nach oben

Journal of NeuroVirology

Erschienen in:

08.03.2019 | Review

HIV-associated neurodegeneration: exploitation of the neuronal cytoskeleton

verfasst von: Erin D. Wenzel, Valeria Avdoshina, Italo Mocchetti

Erschienen in: Journal of NeuroVirology | Ausgabe 3/2019

Einloggen, um Zugang zu erhalten

Abstract

Human immunodeficiency virus-1 (HIV) infection of the central nervous system damages synapses and promotes axonal injury, ultimately resulting in HIV-associated neurocognitive disorders (HAND). The mechanisms through which HIV causes damage to neurons are still under investigation. The cytoskeleton and associated proteins are fundamental for axonal and dendritic integrity. In this article, we review evidence that HIV proteins, such as the envelope protein gp120 and transactivator of transcription (Tat), impair the structure and function of the neuronal cytoskeleton. Investigation into the effects of viral proteins on the neuronal cytoskeleton may provide a better understanding of HIV neurotoxicity and suggest new avenues for additional therapies.

Acquas E, Bachis A, Nosheny RL, Cernak I, Mocchetti I (2004) Human immunodeficiency virus type 1 protein gp120 causes neuronal cell death in the rat brain by activating caspases. Neurotox Res 5:605–615CrossRefPubMed

Adle-Biassette H, Levy Y, Colombel M, Poron F, Natchev S, Keohane C, Gray F (1995) Neuronal apoptosis in HIV infection in adults. Neuropathol Appl Neurobiol 21:218–227CrossRefPubMed

Ahmed F, MacArthur L, De Bernardi MA, Mocchetti I (2009) Retrograde and anterograde transport of HIV protein gp120 in the nervous system. Brain Behav Immun 23:355–364CrossRefPubMed

Alakkas A, Ellis RJ, Watson CW, Umlauf A, Heaton RK, Letendre S, Collier A, Marra C, Clifford DB, Gelman B, Sacktor N, Morgello S, Simpson D, McCutchan JA, Kallianpur A, Gianella S, Marcotte T, Grant I, Fennema-Notestine C, Group C (2018) White matter damage, neuroinflammation, and neuronal integrity in HAND. J Neuro-Oncol. https://doi.org/10.1007/s13365-018-0682-9

Anderson E, Zink W, Xiong H, Gendelman HE (2002) HIV-1-associated dementia: a metabolic encephalopathy perpetrated by virus-infected and immune-competent mononuclear phagocytes. J Acquir Immune Defic Syndr 31(Suppl 2):S43–S54CrossRefPubMed

Aprea S, Del Valle L, Mameli G, Sawaya BE, Khalili K, Peruzzi F (2006) Tubulin-mediated binding of human immunodeficiency virus-1 Tat to the cytoskeleton causes proteasomal-dependent degradation of microtubule-associated protein 2 and neuronal damage. J Neurosci 26:4054–4062CrossRefPubMedPubMedCentral

Avdoshina V, Taraballi F, Dedoni S, Corbo C, Paige M, Saygideger Kont Y, Uren A, Tasciotti E, Mocchetti I (2016a) Identification of a binding site of the human immunodeficiency virus envelope protein gp120 to neuronal-specific tubulin. J Neurochem 137:287–298CrossRefPubMedPubMedCentral

Avdoshina V, Fields JA, Castellano P, Dedoni S, Palchik G, Trejo M, Adame A, Rockenstein E, Eugenin E, Masliah E, Mocchetti I (2016b) The HIV protein gp120 alters mitochondrial dynamics in neurons. Neurotox Res 29:583–593CrossRefPubMedPubMedCentral

Avdoshina V, Caragher SP, Wenzel ED, Taraballi F, Mocchetti I, Harry GJ (2017) The viral protein gp120 decreases the acetylation of neuronal tubulin: potential mechanism of neurotoxicity. J Neurochem 141:606–613CrossRefPubMedPubMedCentral

Bachani M, Sacktor N, McArthur JC, Nath A, Rumbaugh J (2013) Detection of anti-tat antibodies in CSF of individuals with HIV-associated neurocognitive disorders. J Neuro-Oncol 19:82–88

Bachis A, Aden SA, Nosheny RL, Andrews PM, Mocchetti I (2006) Axonal transport of human immunodeficiency virus type 1 envelope protein glycoprotein 120 is found in association with neuronal apoptosis. J Neurosci 26:6771–6780CrossRefPubMedPubMedCentral

Bachis A, Avdoshina V, Zecca L, Parsadanian M, Mocchetti I (2012) Human immunodeficiency virus type 1 alters brain-derived neurotrophic factor processing in neurons. J Neurosci 32:9477–9484CrossRefPubMedPubMedCentral

Bachis A, Wenzel E, Boelk A, Becker J, Mocchetti I (2016) The neurotrophin receptor p75 mediates gp120-induced loss of synaptic spines in aging mice. Neurobiol Aging 46:160–168CrossRefPubMedPubMedCentral

Baird FJ, Bennett CL (2013) Microtubule defects & neurodegeneration. J Genet Syndr Gene Ther 4:203CrossRefPubMedPubMedCentral

Bamburg JR, Bernstein BW (2010) Roles of ADF/cofilin in actin polymerization and beyond. F1000 Biol Rep 2:62PubMedPubMedCentral

