Cited by 168Neurotransmitter Receptor Influence on BehaviorParkinson's Disease Mechanisms and TreatmentsAntioxidant Activity and Oxidative Stress

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Acute or repeated cocaine administration generates reactive oxygen species and induces antioxidant enzyme activity in dopaminergic rat brain structures

Dietrich, Jean-Bernard, Mangeol, Aude, Revel, Marie-Odile, Burgun, Claude, Aunis, Dominique, Zwiller, Jean·2005·Neuropharmacology

DOI 10.1016/j.neuropharm.2005.01.018

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Abstract

Either a single (acute) or repeated daily (chronic) injections (1 injection/day) of 20 mg/kg cocaine for 10 days to rats was found to increase reactive oxygen species production in two dopaminergic brain structures, the frontal cortex and the striatum. We found that the mitochondrial genome was down-regulated after acute cocaine injection. Hydroperoxide and lipid peroxide generation was correlated with an increase in mitochondrial hydrogen peroxide generation and with a reduced functioning of mitochondrial complex I in response to cocaine. As judged from the measurement of caspase-3 activity and TUNEL labeling, neither acute nor chronic cocaine treatment has been found to induce apoptosis in any of the structures examined. This differs dramatically from what has been described for methamphetamine. Cocaine-induced radical formation was accompanied by the induction of the antioxidant enzymes superoxide dismutase and glutathione peroxidase, after both acute and chronic cocaine treatment. In addition, proteasome chymotrypsin-like activity was enhanced following a single cocaine injection in both cortex and striatum. It is proposed that the compensatory mechanisms to oxidative stress occurring in response to cocaine were effective in scavenging reactive oxygen species and in preventing subsequent cellular damage, thus explaining why no significant cell death was found in these brain structures.

