA, Frank I, Schols D, De Clercq E, Kolson DL, Collman RG (1999) Role of CXCR4 in cell-cell fusion and infection of monocyte-derived macrophages by primary human immunodeficiency virus type 1 (HIV-1) strains: two distinct mechanisms of HIV-1 dual tropism. J Virol 73:7117–7125PubMedCentral PubMed
  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 98:185–200CrossRef PubMed
  
• 作者单位：Wenjuan Ru (1)
  Shao-Jun Tang (1)
  
  1. Department of Neuroscience and Cell Biology, University of Texas Medical Branch, Galveston, TX, 77555, USA
  
• 刊物主题：Neurosciences; Immunology; Pharmacology/Toxicology; Virology; Cell Biology;
• 出版者：Springer US
• ISSN：1557-1904

文摘

HIV-1 envelope glycoprotein gp120 (gp120) is a major virulence protein implicated in the pathogenesis of HIV-associated neurocognitive disorders (HAND). Although gp120 has been suggested to cause synaptic and neuronal injuries by disrupting NMDA receptor (NMDAR) function, the underlying mechanism is unclear. Here, we show that gp120Bal down-regulates the phosphorylation of the NMDAR subunit1 NR1 (at Ser896 and Ser897), which is essential for NMDAR function. This effect of gp120Bal is blocked by specific antagonists of both NMDA and AMPA receptors, indicating a critical role of synaptic activation. Furthermore, AMD3100 and maraviroc, antagonists of CCR5 and CXCR4 chemokine receptors, respectively, inhibit the effect of gp120Bal on NR1, suggesting that CXCR4 and CCR5 activation are involved. These findings may provide mechanistic insights into the synaptopathogenesis caused by HIV-1 infection. Keywords HIV-1 gp120 Synapse NMDA receptor Phosphorylation