Bamburg JR, Bernstein BW, Davis RC, Flynn KC, Goldsbury C, Jensen JR, Maloney MT, Marsden IT, Minamide LS, Pak CW, Shaw AE, Whiteman I, Wiggan O (2010) ADF/Cofilin-actin rods in neurodegenerative diseases. Curr Alzheimer Res 7:241–250CrossRefPubMedPubMedCentral

Bansal AK, Mactutus CF, Nath A, Maragos W, Hauser KF, Booze RM (2000) Neurotoxicity of HIV-1 proteins gp120 and tat in the rat striatum. Brain Res 879:42–49CrossRefPubMed

Bar J, Kobler O, van Bommel B, Mikhaylova M (2016) Periodic F-actin structures shape the neck of dendritic spines. Sci Rep 6:37136CrossRefPubMedPubMedCentral

Behnisch T, Francesconi W, Sanna PP (2004) HIV secreted protein tat prevents long-term potentiation in the hippocampal CA1 region. Brain Res 1012:187–189CrossRefPubMed

Berth S, Caicedo HH, Sarma T, Morfini G, Brady ST (2015) Internalization and axonal transport of the HIV glycoprotein gp120. ASN Neuro 7:175909141456818CrossRef

Berthet A, Margolis EB, Zhang J, Hsieh I, Zhang J, Hnasko TS, Ahmad J, Edwards RH, Sesaki H, Huang EJ, Nakamura K (2014) Loss of mitochondrial fission depletes axonal mitochondria in midbrain dopamine neurons. J Neurosci 34:14304–14317CrossRefPubMedPubMedCentral

Bertrand SJ, Mactutus CF, Aksenova MV, Espensen-Sturges TD, Booze RM (2014) Synaptodendritic recovery following HIV Tat exposure: neurorestoration by phytoestrogens. J Neurochem 128:140–151CrossRefPubMed

Bhattacharyya A, Watson FL, Pomeroy SL, Zhang YZ, Stiles CD, Segal RA (2002) High-resolution imaging demonstrates dynein-based vesicular transport of activated Trk receptors. J Neurobiol 51:302–312CrossRefPubMed

Binder LI, Frankfurter A, Rebhun LI (1985) The distribution of tau in the mammalian central nervous system. J Cell Biol 101:1371–1378CrossRefPubMed

Bruce-Keller AJ, Chauhan A, Dimayuga FO, Gee J, Keller JN, Nath A (2003) Synaptic transport of human immunodeficiency virus-tat protein causes neurotoxicity and gliosis in rat brain. J Neurosci 23:8417–8422CrossRefPubMedPubMedCentral

Butler TR, Smith KJ, Self RL, Braden BB, Prendergast MA (2011) Neurodegenerative effects of recombinant HIV-1 Tat(1-86) are associated with inhibition of microtubule formation and oxidative stress-related reductions in microtubule-associated protein-2(a,b). Neurochem Res 36:819–828CrossRefPubMedPubMedCentral

Cambray-Deakin MA, Burgoyne RD (1987) Posttranslational modifications of alpha-tubulin: acetylated and detyrosinated forms in axons of rat cerebellum. J Cell Biol 104:1569–1574CrossRefPubMed

Cameron PU, Saleh S, Sallmann G, Solomon A, Wightman F, Evans VA, Boucher G, Haddad EK, Sekaly RP, Harman AN, Anderson JL, Jones KL, Mak J, Cunningham AL, Jaworowski A, Lewin SR (2010) Establishment of HIV-1 latency in resting CD4+ T cells depends on chemokine-induced changes in the actin cytoskeleton. Proc Natl Acad Sci U S A 107:16934–16939CrossRefPubMedPubMedCentral

Carey AN, Sypek EI, Singh HD, Kaufman MJ, McLaughlin JP (2012) Expression of HIV-Tat protein is associated with learning and memory deficits in the mouse. Behav Brain Res 229:48–56CrossRefPubMed

Carey AN, Liu X, Mintzopoulos D, Paris JJ, Muschamp JW, McLaughlin JP, Kaufman MJ (2013) Conditional Tat protein expression in the GT-tg bigenic mouse brain induces gray matter density reductions. Prog Neuro-Psychopharmacol Biol Psychiatry 43:49–54CrossRef

Carlos AJ, Tong L, Prieto GA, Cotman CW (2017) IL-1beta impairs retrograde flow of BDNF signaling by attenuating endosome trafficking. J Neuroinflammation 14:29CrossRefPubMedPubMedCentral

Cartelli D, Ronchi C, Maggioni MG, Rodighiero S, Giavini E, Cappelletti G (2010) Microtubule dysfunction precedes transport impairment and mitochondria damage in MPP+ -induced neurodegeneration. J Neurochem 115:247–258CrossRefPubMed

Chalasani SH, Baribaud F, Coughlan CM, Sunshine MJ, Lee VM, Doms RW, Littman DR, Raper JA (2003) The chemokine stromal cell-derived factor-1 promotes the survival of embryonic retinal ganglion cells. J Neurosci 23:4601–4612CrossRefPubMedPubMedCentral

Chen D, Wang M, Zhou S, Zhou Q (2002) HIV-1 Tat targets microtubules to induce apoptosis, a process promoted by the pro-apoptotic Bcl-2 relative Bim. EMBO J 21:6801–6810CrossRefPubMedPubMedCentral

Chowdary PD, Che DL, Zhang K, Cui B (2015) Retrograde NGF axonal transport--motor coordination in the unidirectional motility regime. Biophys J 108:2691–2703CrossRefPubMedPubMedCentral