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“Cocaine increases the production of ROS, which in turn leads to oxidative damage to brain cells [8].”
Background
Effect of Cocaine on Fas-Associated Protein with Death Domain in the Rat Brain: Individual Differences in a Model of Differential Vulnerability to Drug Abuse
García-Fuster, M. J., Clinton, S. M., Watson, S. J., & Akil, H. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.88 · Cited by 32
“Cunha-Oliveira et al , 2006 ), although the literature concerning cocaine neurotoxicity in adult brain remains inconclusive (”
Background
Lithium engages autophagy for neuroprotection and neuroplasticity: Translational evidence for therapy
Puglisi‐Allegra, S., Lazzeri, G., Busceti, C. L., Giorgi, F. S., Biagioni, F., & Fornai, F. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105148 · Cited by 33
The Alterations in Mitochondrial DNA Copy Number and Nuclear-Encoded Mitochondrial Genes in Rat Brain Structures after Cocaine Self-Administration
Sadakierska−Chudy, A., Kotarska, A., Frankowska, M., Jastrzębska, J., Wydra, K., Miszkiel, J., Przegaliński, E., & Filip, M. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0153-3 · Cited by 32
Roles of the ubiquitin proteasome system in the effects of drugs of abuse
Massaly, N., Francès, B., & Moulédous, L. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2014.00099 · Cited by 30
Superoxide production after acute and chronic treatment with methylphenidate in young and adult rats
Gomes, K. M., Inácio, C. G., Valvassori, S. S., Réus, G. Z., Boeck, C. R., Dal-Pizzol, F., & Quevedo, J. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.08.060 · Cited by 34
The Sigma-1 Receptor: When Adaptive Regulation of Cell Electrical Activity Contributes to Stimulant Addiction and Cancer
Soriani, O., & Kourrich, S. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01186 · Cited by 29
Targeting redox regulation to treat substance use disorder using N‐acetylcysteine
Womersley, J. S., Townsend, D. M., Kalivas, P. W., & Uys, J. D. K. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14130 · Cited by 28
Longitudinal patterns of illicit drug use, antiretroviral therapy exposure and plasma HIV-1 RNA viral load among HIV-positive people who use illicit drugs
Liang, J., Nosova, E., Reddon, H., Nolan, S., Socias, M. E., Barrios, R., & Milloy, M. (2020) · AIDS · doi:10.1097/qad.0000000000002551 · Cited by 27
“Other studies on synergistic neurotoxicity of cocaine and HIV-1 membrane proteins support a possible mechanism of crack cocaine mediated HIV disease progression with increased ROS and dysregulation of other cellular signalling pathways [26,28].”
Background
The role of mitochondria in cocaine addiction
Thornton, C., Grad, E., & Yaka, R. (2021) · Biochemical Journal · doi:10.1042/bcj20200615 · Cited by 30
Impairment of spatial working memory and oxidative stress induced by repeated crack cocaine inhalation in rats
Lipaus, I. F. S., Gomes, E. F., Martins, C. W., Martins-Silva, C., Pires, R. G. W., Malgarin, F., Schuck, P. F., Nakamura-Palacios, E. M., & Rodrigues, L. C. D. M. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.06.020 · Cited by 28
“The antioxidant enzyme SOD catalyses the dismutation of superoxide radicals into the less reactive hydrogen peroxide [52], suggesting that increased activity might be due to an increase in ROS production in this brain region, possibly caused by crack cocaine inhalation.”
Astrocytic mobilization of glutathione peroxidase-1 contributes to the protective potential against cocaine kindling behaviors in mice via activation of JAK2/STAT3 signaling
Nhu, H., Nguyen, L. T. T., Shin, E., Kim, D.-J., Jeong, J. H., Chung, Y. H., Lei, X. G., Sharma, N., Jang, C., Nabeshima, T., et al. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.12.027 · Cited by 27
Differences between dextroamphetamine and methamphetamine: behavioral changes and oxidative damage in brain of Wistar rats
da-Rosa, D. D., Valvassori, S. S., Steckert, A. V., Arent, C. O., Ferreira, C. L., Lopes-Borges, J., Varela, R. B., Mariot, E., Dal‐Pizzol, F., Andersen, M. L., et al. (2011) · Journal of Neural Transmission · doi:10.1007/s00702-011-0691-9 · Cited by 26
“Initially, the neurotoxicity of amphetamines was thought to result essentially from reactive oxygen species (ROS) that are formed by the oxidation of dopamine ( Dietrich et al. 2005 ).”
Background
Tempol attenuates cocaine-induced death of PC12 cells through decreased oxidative damage
Numa, R., Baron, M., Kohen, R., & Yaka, R. (2010) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2010.10.024 · Cited by 26
Partial connectomes of labeled dopaminergic circuits reveal non-synaptic communication and axonal remodeling after exposure to cocaine
Wildenberg, G. A., Sorokina, A., Koranda, J. L., Monical, A., Heer, C. M., Sheffield, M. E. J., Zhuang, X., McGehee, D. S., & Kasthuri, B. (2021) · University of Chicago · doi:10.6082/232sj-vk702 · Cited by 27
Effects of Cocaine on Nitric Oxide Production in Bovine Coronary Artery Endothelial Cells
