Cargando…

Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system

HIV-associated neurocognitive disorder (HAND), characterized by a wide spectrum of behavioral, cognitive, and motor dysfunctions, continues to affect approximately 50 % of HIV(+) patients despite the success of combination antiretroviral drug therapy (cART) in the periphery. Of note, potential toxic...

Descripción completa

Detalles Bibliográficos
Autores principales: Akay, Cagla, Cooper, Michael, Odeleye, Akinleye, Jensen, Brigid K., White, Michael G., Vassoler, Fair, Gannon, Patrick J., Mankowski, Joseph, Dorsey, Jamie L., Buch, Alison M., Cross, Stephanie A., Cook, Denise R., Peña, Michelle-Marie, Andersen, Emily S., Christofidou-Solomidou, Melpo, Lindl, Kathryn A., Zink, M. Christine, Clements, Janice, Pierce, R. Christopher, Kolson, Dennis L., Jordan-Sciutto, Kelly L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3928514/
https://www.ncbi.nlm.nih.gov/pubmed/24420448
http://dx.doi.org/10.1007/s13365-013-0227-1
_version_ 1782304276997996544
author Akay, Cagla
Cooper, Michael
Odeleye, Akinleye
Jensen, Brigid K.
White, Michael G.
Vassoler, Fair
Gannon, Patrick J.
Mankowski, Joseph
Dorsey, Jamie L.
Buch, Alison M.
Cross, Stephanie A.
Cook, Denise R.
Peña, Michelle-Marie
Andersen, Emily S.
Christofidou-Solomidou, Melpo
Lindl, Kathryn A.
Zink, M. Christine
Clements, Janice
Pierce, R. Christopher
Kolson, Dennis L.
Jordan-Sciutto, Kelly L.
author_facet Akay, Cagla
Cooper, Michael
Odeleye, Akinleye
Jensen, Brigid K.
White, Michael G.
Vassoler, Fair
Gannon, Patrick J.
Mankowski, Joseph
Dorsey, Jamie L.
Buch, Alison M.
Cross, Stephanie A.
Cook, Denise R.
Peña, Michelle-Marie
Andersen, Emily S.
Christofidou-Solomidou, Melpo
Lindl, Kathryn A.
Zink, M. Christine
Clements, Janice
Pierce, R. Christopher
Kolson, Dennis L.
Jordan-Sciutto, Kelly L.
author_sort Akay, Cagla
collection PubMed
description HIV-associated neurocognitive disorder (HAND), characterized by a wide spectrum of behavioral, cognitive, and motor dysfunctions, continues to affect approximately 50 % of HIV(+) patients despite the success of combination antiretroviral drug therapy (cART) in the periphery. Of note, potential toxicity of antiretroviral drugs in the central nervous system (CNS) remains remarkably underexplored and may contribute to the persistence of HAND in the cART era. Previous studies have shown antiretrovirals (ARVs) to be neurotoxic in the peripheral nervous system in vivo and in peripheral neurons in vitro. Alterations in lipid and protein metabolism, mitochondrial damage, and oxidative stress all play a role in peripheral ARV neurotoxicity. We hypothesized that ARVs also induce cellular stresses in the CNS, ultimately leading to neuronal damage and contributing to the changing clinical and pathological picture seen in HIV-positive patients in the cART era. In this report, we show that ARVs are neurotoxic in the CNS in both pigtail macaques and rats in vivo. Furthermore, in vitro, ARVs lead to accumulation of reactive oxygen species (ROS), and ultimately induction of neuronal damage and death. Whereas ARVs alone caused some activation of the endogenous antioxidant response in vitro, augmentation of this response by a fumaric acid ester, monomethyl fumarate (MMF), blocked ARV-induced ROS generation, and neuronal damage/death. These findings implicate oxidative stress as a contributor to the underlying mechanisms of ARV-induced neurotoxicity and will provide an access point for adjunctive therapies to complement ARV therapy and reduce neurotoxicity in this patient population.
format Online
Article
Text
id pubmed-3928514
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher Springer US
record_format MEDLINE/PubMed