Clifford DB, Ances BM (2013) HIV-associated neurocognitive disorder. Lancet Infect Dis 13:976–986CrossRefPubMedPubMedCentral

Coles CH, Bradke F (2015) Coordinating neuronal actin-microtubule dynamics. Curr Biol 25:R677–R691CrossRefPubMed

Conde C, Caceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319–332CrossRefPubMed

Crowell TA, Fletcher JL, Sereti I, Pinyakorn S, Dewar R, Krebs SJ, Chomchey N, Rerknimitr R, Schuetz A, Michael NL, Phanuphak N, Chomont N, Ananworanich J, Group RSS (2016) Initiation of antiretroviral therapy before detection of colonic infiltration by HIV reduces viral reservoirs, inflammation and immune activation. J Int AIDS Soc 19:21163CrossRefPubMedPubMedCentral

D’Este E, Kamin D, Gottfert F, El-Hady A, Hell SW (2015) STED nanoscopy reveals the ubiquity of subcortical cytoskeleton periodicity in living neurons. Cell Rep 10:1246–1251CrossRefPubMed

Dehmelt L, Halpain S (2005) The MAP2/tau family of microtubule-associated proteins. Genome Biol 6:204CrossRefPubMed

Di Stefano M, Gray F, Leitner T, Chiodi F (1996) Analysis of ENV V3 sequences from HIV-1-infected brain indicates restrained virus expression throughout the disease. J Med Virol 49:41–48CrossRefPubMed

Dickey AS, Strack S (2011) PKA/AKAP1 and PP2A/Bbeta2 regulate neuronal morphogenesis via Drp1 phosphorylation and mitochondrial bioenergetics. J Neurosci 31:15716–15726CrossRefPubMedPubMedCentral

Dixit R, Ross JL, Goldman YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 319:1086–1089CrossRefPubMedPubMedCentral

Dong J, Xiong H (2006) Human immunodeficiency virus type 1 gp120 inhibits long-term potentiation via chemokine receptor CXCR4 in rat hippocampal slices. J Neurosci Res 83:489–496CrossRefPubMed

Drewes G, Ebneth A, Preuss U, Mandelkow EM, Mandelkow E (1997) MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89:297–308CrossRefPubMed

Dumas A, Le-Bury G, Marie-Anais F, Herit F, Mazzolini J, Guilbert T, Bourdoncle P, Russell DG, Benichou S, Zahraoui A, Niedergang F (2015) The HIV-1 protein Vpr impairs phagosome maturation by controlling microtubule-dependent trafficking. J Cell Biol 211:359–372CrossRefPubMedPubMedCentral

Eira J, Silva CS, Sousa MM, Liz MA (2016) The cytoskeleton as a novel therapeutic target for old neurodegenerative disorders. Prog Neurobiol 141:61–82CrossRefPubMed

Ellis R, Langford D, Masliah E (2007) HIV and antiretroviral therapy in the brain: neuronal injury and repair. Nat Rev Neurosci 8:33–44CrossRefPubMed

Errea O, Moreno B, Gonzalez-Franquesa A, Garcia-Roves PM, Villoslada P (2015) The disruption of mitochondrial axonal transport is an early event in neuroinflammation. J Neuroinflammation 12:152CrossRefPubMedPubMedCentral

Eugenin EA, King JE, Nath A, Calderon TM, Zukin RS, Bennett MVL, Berman JW (2007) HIV-tat induces formation of an LRP-PSD-95-NMDAR-nNOS complex that promotes apoptosis in neurons and astrocytes. Proc Natl Acad Sci U S A 104:3438–3443CrossRefPubMedPubMedCentral

Everall IP, Hansen LA, Masliah E (2005) The shifting patterns of HIV encephalitis neuropathology. Neurotox Res 8:51–61CrossRefPubMed

Fields J, Dumaop W, Langford TD, Rockenstein E, Masliah E (2014) Role of neurotrophic factor alterations in the neurodegenerative process in HIV associated neurocognitive disorders. J NeuroImmune Pharmacol 9:102–116CrossRefPubMedPubMedCentral

Fields J, Dumaop W, Eleuteri S, Campos S, Serger E, Trejo M, Kosberg K, Adame A, Spencer B, Rockenstein E, He JJ, Masliah E (2015) HIV-1 Tat alters neuronal autophagy by modulating autophagosome fusion to the lysosome: implications for HIV-associated neurocognitive disorders. J Neurosci 35:1921–1938CrossRefPubMedPubMedCentral

Fields JA, Serger E, Campos S, Divakaruni AS, Kim C, Smith K, Trejo M, Adame A, Spencer B, Rockenstein E, Murphy AN, Ellis RJ, Letendre S, Grant I, Masliah E (2016) HIV alters neuronal mitochondrial fission/fusion in the brain during HIV-associated neurocognitive disorders. Neurobiol Dis 86:154–169CrossRefPubMed

Fitting S, Ignatowska-Jankowska BM, Bull C, Skoff RP, Lichtman AH, Wise LE, Fox MA, Su J, Medina AE, Krahe TE, Knapp PE, Guido W, Hauser KF (2013) Synaptic dysfunction in the hippocampus accompanies learning and memory deficits in human immunodeficiency virus type-1 Tat transgenic mice. Biol Psychiatry 73:443–453CrossRefPubMed