He, J., Yang, S., & Zhang, L. (2005) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.087452 · Cited by 24
“In addition, cocaine can increase reactive oxygen species (Moritz et al., 2003; Dietrich et al., 2005) that may contribute to uncoupling of eNOS and a decrease in bioavailable nitric oxide.”
Background
Cocaine evokes a profile of oxidative stress and impacts innate antiviral response pathways in astrocytes
Cisneros, I. E., Erdenizmenli, M., Cunningham, K. A., Paessler, S., & Dineley, K. T. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.03.019 · Cited by 23
“kB signaling within the NAc, frontal cortex and hippocampus (Dietrich et al., 2005; Jang et al., 2015; Muriach et al., 2010).”
Background
Protective Role of Lactobacillus rhamnosus Probiotic in Reversing Cocaine-Induced Oxidative Stress, Glial Activation and Locomotion in Mice
Chivero, E. T., Sil, S., Singh, S., Thangaraj, A., Gordon, L., Evah-Nzoughe, G., Ferguson, N., Callen, S. E., & Buch, S. J. (2021) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-021-10020-9 · Cited by 24
Role of Mitochondrial Dynamics in Cocaine’s Neurotoxicity
Wen, S., Aki, T., Funakoshi, T., Unuma, K., & Uemura, K. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23105418 · Cited by 25
“Cocaine-triggered apoptotic neuronal death has also been demonstrated in in vivo models in mouse, rat, and human [32,55,56].”
Background
A ketogenic diet diminishes behavioral responses to cocaine in young adult male and female rats
Martinez, L. A., Lees, M. E., Ruskin, D. N., & Masino, S. A. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.02.001 · Cited by 22
Early abstinence of crack-cocaine is effective to attenuate oxidative stress and to improve antioxidant defences
Zaparte, A., Viola, T. W., Grassi‐Oliveira, R., Morrone, M. D. S., Moreira, J. C. F., & Bauer, M. E. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3779-8 · Cited by 21
S-Glutathionylation and Redox Protein Signaling in Drug Addiction
Womersley, J. S., & Uys, J. D. K. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.10.001 · Cited by 21
Combined Effects of Simultaneous Exposure to Caffeine and Cocaine in the Mouse Striatum
Muñiz, J. A., Gómez, G., González, B., Rivero‐Echeto, M. C., Cadet, J. L., García‐Rill, E., Urbano, F. J., & Bisagno, V. (2016) · Neurotoxicity Research · doi:10.1007/s12640-016-9601-0 · Cited by 24
“It should be noted that chronic cocaine was found to increase reactive oxygen species production in the striatum (Dietrich et al. 2005).”
Cocaine-induced status epilepticus and death generate oxidative stress in prefrontal cortex and striatum of mice
Macêdo, D. S., Vasconcelos, S. M. M., Andrade‐Neto, M., Belchior, L. D., Júnior, J. E. R. H., Gonçalves, D. O., Fonteles, M. M. D. F., Silva, M. I. G., Aguiar, L. M. V., Viana, G. S. D. B., et al. (2009) · Neurochemistry International · doi:10.1016/j.neuint.2009.10.001 · Cited by 21
Phosphoproteomic analysis of the striatum from pleiotrophin knockout and midkine knockout mice treated with cocaine reveals regulation of oxidative stress-related proteins potentially underlying cocaine-induced neurotoxicity and neurodegeneration
Vicente‐Rodríguez, M., Gramage, E., Herradón, G., & Pérez‐García, C. (2013) · Toxicology · doi:10.1016/j.tox.2013.09.014 · Cited by 20
“In addition, it is interesting to note that a single dose of cocaine within the same dose range has been shown to downregulate mitochondrial genome and to increase the mitochondrial hydrogen peroxide generation together with a reduced functioning of the mitochondrial complex I in the striatum in response to cocaine (D…”
BackgroundResultInfluential
Cortical Consequences of HIV-1 Tat Exposure in Rats are Enhanced by Chronic Cocaine
Wayman, W. N., Chen, L., Persons, A. L., & Napier, T. C. (2015) · Current HIV Research · doi:10.2174/0929867322666150311164504 · Cited by 20
“The absence of neuronal death may reflect ROS buffering as cocaine causes a concomitant increase in the production of antioxidant enzymes which prevents the activation of cellular apoptotic signaling cascades [83].”
Background
Selective Nitric Oxide Synthase Inhibitor 7-Nitroindazole Protects against Cocaine-Induced Oxidative Stress in Rat Brain
Vitcheva, V., Simeonova, R., Kondeva-Burdina, M., & Mitcheva, M. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/157876 · Cited by 19
Cocainomics: New Insights into the Molecular Basis of Cocaine Addiction
Hemby, S. E. (2010) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-009-9189-8 · Cited by 19
“enzyme activity, and elevates reactive oxygen species in dopaminergic projection areas (Dietrich et al. 2005; Macedo et al. 2005).”
Background
Change of cystine/glutamate antiporter expression in ethanol-dependent rats
Peana, A. T., Muggironi, G., & Bennardini, F. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00311 · Cited by 18
“Nonetheless, studies in experimental animal models have shown that ethanol (Bailey et al., 1999; Dahchour et al., 2005), cocaine (Dietrich et al., 2005), heroin (Pan et al., 2005), and nicotine (Jain and Jaimes, 2013) increase reactive oxygen species.”
