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Citations to this article

Apoptosis induced by HIV-1 infection of the central nervous system.
B Shi, … , J Busciglio, D Gabuzda
B Shi, … , J Busciglio, D Gabuzda
Published November 1, 1996
Citation Information: J Clin Invest. 1996;98(9):1979-1990. https://doi.org/10.1172/JCI119002.
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Research Article

Apoptosis induced by HIV-1 infection of the central nervous system.

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Abstract

Apoptosis plays a role in AIDS pathogenesis in the immune system, but its role in HIV-1-induced neurological disease is unknown. In this study, we examine apoptosis induced by HIV-1 infection of the central nervous system (CNS) in an in vitro model and in brain tissue from AIDS patients. HIV-1 infection of primary brain cultures induced apoptosis in neurons and astrocytes in vitro as determined by terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling (TUNEL) and propidium iodide staining and by electron microscopy. Apoptosis was not significantly induced until 1-2 wk after the time of peak virus production, suggesting induction by soluble factors rather than by direct viral infection. Apoptosis of neurons and astrocytes was also detected in brain tissue from 10/11 AIDS patients, including 5/5 patients with HIV-1 dementia and 4/5 nondemented patients. In addition, endothelial cell apoptosis was frequently detected in the brain of AIDS patients and was confirmed by electron microscopy. Most of the apoptotic cells were not localized adjacent to HIV-1-infected cells, providing further evidence for induction by soluble factors. In six non-AIDS control patients with normal brain, apoptotic cells were absent or limited to rare astrocytes. However, TUNEL-positive neurons and astrocytes were frequently detected in seven patients with Alzheimer's disease or abundant senile plaques. These studies suggest that apoptosis is a mechanism of CNS injury in AIDS which is likely to be induced by soluble factors. The apoptosis of endothelial cells in the CNS raises the possibility that some of these factors may be blood-derived.