Fois AF, Brew BJ (2015) The potential of the CNS as a reservoir for HIV-1 infection: implications for HIV eradication. Curr HIV/AIDS Rep 12:299–303CrossRefPubMed

Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, Inokuchi K (2003) Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38:447–460CrossRefPubMed

Fulga TA, Elson-Schwab I, Khurana V, Steinhilb ML, Spires TL, Hyman BT, Feany MB (2007) Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo. Nat Cell Biol 9:139–148CrossRefPubMed

Gates TM, Cysique LA, Siefried KJ, Chaganti J, Moffat KJ, Brew BJ (2016) Maraviroc-intensified combined antiretroviral therapy improves cognition in virally suppressed HIV-associated neurocognitive disorder. AIDS 30:591–600CrossRefPubMed

Gelman BB (2015) Neuropathology of HAND with suppressive antiretroviral therapy: encephalitis and neurodegeneration reconsidered. Curr HIV/AIDS Rep 12:272–279CrossRefPubMedPubMedCentral

Ginsberg SD, Alldred MJ, Gunnam SM, Schiroli C, Lee SH, Morgello S, Fischer T (2018) Expression profiling suggests microglial impairment in human immunodeficiency virus neuropathogenesis. Ann Neurol 83:406–417CrossRefPubMedPubMedCentral

Gisslen M, Hagberg L, Brew BJ, Cinque P, Price RW, Rosengren L (2007) Elevated cerebrospinal fluid neurofilament light protein concentrations predict the development of AIDS dementia complex. J Infect Dis 195:1774–1778CrossRefPubMed

Gisslen M, Price RW, Andreasson U, Norgren N, Nilsson S, Hagberg L, Fuchs D, Spudich S, Blennow K, Zetterberg H (2016) Plasma concentration of the neurofilament light protein (NFL) is a biomarker of CNS injury in HIV infection: a cross-sectional study. EBioMedicine 3:135–140CrossRefPubMed

Gleichmann M, Mattson MP (2011) Neuronal calcium homeostasis and dysregulation. Antioxid Redox Signal 14:1261–1273CrossRefPubMedPubMedCentral

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 G (2009) White matter tract injury and cognitive impairment in human immunodeficiency virus-infected individuals. J Neuro-Oncol 15:187–195

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–S61CrossRefPubMed

Haughey NJ, Nath A, Mattson MP, Slevin JT, Geiger JD (2001) HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J Neurochem 78:457–467CrossRefPubMed

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, For the CHARTER Group (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 75:2087–2096CrossRefPubMedPubMedCentral

Heaton RK et al (2011) HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neuro-Oncol 17:3–16

Hinckelmann MV, Zala D, Saudou F (2013) Releasing the brake: restoring fast axonal transport in neurodegenerative disorders. Trends Cell Biol 23:634–643CrossRefPubMed

Hirokawa N, Shiomura Y, Okabe S (1988) Tau proteins: the molecular structure and mode of binding on microtubules. J Cell Biol 107:1449–1459CrossRefPubMed

Hirokawa N, Niwa S, Tanaka Y (2010) Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 68:610–638CrossRefPubMed

Hoffman PN, Cleveland DW, Griffin JW, Landes PW, Cowan NJ, Price DL (1987) Neurofilament gene expression: a major determinant of axonal caliber. Proc Natl Acad Sci U S A 84:3472–3476CrossRefPubMedPubMedCentral

Hotulainen P, Hoogenraad CC (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189:619–629CrossRefPubMedPubMedCentral

Hu XT (2016) HIV-1 Tat-mediated calcium dysregulation and neuronal dysfunction in vulnerable brain regions. Curr Drug Targets 17:4–14CrossRefPubMedPubMedCentral

Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, Yoshida M, Wang XF, Yao TP (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417:455–458CrossRefPubMed

Jessen Krut J, Mellberg T, Price RW, Hagberg L, Fuchs D, Rosengren L, Nilsson S, Zetterberg H, Gisslen M (2014) Biomarker evidence of axonal injury in neuroasymptomatic HIV-1 patients. PLoS One 9:e88591CrossRefPubMedPubMedCentral

Johnson TP, Nath A (2016) Protocol for detection of HIV-Tat protein in cerebrospinal fluid by a sandwich enzyme-linked immunosorbent assay. Methods Mol Biol 1354:343–352CrossRefPubMed

Kanmogne G, Grammas P, Kennedy R (2000) Analysis of human endothelial cells and cortical neurons for susceptibility to HIV-1 infection and co-receptor expression. J Neuro-Oncol 6:519–528

Kanmogne GD, Kennedy RC, Grammas P (2002) HIV-1 gp120 proteins and gp160 peptides are toxic to brain endothelial cells and neurons: possible pathway for HIV entry into the brain and HIV-associated dementia. J Neuropathol Exp Neurol 61:992–1000CrossRefPubMed

Kaul M, Garden G, Lipton S (2001) Pathways to neuronal injury and apotosis in HIV-associated dementia. Nature 410:988–994CrossRefPubMed

Keys B, Karis J, Fadeel B, Valentin A, Norkrans G, Hagberg L, Chiodi F (1993) V3 sequences of paired HIV-1 isolates from blood and cerebrospinal fluid cluster according to host and show variation related to the clinical stage of disease. Virology 196:475–483CrossRefPubMed

Khalil M, Teunissen CE, Otto M, Piehl F, Sormani MP, Gattringer T, Barro C, Kappos L, Comabella M, Fazekas F, Petzold A, Blennow K, Zetterberg H, Kuhle J (2018) Neurofilaments as biomarkers in neurological disorders. Nat Rev Neurol 10:577–589