Background
Crossroads of Drug Abuse and HIV Infection: Neurotoxicity and CNS Reservoir
Sonti, S., Tyagi, K., Pande, A., Daniel, R., Sharma, A. L., & Tyagi, M. (2022) · Vaccines · doi:10.3390/vaccines10020202 · Cited by 17
Angiotensin II modulates amphetamine‐induced glial and brain vascular responses, and attention deficit via angiotensin type 1 receptor: Evidence from brain regional sensitivity to amphetamine
Marchese, N. A., Occhieppo, V. B., Basmadjian, O. M., Casarsa, B. S., Baiardi, G., & Bregonzio, C. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14605 · Cited by 18
“The analyses of HPC (Figure 4) indicated that there were no significant differences in the percentage of GFAP nor CD11bpositive area (treatment*drug interaction F(1,23) = 0.00005 p = .99 and F(1,25) = 0.00004 p = .99, respectively).”
BackgroundInfluential
Cocaine induces the expression of homer 1b/c, homer 3a/b, and hsp 27 proteins in rat cerebellum
Dietrich, J., Arpin‐Bott, M., Kao, D., Dirrig‐Grosch, S., Aunis, D., & Zwiller, J. (2007) · Synapse · doi:10.1002/syn.20412 · Cited by 16
“We recently reported that acute or repeated cocaine administration to rats generated reactive oxygen species (ROS) in dopaminergic brain structures (Dietrich et al., 2005).”
BackgroundSelf-citation
Environmental enrichment reduces cocaine neurotoxicity during cocaine-conditioned place preference in male rats
Freese, L., Almeida, F. B., Heidrich, N., Hansen, A. W., Reinhardt, L. S., Steinmetz, A., Moura, D. J., Gomez, R., & Barros, H. M. T. (2018) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2018.04.001 · Cited by 16
“break in the chain of events that ensure genomic stability in dopaminergic brain structures and can induce a potent genotoxic effect, as demonstrated by ROS increase and DNA damage (Pereira et al., 2015; Dietrich et al., 2005; Alvarenga et al., 2010).”
BackgroundInfluential
Efavirenz exposure, alone and in combination with known drugs of abuse, engenders addictive-like bio-behavioural changes in rats
Möller, M., Fourie, J., & Harvey, B. H. (2018) · Scientific Reports · doi:10.1038/s41598-018-29978-3 · Cited by 15
Role of Multifunctional FADD (Fas-Associated Death Domain) Adaptor in Drug Addiction
Ramos‐Miguel, A., Álvaro-Bartolomé, M., Julià, M., & Jesus, A. (2012) · InTech eBooks · doi:10.5772/34273 · Cited by 15
“However, the aberrant activation of several cell death mechanisms by cocaine, including those mediated by the Fas/FADD complex, in the adult rat brain remains inconclusive (Dietrich et al, 2005; García-Fuster et al., 2009).”
Background
Cocaine potentiates MDMA-induced oxidative stress but not dopaminergic neurotoxicity in mice: implications for the pathogenesis of free radical-induced neurodegenerative disorders
Peraile, I., Granado, N., Torres, E., Gutiérrez‐López, M. D., Moratalla, R., Colado, M. I., & O’Shea, E. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3142-5 · Cited by 15
Identification of biochemical and cytotoxic markers in cocaine treated PC12 cells
Badisa, R. B., Batton, C. S., MAZZIO, E. A., Grant, S. C., & Goodman, C. B. (2018) · Scientific Reports · doi:10.1038/s41598-018-21182-7 · Cited by 15
Anhydroecgonine Methyl Ester (AEME), a Product of Cocaine Pyrolysis, Impairs Spatial Working Memory and Induces Striatal Oxidative Stress in Rats
Gomes, E. F., Lipaus, I. F. S., Martins, C. W., Araújo, A. M., Mendonça, J. B., Pelição, F. S., Lebarch, E. C., Rodrigues, L. C. D. M., & Nakamura-Palacios, E. M. (2017) · Neurotoxicity Research · doi:10.1007/s12640-017-9813-y · Cited by 15
“To this end, the integrity of PFC integration with the hippocampus (HPC) and striatum (STR) is essential (Doeller et al. 2005; Floresco et al. 1997; Poch and Campo 2012; Seamans et al. 1998).”
Background
P53 knockout mice are protected from cocaine-induced kindling behaviors via inhibiting mitochondrial oxidative burdens, mitochondrial dysfunction, and proapoptotic changes
Nhu, H., Sharma, N., Jeong, J. H., Shin, E., Pham, D. T., Trinh, Q. D., Lee, Y. J., Jang, C., Nah, S.-Y., Bing, G., et al. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2018.12.017 · Cited by 15
“, superoxide dismutase, glutathione peroxidase, and catalase) (Dietrich et al., 2005; Macedo et al., 2010; Pomierny-Chamiolo et al., 2013).”
Influential
The Role of Oxidative Stress in Cocaine Addiction
Beiser, T., & Yaka, R. (2019) · Journal of Neurology and Neuromedicine · doi:10.29245/2572.942x/2019/1.1239 · Cited by 15
The cellular basis of fetal endoplasmic reticulum stress and oxidative stress in drug-induced neurodevelopmental deficits
Tsai, S.-Y. A., Bendriem, R. M., & Lee, C.-T. D. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100145 · Cited by 15
“…pathways as revealed by studies in which both acute and chronic cocaine and/or METH exposure generated reactive oxygen species and altered CNS activities in various brain subregions (Bashkatova et al., 2005; Dietrich et al., 2005; Macedo et al., 2005; Pubill et al., 2005; Yamamoto and Zhu, 1998).”
Background