Authors

B Shi, U De Girolami, J He, S Wang, A Lorenzo, J Busciglio, D Gabuzda

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Detection of HIV-1 DNA in microglia/macrophages, astrocytes and neurons isolated from brain tissue with HIV-1 encephalitis by laser capture microdissection.
Trillo-Pazos G, Diamanturos A, Rislove L, Menza T, Chao W, Belem P, Sadiq S, Morgello S, Sharer L, Volsky DJ
Brain Pathology 2003
Angiogenic effects of extracellular human immunodeficiency virus type 1 Tat protein and its role in the pathogenesis of AIDS-associated Kaposi's sarcoma
G Barillari, B Ensoli
Clinical microbiology reviews 2002
HIV associated thrombotic microangiopathy
S Ahmed, RK Siddiqui, AK Siddiqui, SA Zaidi, J Cervia
Postgraduate medical journal 2002
Altered Metabolism of the Amyloid β Precursor Protein Is Associated with Mitochondrial Dysfunction in Down's Syndrome
J Busciglio, A Pelsman, C Wong, G Pigino, M Yuan, H Mori, BA Yankner
Neuron 2002
Advances in Cell Aging and Gerontology
T Fülöp, K Hirokawa, G Dupuis, A Larbi, G Pawelec
Advances in Cell Aging and Gerontology 2002
Ethanol Strongly Potentiates Apoptosis Induced by HIV-1 Proteins in Primary Human Brain Microvascular Endothelial Cells
E Acheampong, M Mukhtar, Z Parveen, N Ngoubilly, N Ahmad, C Patel, RJ Pomerantz
Virology 2002
Universes in Delicate Balance
RH Miller, S Robinson
Universes in Delicate Balance 2002
Neuropathogenesis of central nervous system HIV-1 infection
DL Kolson
Clinics in Laboratory Medicine 2002
Progress in Clinical Neurosciences: The Neuropathogenesis of HIV Infection: Host-Virus Interaction and the Impact of Therapy
C Power, MJ Gill, RT Johnson
CAN J NEUROL SCI 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
GD Kanmogne, RC Kennedy, P Grammas
Journal of Neuropathology and Experimental Neurology 2002
Neuropathological Changes in a Mouse Model of Progressive Myoclonus Epilepsy: Cystatin B Deficiency and Unverricht-Lundborg Disease
P Shannon, LA Pennacchio, MK Houseweart, BA Minassian, RM Myers
Journal of Neuropathology and Experimental Neurology 2002
Development of a Human Neuronal Cell Model for Human Immunodeficiency Virus (HIV)-Infected Macrophage-Induced Neurotoxicity: Apoptosis Induced by HIV Type 1 Primary Isolates and Evidence for Involvement of the Bcl-2/Bcl-xL-Sensitive Intrinsic Apoptosis Pathway
W Chen, J Sulcove, I Frank, S Jaffer, H Ozdener, DL Kolson
Journal of virology 2002
Increased CCR5 Affinity and Reduced CCR5/CD4 Dependence of a Neurovirulent Primary Human Immunodeficiency Virus Type 1 Isolate
PR Gorry, J Taylor, GH Holm, A Mehle, T Morgan, M Cayabyab, M Farzan, H Wang, JE Bell, K Kunstman, JP Moore, SM Wolinsky, D Gabuzda
Journal of virology 2002
Microglia in human immunodeficiency virus-associated neurodegeneration
GA Garden
Glia 2002
Identification and cloning of human astrocyte genes displaying elevated expression after infection with HIV-1 or exposure to HIV-1 envelope glycoprotein by rapid subtraction hybridization, RaSH
Z Su, D Kang, Y Chen, O Pekarskaya, W Chao, DJ Volsky, PB Fisher
Oncogene 2002
Protective and Pathological Immune Responses in the CNS
B Dietzschold, JA Richt
2002
Caspase cascades in human immunodeficiency virus-associated neurodegeneration
Gwenn A Garden, Samantha L Budd, Elena Tsai, Lisa Hanson, Marcus Kaul, Danielle M D'Emilia, Robert M Friedlander, Junying Yuan, Eliezer Masliah, Stuart A Lipton
The Journal of neuroscience : the official journal of the Society for Neuroscience 2002
Insights into the role of immune activation in HIV neuropathogenesis.
Gartner S, Liu Y
Journal of Neurovirology 2002
Lentiviral expression of HIV-1 Vpr induces apoptosis in human neurons.
Patel CA, Mukhtar M, Harley S, Kulkosky J, Pomerantz RJ
Journal of Neurovirology 2002
Caspase Cascades in Human Immunodeficiency Virus-Associated Neurodegeneration
Garden GA, Budd SL, Tsai E, Hanson L, Kaul M, D'Emilia DM, Friedlander RM, Yuan J, Masliah E, Lipton SA
Journal of Neuroscience 2002
ROLE OF CD23 IN ASTROCYTES INFLAMMATORY REACTION DURING HIV-1 RELATED ENCEPHALITIS
N Dugas, C Lacroix, E Kilchherr, JF Delfraissy, M Tardieu
Cytokine 2001
CPI-1189 attenuates effects of suspected neurotoxins associated with AIDS dementia: a possible role for ERK activation
L Pulliam, I Irwin, L Kusdra, H Rempel, WD Flitter, WA Garland
Brain Research 2001
Microglia in HIV-associated neurological diseases
JD Glass, SL Wesselingh
Microscopy Research and Technique 2001
Pathways to neuronal injury and apoptosis in HIV-associated dementia
M Kaul, GA Garden, SA Lipton
Nature 2001
Neuronal Apoptosis Mediated by IL-1β Expression in Viral Encephalitis Caused by a Neuroadapted Strain of the Mumps Virus (Kilham Strain) in Hamsters