Klein RS, Williams KC, Alvarez-Hernandez X, Westmoreland S, Force T, Lackner AA, Luster AD (1999) Chemokine receptor expression and signaling in macaque and human fetal neurons and astrocytes: implications for the neuropathogenesis of AIDS. J Immunol 163:1636–1646PubMed

Koka P, He K, Camerini D, Tran T, Yashar SS, Merrill JE (1995) The mapping of HIV-1 gp160 epitopes required for interleukin-1 and tumor necrosis factor alpha production in glial cells. J Neuroimmunol 57:179–191CrossRefPubMed

Konietzny A, Bar J, Mikhaylova M (2017) Dendritic actin cytoskeleton: structure, functions, and regulations. Front Cell Neurosci 11:147CrossRefPubMedPubMedCentral

Krogh KA, Lyddon E, Thayer SA (2015) HIV-1 Tat activates a RhoA signaling pathway to reduce NMDA-evoked calcium responses in hippocampal neurons via an actin-dependent mechanism. J Neurochem 132:354–366CrossRefPubMed

Krucker T, Toggas SM, Mucke L, Siggins GR (1998) Transgenic mice with cerebral expression of human immunodeficiency virus type-1 coat protein gp120 show divergent changes in short- and long-term potentiation in CA1 hippocampus. Neuroscience 83:691–700CrossRefPubMed

Krucker T, Siggins GR, Halpain S (2000) Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci U S A 97:6856–6861CrossRefPubMedPubMedCentral

Kumar AM, Ownby RL, Waldrop-Valverde D, Fernandez B, Kumar M (2011) Human immunodeficiency virus infection in the CNS and decreased dopamine availability: relationship with neuropsychological performance. J Neuro-Oncol 17:26–40

Kyei GB, Dinkins C, Davis AS, Roberts E, Singh SB, Dong C, Wu L, Kominami E, Ueno T, Yamamoto A, Federico M, Panganiban A, Vergne I, Deretic V (2009) Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J Cell Biol 186:255–268CrossRefPubMedPubMedCentral

Langford D, Grigorian A, Hurford R, Adame A, Crews L, Masliah E (2004) The role of mitochondrial alterations in the combined toxic effects of human immunodeficiency virus Tat protein and methamphetamine on calbindin positive-neurons. J Neuro-Oncol 10:327–337

Langford D, Oh Kim B, Zou W, Fan Y, Rahimain P, Liu Y, He JJ (2018) Doxycycline-inducible and astrocyte-specific HIV-1 Tat transgenic mice (iTat) as an HIV/neuroAIDS model. J Neuro-Oncol 24:168–179

Lee MH, Amin ND, Venkatesan A, Wang T, Tyagi R, Pant HC, Nath A (2013) Impaired neurogenesis and neurite outgrowth in an HIV-gp120 transgenic model is reversed by exercise via BDNF production and Cdk5 regulation. J Neuro-Oncol 19:418–431

Levy M, Faas GC, Saggau P, Craigen WJ, Sweatt JD (2003) Mitochondrial regulation of synaptic plasticity in the hippocampus. J Biol Chem 278:17727–17734CrossRefPubMed

Lewis SA, Wang DH, Cowan NJ (1988) Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science 242:936–939CrossRefPubMed

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 55:362–371CrossRefPubMed

Li W, Huang Y, Reid R, Steiner J, Malpica-Llanos T, Darden TA, Shankar SK, Mahadevan A, Satishchandra P, Nath A (2008) NMDA receptor activation by HIV-Tat protein is clade dependent. J Neurosci 28:12190–12198CrossRefPubMedPubMedCentral

Liem RK, Messing A (2009) Dysfunctions of neuronal and glial intermediate filaments in disease. J Clin Invest 119:1814–1824CrossRefPubMedPubMedCentral

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 6:1380–1387CrossRefPubMed

Lucera MB, Fleissner Z, Tabler CO, Schlatzer DM, Troyer Z, Tilton JC (2017) HIV signaling through CD4 and CCR5 activates rho family GTPases that are required for optimal infection of primary CD4+ T cells. Retrovirology 14:4CrossRefPubMedPubMedCentral

Maday S, Wallace KE, Holzbaur EL (2012) Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J Cell Biol 196:407–417CrossRefPubMedPubMedCentral

Mahy M, Autenrieth CS, Stanecki K, Wynd S (2014) Increasing trends in HIV prevalence among people aged 50 years and older: evidence from estimates and survey data. AIDS 28(Suppl 4):S453–S459CrossRefPubMed

Maragos WF, Tillman P, Jones M, Bruce-Keller AJ, Roth S, Bell JE, Nath A (2003) Neuronal injury in hippocampus with human immunodeficiency virus transactivating protein, tat. Neuroscience 117:43–53CrossRefPubMed

Mariga A, Mitre M, Chao MV (2017) Consequences of brain-derived neurotrophic factor withdrawal in CNS neurons and implications in disease. Neurobiol Dis 97:73–79CrossRefPubMed

Masliah E, Achim CL, Ge N, DeTeresa R, Terry RD, Wiley CA (1992) Spectrum of human immunodeficiency virus-associated neocortical damage. Ann Neurol 32:321–329CrossRefPubMed

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 42:963–972CrossRefPubMed

Matus A (2000) Actin-based plasticity in dendritic spines. Science 290:754–758CrossRefPubMed