Authors: Dietrich, J.-B., Mangeol, A., Revel, M.-O., Burgun, C., Aunis, D., & Zwiller, J.
Affiliations: Inserm (FR)
Corresponding author: Dietrich, Jean-Bernard
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2005-06
Volume: 48
Issue: 7
Pages: 965-974
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2005.01.018
OpenAlex: W2061764945
Cited by: 168
References: 34
Citations by year: 2026: 8 · 2025: 5 · 2024: 4 · 2023: 5 · 2022: 7 · 2021: 13 · 2020: 5 · 2019: 11 · 2018: 13 · 2017: 7 · 2016: 9 · 2015: 9 · 2014: 16 · 2013: 11 · 2012: 8
FWCI: 2.16
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
Health Sciences › Medicine › Biochemistry (medical) › Antioxidant Activity and Oxidative Stress
Keywords: cocaine, reactive oxygen species, oxidative stress, antioxidant enzymes, superoxide dismutase, glutathione peroxidase, dopaminergic neurons, frontal cortex, striatum, mitochondrial hydrogen peroxide, mitochondrial complex I, lipid peroxidation, caspase-3, apoptosis, methamphetamine
MeSH terms: Animals, Antioxidants, Brain, Cocaine, Dopamine, Enzyme Induction, Glutathione Peroxidase, Male, Superoxide Dismutase, Rats, Wistar, Reactive Oxygen Species, Rats

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Acute or repeated cocaine administration generates reactive oxygen species and induces antioxidant enzyme activity in dopaminergic rat brain structures

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