S Takikita, T Takano, T Narita, M Takikita, M Ohno, M Shimada
Experimental Neurology 2001
Reduction in glial immunity and neuropathology by a PAF antagonist and an MMP and TNFα inhibitor in SCID mice with HIV-1 encephalitis
Y Persidsky, J Limoges, J Rasmussen, J Zheng, A Gearing, HE Gendelman
Journal of Neuroimmunology 2001
Correlation between neurological progression and astrocyte apoptosis in HIV-associated dementia
KA Thompson, JC McArthur, SL Wesselingh
Annals of Neurology 2001
HIV Type 1 Infection of Human Astrocytes Is Restricted by Inefficient Viral Entry
B Schweighardt, WJ Atwood
AIDS Research and Human Retroviruses 2001
HIV-1 infected immune competent mononuclear phagocytes influence the pathways to neuronal demise
J Zheng, MR Thylin, Y Persidsky, CE Williams, RL Cotter, W Zink, L Ryan, A Ghorpade, K Lewis, HE Gendelman
Neurotoxicity Research 2001
The Efficacy of Potent Anti-retroviral Drug Combinations Tested in a Murine Model of HIV-1 Encephalitis
J Limoges, L Poluektova, W Ratanasuwan, J Rasmussen, M Zelivyanskaya, DR McClernon, ER Lanier, HE Gendelman, Y Persidsky
Virology 2001
Neuropathology of NFHgp160 Transgenic Mice Expressing HIV-1 Env protein in Neurons
J Michaud, R Fajardo, G Charron, A Sauvageau, F Berrada, D Ramla, H Dilhuydy, Y Robitaille, A Kessous-Elbaz
Journal of Neuropathology and Experimental Neurology 2001
Detection of HIV-1 Gene Sequences in Hippocampal Neurons Isolated from postmortem AIDS Brains by Laser Capture Microdissection
J Torres-Muñoz, P Stockton, N Tacoronte, B Roberts, RR Maronpot, CK Petito
Journal of Neuropathology and Experimental Neurology 2001
The Mechanisms of Neuronal Damage in Virus Infections of the Nervous System
G Gosztonyi
2001
Chemokines and viral diseases of the central nervous system.
Asensio VC, Campbell IL
Advances in virus research 2001
CXCR4 is the primary receptor for feline immunodeficiency virus in astrocytes.
Nakagaki K, Nakagaki K, Takahashi K, Schols D, De Clercq E, Tabira T
Journal of Neurovirology 2001
HIV-1 infected immune competent mononuclear phagocytes influence the pathways to neuronal demise.
Zheng J, Thylin MR, Persidsky Y, Williams CE, Cotter RL, Zink W, Ryan L, Ghorpade A, Lewis K, Gendelman HE
Neurotoxicity Research 2001
Microglial activation precedes acute neurodegeneration in Sandhoff disease and is suppressed by bone marrow transplantation
R Wada, CJ Tifft, RL Proia
Proceedings of the National Academy of Sciences 2000
Could Nef and Vpr Proteins Contribute to Disease Progression by Promoting Depletion of Bystander Cells and Prolonged Survival of HIV-Infected Cells?
AA Azad
Biochemical and Biophysical Research Communications 2000
Expression of multiple functional chemokine receptors and monocyte chemoattractant protein-1 in human neurons
VG Sasseville, MM Smith, CR Mackay, DR Pauley, KG Mansfield, DJ Ringler, AA Lackner
Neuroscience 2000
Apoptosis: ser o no ser, ésa es la cuestión
M Vaquero
Medicina Clínica 2000
The Effects of HIV Infection on Endothelial Function
D Chi, J Henry, J Kelley, R Thorpe, JK Smith, G Krishnaswamy
Endothelium : journal of endothelial cell research 2000
Damage and Repair of DNA in HIV Encephalitis
CA Wiley, CL Achim, R Hammond, S Love, E Masliah, L Radhakrishnan, V Sanders, G Wang
Journal of Neuropathology and Experimental Neurology 2000
Human Immunodeficiency Virus Type 1 Vpr Induces Apoptosis in Human Neuronal Cells
CA Patel, M Mukhtar, RJ Pomerantz
Journal of virology 2000
Apelin, the Natural Ligand of the Orphan Seven-Transmembrane Receptor APJ, Inhibits Human Immunodeficiency Virus Type 1 Entry
M Cayabyab, S Hinuma, M Farzan, H Choe, S Fukusumi, C Kitada, N Nishizawa, M Hosoya, O Nishimura, T Messele, G Pollakis, J Goudsmit, M Fujino, J Sodroski
Journal of virology 2000
Wild-type but not Alzheimer-mutant amyloid precursor protein confers resistance against p53-mediated apoptosis
X Xu, D Yang, T Wyss-Coray, J Yan, L Gan, Y Sun, L Mucke
Proceedings of the National Academy of Sciences 1999
Lymphotropic virions affect chemokine receptor-mediated neural signaling and apoptosis: implications for human immunodeficiency virus type 1-associated dementia
J Zheng, A Ghorpade, D Niemann, RL Cotter, MR Thylin, L Epstein, JM Swartz, RB Shepard, X Liu, A Nukuna, HE Gendelman
Journal of virology 1999
Evidence that Par-4 participates in the pathogenesis of HIV encephalitis
II Kruman, A Nath, WF Maragos, SL Chan, M Jones, VM Rangnekar, RJ Jakel, MP Mattson
The American Journal of Pathology 1999
Apoptosis induced by infection of primary brain cultures with diverse human immunodeficiency virus type 1 isolates: evidence for a role of the envelope
A Ohagen, S Ghosh, J He, K Huang, Y Chen, M Yuan, R Osathanondh, S Gartner, B Shi, G Shaw, D Gabuzda
Journal of virology 1999