Maung R, Hoefer MM, Sanchez AB, Sejbuk NE, Medders KE, Desai MK, Catalan IC, Dowling CC, de Rozieres CM, Garden GA, Russo R, Roberts AJ, Williams R, Kaul M (2014) CCR5 knockout prevents neuronal injury and behavioral impairment induced in a transgenic mouse model by a CXCR4-using HIV-1 glycoprotein 120. J Immunol 193:1895–1910CrossRefPubMed

McArthur JC (2004) HIV dementia: an evolving disease. J Neuroimmunol 157:3–10CrossRefPubMed

McCarthy M, Vidaurre I, Geffin R (2006) Maturing neurons are selectively sensitive to human immunodeficiency virus type 1 exposure in differentiating human neuroepithelial progenitor cell cultures. J Neuro-Oncol 12:333–348

McMurray C (2000) Nerurodegeration: diseases of the cytoskeleton? Cell Death Differ 7:861–865CrossRefPubMed

Melli G, Keswani SC, Fischer A, Chen W, Hoke A (2006) Spatially distinct and functionally independent mechanisms of axonal degeneration in a model of HIV-associated sensory neuropathy. Brain 129:1330–1338CrossRefPubMed

Merrill RA, Dagda RK, Dickey AS, Cribbs JT, Green SH, Usachev YM, Strack S (2011) Mechanism of neuroprotective mitochondrial remodeling by PKA/AKAP1. PLoS Biol 9:e1000612CrossRefPubMedPubMedCentral

Millecamps S, Julien JP (2013) Axonal transport deficits and neurodegenerative diseases. Nat Rev Neurosci 14:161–176CrossRefPubMed

Minamide LS, Striegl AM, Boyle JA, Meberg PJ, Bamburg JR (2000) Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat Cell Biol 2:628–636CrossRefPubMed

Mocchetti I, Bachis A, Campbell LA, Avdoshina V (2014) Implementing neuronal plasticity in NeuroAIDS: the experience of brain-derived neurotrophic factor and other neurotrophic factors. J NeuroImmune Pharmacol 9:80–91CrossRefPubMed

Nath A (2002) Human immunodeficiency virus (HIV) proteins in neuropathologenesis of HIV dementia. J Infect Dis 186:S193–S198CrossRefPubMed

Nichols MJ, Gates TM, Soares JR, Moffat KJ, Rae CD, Brew BJ, Cysique LA (2018) Atrophic brain signatures of mild forms of neurocognitive impairment in virally suppressed HIV infection. AIDS:1. https://doi.org/10.1097/QAD.0000000000002042

Nogales E, Wolf SG, Downing KH (1998) Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391:199–203CrossRefPubMed

Nonaka M, Ma BY, Ohtani M, Yamamoto A, Murata M, Totani K, Ito Y, Miwa K, Nogami W, Kawasaki N, Kawasaki T (2007) Subcellular localization and physiological significance of intracellular mannan-binding protein. J Biol Chem 282:17908–17920CrossRefPubMed

Olson KR, McIntosh JR, Olmsted JB (1995) Analysis of MAP 4 function in living cells using green fluorescent protein (GFP) chimeras. J Cell Biol 130:639–650CrossRefPubMed

Ordonez DG, Lee MK, Feany MB (2018) Alpha-synuclein induces mitochondrial dysfunction through spectrin and the actin cytoskeleton. Neuron 97(108–124):e106

Ospina Stella A, Turville S (2018) All-round manipulation of the actin cytoskeleton by HIV. Viruses 10:63CrossRefPubMedCentral

Pacheco A, Gallo G (2016) Actin filament-microtubule interactions in axon initiation and branching. Brain Res Bull 126:300–310CrossRefPubMedPubMedCentral

Petito C, Roberts B (1995) Evidence of apoptic cell death in HIV encephalitis. Am J Pathol 146:1121–1130PubMedPubMedCentral

Price RW, Brew B, Sidtis J, Rosenblum M, Scheck AC, Cleary P (1988) The brain in AIDS: central nervous system HIV-1 infection and AIDS dementia complex. Science 239:586–592CrossRefPubMed

Qu Y, Hahn I, Webb SE, Pearce SP, Prokop A (2017) Periodic actin structures in neuronal axons are required to maintain microtubules. Mol Biol Cell 28:296–308CrossRefPubMedPubMedCentral

Quinlan EM, Halpain S (1996) Postsynaptic mechanisms for bidirectional control of MAP2 phosphorylation by glutamate receptors. Neuron 16:357–368CrossRefPubMed

Rajakyla EK, Vartiainen MK (2014) Rho, nuclear actin, and actin-binding proteins in the regulation of transcription and gene expression. Small GTPases 5:e27539CrossRefPubMedPubMedCentral

Raybuck JD, Hargus NJ, Thayer SA (2017) A GluN2B-selective NMDAR antagonist reverses synapse loss and cognitive impairment produced by the HIV-1 protein Tat. J Neurosci 37:7837–7847CrossRefPubMedPubMedCentral

Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16:2166–2172CrossRefPubMed

Rivieccio MA, Brochier C, Willis DE, Walker BA, D’Annibale MA, McLaughlin K, Siddiq A, Kozikowski AP, Jaffrey SR, Twiss JL, Ratan RR, Langley B (2009) HDAC6 is a target for protection and regeneration following injury in the nervous system. Proc Natl Acad Sci U S A 106:19599–19604CrossRefPubMedPubMedCentral

