Cited by 347Neuroinflammation and Neurodegeneration MechanismsParkinson's Disease Mechanisms and TreatmentsNuclear Receptors and Signaling

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Naloxone Protects Rat Dopaminergic Neurons against Inflammatory Damage through Inhibition of Microglia Activation and Superoxide Generation

Liu, Bin, Du, Lina, Hong, Jau-Shyong·2000·The Journal of Pharmacology and Experimental Therapeutics

DOI 10.1016/s0022-3565(24)39275-4

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Abstract

Degeneration of dopaminergicrgic neurons in the substantia nigra of the brain is a hallmark of Parkinson's disease and inflammation and oxidative stress are closely associated with the pathogenesis of degenerative neurological disorders. Treatment of rat mesencephalic mixed neuron-glia cultures with lipopolysaccharide (LPS)-activated microglia, resident immune cells of the brain, to release proinflammatory and neurotoxic factors tumor necrosis factor-alpha, interleukin-1beta, nitric oxide, and superoxide and subsequently caused damage to midbrain neurons, including dopaminergic neurons. The LPS-induced degeneration of the midbrain neurons was significantly reduced by cotreatment with naloxone, an opioid receptor antagonist. This study focused on understanding the mechanism of action for the protective effect of naloxone on dopaminergic neurons because of relevance to Parkinson's disease. Both naloxone and its opioid receptor inactive stereoisomer (+)-naloxone protected the dopaminergic neurons with equal potency. Naloxone inhibited LPS-induced activation of microglia and release of proinflammatory factors, and inhibition of microglia generation of superoxide free radical best correlated with the neuroprotective effect of naloxone isomers. To further delineate the site of action, naloxone was found to partially inhibit the binding of [(3)H]LPS to cell membranes, whereas it failed to prevent damage to dopaminergic neurons by peroxynitrite, a product of nitric oxide and superoxide. These results suggest that naloxone at least in part interferes with the binding of LPS to cell membranes to inhibit microglia activation and protect dopaminergic neurons as well as other neurons in the midbrain cultures from inflammatory damage.