spelling pubmed-39285142014-02-25 Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system Akay, Cagla Cooper, Michael Odeleye, Akinleye Jensen, Brigid K. White, Michael G. Vassoler, Fair Gannon, Patrick J. Mankowski, Joseph Dorsey, Jamie L. Buch, Alison M. Cross, Stephanie A. Cook, Denise R. Peña, Michelle-Marie Andersen, Emily S. Christofidou-Solomidou, Melpo Lindl, Kathryn A. Zink, M. Christine Clements, Janice Pierce, R. Christopher Kolson, Dennis L. Jordan-Sciutto, Kelly L. J Neurovirol Article HIV-associated neurocognitive disorder (HAND), characterized by a wide spectrum of behavioral, cognitive, and motor dysfunctions, continues to affect approximately 50 % of HIV(+) patients despite the success of combination antiretroviral drug therapy (cART) in the periphery. Of note, potential toxicity of antiretroviral drugs in the central nervous system (CNS) remains remarkably underexplored and may contribute to the persistence of HAND in the cART era. Previous studies have shown antiretrovirals (ARVs) to be neurotoxic in the peripheral nervous system in vivo and in peripheral neurons in vitro. Alterations in lipid and protein metabolism, mitochondrial damage, and oxidative stress all play a role in peripheral ARV neurotoxicity. We hypothesized that ARVs also induce cellular stresses in the CNS, ultimately leading to neuronal damage and contributing to the changing clinical and pathological picture seen in HIV-positive patients in the cART era. In this report, we show that ARVs are neurotoxic in the CNS in both pigtail macaques and rats in vivo. Furthermore, in vitro, ARVs lead to accumulation of reactive oxygen species (ROS), and ultimately induction of neuronal damage and death. Whereas ARVs alone caused some activation of the endogenous antioxidant response in vitro, augmentation of this response by a fumaric acid ester, monomethyl fumarate (MMF), blocked ARV-induced ROS generation, and neuronal damage/death. These findings implicate oxidative stress as a contributor to the underlying mechanisms of ARV-induced neurotoxicity and will provide an access point for adjunctive therapies to complement ARV therapy and reduce neurotoxicity in this patient population. Springer US 2014-01-14 2014 /pmc/articles/PMC3928514/ /pubmed/24420448 http://dx.doi.org/10.1007/s13365-013-0227-1 Text en © The Author(s) 2014 https://creativecommons.org/licenses/by/2.0/ Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
spellingShingle Article
Akay, Cagla
Cooper, Michael
Odeleye, Akinleye
Jensen, Brigid K.
White, Michael G.
Vassoler, Fair
Gannon, Patrick J.
Mankowski, Joseph
Dorsey, Jamie L.
Buch, Alison M.
Cross, Stephanie A.
Cook, Denise R.
Peña, Michelle-Marie
Andersen, Emily S.
Christofidou-Solomidou, Melpo
Lindl, Kathryn A.
Zink, M. Christine
Clements, Janice
Pierce, R. Christopher
Kolson, Dennis L.
Jordan-Sciutto, Kelly L.
Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system
title Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system
title_full Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system
title_fullStr Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system
title_full_unstemmed Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system
title_short Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system
title_sort antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3928514/
https://www.ncbi.nlm.nih.gov/pubmed/24420448
http://dx.doi.org/10.1007/s13365-013-0227-1
work_keys_str_mv AT akaycagla antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT coopermichael antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT odeleyeakinleye antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT jensenbrigidk antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT whitemichaelg antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT vassolerfair antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT gannonpatrickj antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT mankowskijoseph antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT dorseyjamiel antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT buchalisonm antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT crossstephaniea antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT cookdeniser antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT penamichellemarie antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT andersenemilys antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT christofidousolomidoumelpo antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT lindlkathryna antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT zinkmchristine antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT clementsjanice antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT piercerchristopher antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT kolsondennisl antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem
AT jordansciuttokellyl antiretroviraldrugsinduceoxidativestressandneuronaldamageinthecentralnervoussystem