Rozzi SJ, Avdoshina V, Fields JA, Mocchetti I (2018) Human immunodeficiency virus Tat impairs mitochondrial fission in neurons. Cell Death Discov 4:8CrossRefPubMedPubMedCentral

Rubin LH, Sacktor N, Creighton J, Du Y, Endres CJ, Pomper MG, Coughlin JM (2018) Microglial activation is inversely associated with cognition in individuals living with HIV on effective antiretroviral therapy. AIDS 32:1661–1667CrossRefPubMed

Sabatier J, Vives E, Marbrouk 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 65:961–967PubMedPubMedCentral

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 Neuro-Oncol 8:136–142

Sainath R, Gallo G (2015) The dynein inhibitor Ciliobrevin D inhibits the bidirectional transport of organelles along sensory axons and impairs NGF-mediated regulation of growth cones and axon branches. Dev Neurobiol 75:757–777CrossRefPubMed

Sanchez C, Diaz-Nido J, Avila J (2000) Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobiol 61:133–168CrossRefPubMed

Sanchez-Alavez M, Criado J, Gomez-Chavarin M, Jimenez-Anguiano A, Navarro L, Diaz-Ruiz O, Galicia O, Sanchez-Narvaez F, Murillo-Rodriguez E, Henriksen SJ, Elder JH, Prospero-Garcia O (2000) HIV- and FIV-derived gp120 alter spatial memory, LTP, and sleep in rats. Neurobiol Dis 7:384–394CrossRefPubMed

Sandler NG, Sereti I (2014) Can early therapy reduce inflammation? Curr Opin HIV AIDS 9:72–79CrossRefPubMedPubMedCentral

Saylor D, Dickens AM, Sacktor N, Haughey N, Slusher B, Pletnikov M, Mankowski JL, Brown A, Volsky DJ, McArthur JC (2016) HIV-associated neurocognitive disorder--pathogenesis and prospects for treatment. Nat Rev Neurol 12:234–248CrossRefPubMedPubMedCentral

Schifitto G, Yiannoutsos CT, Ernst T, Navia BA, Nath A, Sacktor N, Anderson C, Marra CM, Clifford DB, Team A (2009) Selegiline and oxidative stress in HIV-associated cognitive impairment. Neurology 73:1975–1981CrossRefPubMedPubMedCentral

Sheppard DP, Iudicello JE, Bondi MW, Doyle KL, Morgan EE, Massman PJ, Gilbert PE, Woods SP (2015) Elevated rates of mild cognitive impairment in HIV disease. J Neuro-Oncol 21:576–584

Shin AH, Kim HJ, Thayer SA (2012) Subtype selective NMDA receptor antagonists induce recovery of synapses lost following exposure to HIV-1 tat. Br J Pharmacol 166:1002–1017CrossRefPubMedPubMedCentral

Sit ST, Manser E (2011) Rho GTPases and their role in organizing the actin cytoskeleton. J Cell Sci 124:679–683CrossRefPubMed

Song Y, Brady ST (2015) Post-translational modifications of tubulin: pathways to functional diversity of microtubules. Trends Cell Biol 25:125–136CrossRefPubMed

Song L, Nath A, Geiger JD, Moore A, Hochman S (2003) Human immunodeficiency virus type 1 Tat protein directly activates neuronal N-methyl-D-aspartate receptors at an allosteric zinc-sensitive site. J Neuro-Oncol 9:399–403

Steiner JP, Bachani M, Wolfson-Stofko B, Lee MH, Wang T, Li G, Li W, Strayer D, Haughey NJ, Nath A (2015) Interaction of paroxetine with mitochondrial proteins mediates neuroprotection. Neurotherapeutics 12:200–216CrossRefPubMed

Stern JL, Lessard DV, Hoeprich GJ, Morfini GA, Berger CL (2017) Phosphoregulation of Tau modulates inhibition of kinesin-1 motility. Mol Biol Cell 28:1079–1087CrossRefPubMedPubMedCentral

Stumm RK, Zhou C, Ara T, Lazarini F, Dubois-Dalcq M, Nagasawa T, Hollt V, Schulz S (2003) CXCR4 regulates interneuron migration in the developing neocortex. J Neurosci 23:5123–5130CrossRefPubMedPubMedCentral

Szabo EC, Manguinhas R, Fonseca R (2016) The interplay between neuronal activity and actin dynamics mimic the setting of an LTD synaptic tag. Sci Rep 6:33685CrossRefPubMedPubMedCentral

Tan IL, McArthur JC (2011) HIV-associated central nervous system diseases in the era of combination antiretroviral therapy. Eur J Neurol 18:371–372CrossRefPubMed

Teodorof C, Divakar S, Soontornniyomkij B, Achim CL, Kaul M, Singh KK (2014) Intracellular mannose binding lectin mediates subcellular trafficking of HIV-1 gp120 in neurons. Neurobiol Dis 69:54–64CrossRefPubMedPubMedCentral

Teodorof-Diedrich C, Spector SA (2018) Human immunodeficiency virus Type-1 gp120 and Tat induce mitochondrial fragmentation and incomplete mitophagy in human neurons. J Virol. https://doi.org/10.1128/JVI.00993-18

Terman JR, Kashina A (2013) Post-translational modification and regulation of actin. Curr Opin Cell Biol 25:30–38CrossRefPubMed