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BackgroundMethod
Naloxone Inhibition of Lipopolysaccharide-Induced Activation of Retinal Microglia is Partly Mediated via the p38 Mitogen Activated Protein Kinase Signalling Pathway
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Gö6976 Protects Mesencephalic Neurons from Lipopolysaccharide‐Elicited Death by Inhibiting p38 MAP Kinase Phosphorylation
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Fyn Kinase-Mediated PKCδ Y311 Phosphorylation Induces Dopaminergic Degeneration in Cell Culture and Animal Models: Implications for the Identification of a New Pharmacological Target for Parkinson’s Disease
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“Seven days after seeding, the neuron–glia cultures made up of about 10% microglia, 50% astrocytes, and 40% neurons based on the visual counting of immunostained cells with antibodies against cell-type specific markers: neurons (Neu-N), microglia (OX-42), and astrocytes (GFAP) [28].”
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“However, recent studies have shown that the inflammatory reaction induced by lipopolysaccharide (LPS) has a degenerative effect on dopaminergic neurons in vitro (9,10) and in vivo (11,12).”
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The Degenerating Substantia Nigra as a Susceptible Region for Gene Transfer-Mediated Inflammation
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“lipopolysaccharide (LPS) to the membrane and consequently prevents microglial activation, hence protecting dopaminergic neurons (Liu et al., 2000).”
Background
Determining the neuroprotective effects of dextromethorphan in lipopolysaccharide-stimulated BV2 microglia
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“Previous studies have demonstrated that naloxone, another analogue of morphinan, protects against lipopolysaccharide (LPS)-induced neurotoxicity in vitro and in vivo through the inhibition of the release of proinflammatory factors and free radicals (15-18).”
Evidence for dopamine-derived hydroxyl radical formation in the nigrostriatal system in response to axotomy
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Tolerized Microglia Protect Neurons Against Endotoxin-Induced TNF-α Production via an LBP-Dependent Intracellular p38 MAPK Signaling Pathway
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In Vitro Models for Neuroelectrodes: A Paradigm for Studying Tissue–Materials Interactions in the Brain
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Self-citation
Down-regulation of microglial activity attenuates axotomized nigral dopaminergic neuronal cell loss
Song, D., Yu, H.-N., Park, C.-R., Lee, J.-S., Lee, J., Park, B.-G., Woo, R., Han, J.-T., Cho, B., & Baik, T. (2013) · BMC Neuroscience · doi:10.1186/1471-2202-14-112 · Cited by 8
“These events were attenuated by pretreatment with anti-inflammatory agents, such as naloxone [21] and minocycline [22].”
(E)-2-methoxy-4-(3-(4-methoxyphenyl) prop-1-en-1-yl) Phenol Ameliorates MPTP-Induced Dopaminergic Neurodegeneration by Inhibiting the STAT3 Pathway
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“For instance, naloxone [32] inhibits microglial activation and reduces superoxide production in the lipopolysaccharide-induced PD model, and vasoactive intestinal peptide [33] blocks microglial activation by decreasing THF-α, IL-1β, and iNOS expression in the MPTP-induced PD model.”
BackgroundSelf-citation
Effect of Pramipexole on Inflammatory Response in Central Nervous System of Parkinson's Disease Rat Model
Jiang, S., Gao, H., Yong, Y., Zhang, H., Li, P., Li, Y., Luo, Q., & Yang, X. (2021) · Archives of Medical Research · doi:10.1016/j.arcmed.2021.06.007 · Cited by 8
A randomized, double-blind, placebo-controlled, hybrid parallel-arm study of low-dose naltrexone as an adjunctive anti-inflammatory treatment for major depressive disorder
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Background
Effect of μ and κ opioids on injury-induced microglial accumulation in leech CNS: Involvement of the nitric oxide pathway
Yahyavi‐Firouz‐Abadi, N., Tahsili‐Fahadan, P., & Ostad, S. N. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.10.036 · Cited by 8
Serum‐Dependence of LPS‐Induced Neurotoxicity in Rat Cortical Neurons
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Characterization of a SILAC method for proteomic analysis of primary rat microglia
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Self-citation
Ischemia‐responsive protein 94 is a key mediator of ischemic neuronal injury‐induced microglial activation
Tikamdas, R., Singhal, S. M., Zhang, P., Smith, J. A., Krause, E. G., Stevens, S. M., Song, S., & Liu, B. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14111 · Cited by 7
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Neuroprotective effect of benzylideneacetophenone derivative on the MPTP model of neurodegeneration in mice
Kang, J. M., Jung, J., Kim, H., Lim, H., Jang, S., & Oh, S. (2008) · Archives of Pharmacal Research · doi:10.1007/s12272-001-1275-5 · Cited by 7
“However, inhibition of microglial production of superoxide, but not the other factors, was most effective in protecting neurons, indicating that superoxide was a dominant degenerative factor for the dopaminergic neurons in the culture (Liu et al., 2000).”
Background
β-Funaltrexamine inhibits chemokine (CXCL10) expression in normal human astrocytes
Davis, R. L., Das, S., Buck, D. J., & Stevens, C. W. (2013) · Neurochemistry International · doi:10.1016/j.neuint.2013.01.013 · Cited by 7
“Furthermore, it was determined that the inactive stereoisomer, (+)-naloxone, was equally effective as (−)-naloxone (Liu et al., 2000).”
BackgroundMethodResultInfluential
Obesity-mediated Lipoinflammation Modulates Food Reward Responses
Huerta, C., Caba, M., & Camacho‐Morales, A. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.08.019 · Cited by 8
Etiology and Progression of Parkinson's Disease: Cross-Talk Between Environmental Factors and Genetic Vulnerability
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Genetic contributions to influenza virus attenuation in the rat brain
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“These cultures consist of approximately 50% atrocytes, 40% neurons, and 10% microglia and other cell types, as demonstrated previously (Kim et al, 2000; Liu et al, 2000).”
Background
Baseline‐ and treatment‐associated pain in the X:BOT comparative effectiveness study of extended‐release naltrexone versus buprenorphine‐naloxone for OUD
Wang, A., Shulman, M., Choo, T.-H. J., Pavlicová, M., Langleben, D. D., Nunes, E. V., & Rotrosen, J. (2021) · Addiction Biology · doi:10.1111/adb.13112 · Cited by 5
“Another explanation could be that XR-NTX reduced pain through its anti-inflammatory effects.(37) This is supported by previous studies showing naltrexone's antagonist effect on central nervous system immune cells (e.”
Result
Chronic Treatment with Naltrexone Prevents Memory Retention Deficits in Rats Poisoned with the Sarin Analog Diisopropylfluorophosphate (DFP) and Treated with Atropine and Pralidoxime
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“agent with anti-inflammatory properties [18, 19], was found to prevent deficits in spatial learning in rats given lethal doses of DFP [6].”
Background
Oxycodone-Naloxone Combination Hinders Opioid Consumption in Osteoarthritic Chronic Low Back Pain: A Retrospective Study with Two Years of Follow-Up
Polati, E., Nizzero, M., Rama, J., Martini, A., Gottin, L., Donadello, K., Balzo, G. D., Varrassi, G., Marinangeli, F., Vittori, A., et al. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph192013354 · Cited by 5
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Background
Protective Effects of Two Constituents of Chinese Herbs on Spinal Motor Neurons from Embryonic Rats with Hypoxia Injury
Chen, J.-F., Fan, J., Tian, X.-W., & Tang, T.-S. (2012) · African Journal of Traditional Complementary and Alternative Medicines · doi:10.4314/ajtcam.v9i2.8 · Cited by 5
Roles of Microglia in Inflammation-Mediated Neurodegeneration: Models, Mechanisms, and Therapeutic Interventions for Parkinson's Disease
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Self-citation
Pilot study of tolerability and safety of opioid receptor antagonists as novel therapies for chronic pain among persons living with HIV with past year heavy drinking: a randomized controlled trial
Bendiks, S., Cheng, D. M., Blokhina, E. A., Vetrova, M., Verbitskaya, E. V., Gnatienko, N., BRYANT, K. J., Krupitsky, E. M., Samet, J. H., & Tsui, J. I. (2021) · AIDS Care · doi:10.1080/09540121.2021.1896663 · Cited by 4
“…including increased production of endogenous opioids or upregulation of opioid receptors (Brown & Panksepp, 2009), as well as research suggesting inhibition of microglia (Chang et al., 2000; Hutchinson et al., 2008; Liu et al., 2000) and suppression of inflammatory cytokines (Liu et al., 2006).”
Background