Evidence for a synergistic effect of the HIV-1 envelope protein gp120 and brain-derived neurotrophic factor (BDNF) leading to enhanced expression of somatostatin neurons in aggregate cultures derived from the human fetal cortex
A Barnea, J Roberts, RH Ho
Brain Research 1999
Unraveling the Mechanisms of Neurotoxicity in HIV Type 1-Associated Dementia: Inhibition of Neuronal Synaptic Transmission by Macrophage Secretory Products
H Xiong, J Zheng, M Thylin, HE Gendelman
AIDS Research and Human Retroviruses 1999
Neuroprotection by caspase inhibitors
JS Braun, EI Tuomanen, JL Cleveland
Expert Opinion on Investigational Drugs 1999
Nitric oxide synthase expression and apoptotic cell death in brains of AIDS and AIDS dementia patients
VA Vincent, CJ de Groot, PJ Lucassen, P Portegies, D Troost, FJ Tilders, AM Dam
AIDS 1999
Stable expression of HIV-1 Nef induces changes in growth properties and activation state of human astrocytes
B Kohleisen, E Shumay, G Sutter, R Foerster, R Brack-Werner, M Nuesse, V Erfle
AIDS 1999
Neuronal apoptosis does not correlate with dementia in HIV infection but is related to microglial activation and axonal damage
Adle-Biassette, Chretien, Wingertsmann, Hery, Ereau, Scaravilli, Tardieu, Gray
Neuropathology and Applied Neurobiology 1999
Tat, a human immunodeficiency virus-1 derived protein, augments excitotoxic hippocampal injury in neonatal rats
P Wang, JD Barks, FS Silverstein
Neuroscience 1999
Intracellular CXCR4 signaling, neuronal apoptosis and neuropathogenic mechanisms of HIV-1-associated dementia
J Zheng, MR Thylin, A Ghorpade, H Xiong, Y Persidsky, R Cotter, D Niemann, MH Che, YC Zeng, HA Gelbard, RB Shepard, JM Swartz, HE Gendelman
Journal of Neuroimmunology 1999
Coreceptor Ligand Inhibition of Fetal Brain Cell Infection by HIV Type 1
S Hibbitts, JD Reeves, G Simmons, PW Gray, LG Epstein, D Schols, ED Clercq, TN Wells, AE Proudfoot, PR Clapham
AIDS Research and Human Retroviruses 1999
Apoptosis Detection in Brain Using Low-Magnification Dark-Field Microscopy
MS Lange, MV Johnston, EE Tseng, WA Baumgartner, ME Blue
Experimental Neurology 1999
Temporal Profile of Apoptotic-like Changes in Neurons and Astrocytes Following Controlled Cortical Impact Injury in the Rat
JK Newcomb, X Zhao, BR Pike, RL Hayes
Experimental Neurology 1999
HIV-1 kills renal tubular epithelial cells in vitro by triggering an apoptotic pathway involving caspase activation and Fas upregulation
PG Conaldi, L Biancone, A Bottelli, A Wade-Evans, LC Racusen, M Boccellino, V Orlandi, C Serra, G Camussi, A Toniolo
Journal of Clinical Investigation 1998
HIV-1 Protein Tat Induces Apoptosis of Hippocampal Neurons by a Mechanism Involving Caspase Activation, Calcium Overload, and Oxidative Stress
II Kruman, A Nath, MP Mattson
Experimental Neurology 1998
Local production of TGF β1 inhibits cerebral edema, enhances TNF-α induced apoptosis and improves survival in a murine glioma model
DM Ashley, JH Sampson, GE Archer, LP Hale, DD Bigner
Journal of Neuroimmunology 1998
Acute, relapsing brain oedema with diffuse blood-brain barrier alteration and axonal damage in the acquired immunodeficiency syndrome
Gray, Belec, Chretien, Dubreuil-Lemaire, Ricolfi, Wingertsmann, Poron, Gherardi
Neuropathology and Applied Neurobiology 1998
DNA breaks detected by in situ end-labelling in dorsal root ganglia of patients with AIDS
Adle-Biassette, Bell, Creange, Sazdovitch, Authier, Gray, Hauw, Gherardi
Neuropathology and Applied Neurobiology 1998
Differential modulation of cell death proteins in human brain cells by tumor necrosis factor alpha and platelet activating factor
L Pulliam, M Zhou, M Stubblebine, C M Bitler
Journal of Neuroscience Research 1998
Neuroimmunodegeneration
PK Wong, WS Lynn
1998
Astrocyte apoptosis induced by HIV-1 transactivation of the c-kit protooncogene
J He, CM deCastro, GR Vandenbark, J Busciglio, D Gabuzda
Proceedings of the National Academy of Sciences 1997
Advances in Molecular and Cell Biology
KJ Clemetson
Advances in Molecular and Cell Biology 1997
CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia
J He, Y Chen, M Farzan, H Choe, A Ohagen, S Gartner, J Busciglio, X Yang, W Hofmann, W Newman, CR Mackay, J Sodroski, D Gabuzda
Nature 1997
HIV-Infekt
NH Brockmeyer, L Mertins
1997
Thrombotic Thrombocytopenic Purpura and Sporadic Hemolytic-Uremic Syndrome Plasmas Induce Apoptosis in Restricted Lineages of Human Microvascular Endothelial Cells
D Mitra, EA Jaffe, B Weksler, KA Hajjar, C Soderland, J Laurence
Blood 1997
Advances in Pharmacology
B Drenger, Y Ginosar, Y Gozal
Advances in Pharmacology 1994
International Review of Cytology
RA Miller
International Review of Cytology 1991

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