Tian L, Stefanidakis M, Ning L, Van Lint P, Nyman-Huttunen H, Libert C, Itohara S, Mishina M, Rauvala H, Gahmberg CG (2007) Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage. J Cell Biol 178:687–700CrossRefPubMedPubMedCentral

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 367:188–193CrossRefPubMed

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 45:174–182CrossRefPubMed

Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J, Deeney JT, Corkey BE, Shirihai OS (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27:433–446CrossRefPubMedPubMedCentral

Uchimura S, Oguchi Y, Katsuki M, Usui T, Osada H, Nikawa J, Ishiwata S, Muto E (2006) Identification of a strong binding site for kinesin on the microtubule using mutant analysis of tubulin. EMBO J 25:5932–5941CrossRefPubMedPubMedCentral

Vallee RB, Williams JC, Varma D, Barnhart LE (2004) Dynein: an ancient motor protein involved in multiple modes of transport. J Neurobiol 58:189–200CrossRefPubMed

van der Bliek AM, Shen Q, Kawajiri S (2013) Mechanisms of mitochondrial fission and fusion. Cold Spring Harb Perspect Biol 5:a011072

Verhey KJ, Hammond JW (2009) Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 10:765–777CrossRefPubMed

Villeneuve LM, Purnell PR, Stauch KL, Callen SE, Buch SJ, Fox HS (2016) HIV-1 transgenic rats display mitochondrial abnormalities consistent with abnormal energy generation and distribution. J Neuro-Oncol 22:564–574

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 281:30212–30222CrossRefPubMed

Wenzel ED, Bachis A, Avdoshina V, Taraballi F, Tasciotti E, Mocchetti I (2017) Endocytic trafficking of HIV gp120 is mediated by dynamin and plays a role in gp120 neurotoxicity. J NeuroImmune Pharmacol 12:492–503CrossRefPubMedPubMedCentral

Westermann B (2010) Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 11:872–884CrossRefPubMed

Westermann S, Weber K (2003) Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol 4:938–947CrossRefPubMed

Wiley CA, Achim C (1994) Human immunodeficiency virus encephalitis is the pathological correlate of dementia in acquired immunodeficiency syndrome. Ann Neurol 36:673–676CrossRefPubMed

Yang G, Pan F, Gan WB (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462:920–924CrossRefPubMedPubMedCentral

Yang Y, Wu J, Lu Y (2010) Mechanism of HIV-1-TAT induction of interleukin-1beta from human monocytes: involvement of the phospholipase C/protein kinase C signaling cascade. J Med Virol 82:735–746CrossRefPubMedPubMedCentral

Yuan A, Rao MV, Veeranna, Nixon RA (2012) Neurofilaments at a glance. J Cell Sci 125:3257–3263CrossRefPubMedPubMedCentral

Zhao X, Chen XQ, Han E, Hu Y, Paik P, Ding Z, Overman J, Lau AL, Shahmoradian SH, Chiu W, Thompson LM, Wu C, Mobley WC (2016) TRiC subunits enhance BDNF axonal transport and rescue striatal atrophy in Huntington’s disease. Proc Natl Acad Sci U S A 113:E5655–E5664CrossRefPubMedPubMedCentral

Zhou FQ, Snider WD (2005) Cell biology. GSK-3beta and microtubule assembly in axons. Science 308:211–214CrossRefPubMed

Zhu J, Ananthan S, Zhan CG (2018) The role of human dopamine transporter in NeuroAIDS. Pharmacol Ther 183:78–89CrossRefPubMed

Titel: HIV-associated neurodegeneration: exploitation of the neuronal cytoskeleton
verfasst von: Erin D. Wenzel
Valeria Avdoshina
Italo Mocchetti
Publikationsdatum: 08.03.2019
Verlag: Springer International Publishing
Erschienen in: Journal of NeuroVirology / Ausgabe 3/2019
Print ISSN: 1355-0284
Elektronische ISSN: 1538-2443
DOI: https://doi.org/10.1007/s13365-019-00737-y

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Frühe Alzheimertherapie lohnt sich

25.04.2024 AAN-Jahrestagung 2024 Nachrichten

Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.

Viel Bewegung in der Parkinsonforschung

25.04.2024 Parkinson-Krankheit Nachrichten

Neue arznei- und zellbasierte Ansätze, Frühdiagnose mit Bewegungssensoren, Rückenmarkstimulation gegen Gehblockaden – in der Parkinsonforschung tut sich einiges. Auf dem Deutschen Parkinsonkongress ging es auch viel um technische Innovationen.

Demenzkranke durch Antipsychotika vielfach gefährdet

23.04.2024 Demenz Nachrichten

Wenn Demenzkranke aufgrund von Symptomen wie Agitation oder Aggressivität mit Antipsychotika behandelt werden, sind damit offenbar noch mehr Risiken verbunden als bislang angenommen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 3/2019

Self-initiated continuation of and adherence to HIV pre-exposure prophylaxis (PrEP) after PrEP demonstration project roll-off in men who have sex with men: associations with risky decision making, impulsivity/disinhibition, and sensation seeking

High-dose corticosteroids for acute cytomegalovirus-associated transverse myelitis in the immunocompetent patient: a case report and systematic review

Human T cell leukemia virus type 1 and Zika virus: tale of two reemerging viruses with neuropathological sequelae of public health concern

Acute paraplegia due to schistosomiasis: an uncommon cause in developed countries

Microglial cell depletion is fatal with low level picornavirus infection of the central nervous system