Authors: Liu, B., Du, L., & Hong, J.-S.
Affiliations: National Institutes of Health (US)
National Institute of Environmental Health Sciences (US)
Corresponding author: Liu, Bin
ORCID: Liu, Bin
Du, Lina
Hong, Jau-Shyong
Venue: The Journal of Pharmacology and Experimental Therapeutics
Publisher: Elsevier BV
Published: 2000-04
Volume: 293
Issue: 2
Pages: 607-617
ISSN: 0022-3565 (ISSN-L)
DOI: 10.1016/s0022-3565(24)39275-4
OpenAlex: W1891696008
Cited by: 347
References: 43
Citations by year: 2026: 4 · 2025: 6 · 2024: 4 · 2023: 11 · 2022: 11 · 2021: 10 · 2020: 5 · 2019: 2 · 2018: 7 · 2017: 12 · 2016: 10 · 2015: 16 · 2014: 11 · 2013: 13 · 2012: 26
FWCI: 8.42
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Journal of Pharmacology and Experimental Therapeutics (publishedVersion)
PubMed (publishedVersion)
PubMed
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Receptors and Signaling
Keywords: naloxone, dopaminergic neurons, Parkinson's disease, microglial activation, lipopolysaccharide, neuroinflammation, oxidative stress, superoxide, neuroprotection, substantia nigra, opioid antagonists, peroxynitrite, nitric oxide, inflammatory cytokines
MeSH terms: Animals, Cells, Cultured, Dopamine, Immunohistochemistry, Inflammation, Interleukin-1, Lipopolysaccharides, Mesencephalon, Naloxone, Narcotic Antagonists, Neurons, Nitrates, Nitrites, Rats, Inbred F344, Stereoisomerism, Substantia Nigra, Superoxides, Tumor Necrosis Factor-alpha, Tyrosine 3-Monooxygenase, Oxidants, Microglia, Mitogen-Activated Protein Kinases, Mitogen-Activated Protein Kinase 3, Rats

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Naloxone Protects Rat Dopaminergic Neurons against Inflammatory Damage through Inhibition of Microglia Activation and Superoxide Generation

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