Molecular changes evoked by the beta-lactam antibiotic ceftriaxone across rodent models of substance use disorder and neurological disease

Smaga, Irena; Fierro, Daniel; Mesa, Javier; Filip, Malgorzata; Knackstedt, Lori A

doi:10.1016/j.neubiorev.2020.05.016

Cited by 69Neuroscience and Neuropharmacology ResearchAmino Acid Enzymes and MetabolismAlzheimer's disease research and treatments

Molecular changes evoked by the beta-lactam antibiotic ceftriaxone across rodent models of substance use disorder and neurological disease

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Smaga, Irena, Fierro, Daniel, Mesa, Javier, Filip, Malgorzata, Knackstedt, Lori A·2020·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2020.05.016PMC PMC7483567

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Abstract

Ceftriaxone is a beta-lactam antibiotic that increases the expression of the major glutamate transporter, GLT-1. As such, ceftriaxone ameliorates symptoms across multiple rodent models of neurological diseases and substance use disorders. However, the mechanism behind GLT-1 upregulation is unknown. The present review synthesizes this literature in order to identify commonalities in molecular changes. We find that ceftriaxone (200 mg/kg for at least two days) consistently restores GLT-1 expression in multiple rodent models of neurological disease, especially when GLT-1 is decreased in the disease model. The same dose given to healthy/drug-naive rodents does not reliably upregulate GLT-1 in any brain region except the hippocampus. Increased GLT-1 expression does not consistently arise from transcriptional regulation, and is likely to be due to trafficking changes. In addition to altered transporter expression, ceftriaxone ameliorates neuropathologies (e.g. tau, amyloid beta, cell death) and aberrant protein expression associated with a number of neurological disease models. Taken together, these results indicate that ceftriaxone remains a strong candidate for treatment of multiple disorders in the clinic.

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Antibiotics have recently found new uses in the treatment of neurodegenerative diseases.
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CTX binds to α-synuclein with considerable affinity in vitro.
“Moreover, it has been observed that CTX binds to α-synuclein with considerable affinity and prevents its polymerization in vitro [226,230,231].”
From The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment (2022) · cites this paper as [231]

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A novel rat model of comorbid PTSD and addiction reveals intersections between stress susceptibility and enhanced cocaine seeking with a role for mGlu5 receptors
Schwendt, M., Shallcross, J., Hadad, N. A., Namba, M. D., Hiller, H., Wu, L., Krause, E. G., & Knackstedt, L. A. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0265-9 · Cited by 57 · see citing works
Self-citation
Beta Lactams Antibiotic Ceftriaxone Modulates Seizures, Oxidative Stress and Connexin 43 Expression in Hippocampus of Pentylenetetrazole Kindled Rats
Hussein, A. M., Ghalwash, M., Magdy, K., & Abulseoud, O. A. (2016) · Journal of Epilepsy Research · doi:10.14581/jer.16002 · Cited by 51 · see citing works
Ceftriaxone attenuates cocaine relapse after abstinence through modulation of nucleus accumbens AMPA subunit expression
LaCrosse, A., Hill, K., & Knackstedt, L. A. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.12.022 · Cited by 50 · see citing works
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Alcohol consumption increases basal extracellular glutamate in the nucleus accumbens core of S prague– D awley rats without increasing spontaneous glutamate release
Pati, D., Kelly, K. B., Stennett, B., Frazier, C. J., & Knackstedt, L. A. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13284 · Cited by 50 · see citing works
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Beneficial Effects of Ceftriaxone Against Pentylenetetrazole-Evoked Convulsions
Jelenković, A., Jovanović, M., Stanimirovic, D. D., Bokonjić, D., Ocic, G. G., & Bošković, B. (2008) · Experimental Biology and Medicine · doi:10.3181/0803-rm-83 · Cited by 49 · see citing works
Ceftriaxone attenuates hypoxic-ischemic brain injury in neonatal rats
Lai, P., Huang, Y., Wu, C. C., Lai, C.-J., Wang, P. J., & Chiu, T. H. (2011) · Journal of Biomedical Science · doi:10.1186/1423-0127-18-69 · Cited by 46 · see citing works
N-Acetylcysteine and Ceftriaxone as Preconditioning Strategies in Focal Brain Ischemia: Influence on Glutamate Transporters Expression
Krzyżanowska, W., Pomierny, B., Budziszewska, B., Filip, M., & Pera, J. (2016) · Neurotoxicity Research · doi:10.1007/s12640-016-9602-z · Cited by 46 · see citing works
Self-citation
Glutamatergic mechanisms of comorbidity between acute stress and cocaine self-administration
García‐Keller, C., Kupchik, Y. M., Gipson, C. D., Brown, R. M., Spencer, S. M., Bollati, F. A., Esparza, M. A., Roberts-Wolfe, D., Heinsbroek, J. A., Bobadilla, A., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.151 · Cited by 45 · see citing works
Beta-lactam antibiotic decreases acquisition of and motivation to respond for cocaine, but not sweet food, in C57Bl/6 mice
Ward, S. J., Rasmussen, B. A., Corley, G., Henry, C., Kim, J. K., Walker, E. A., & Rawls, S. M. (2011) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3283473c10 · Cited by 41 · see citing works
Ceftriaxone and cefazolin attenuate the cue-primed reinstatement of alcohol-seeking
Weiland, A. K., Garcia, S., & Knackstedt, L. A. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00044 · Cited by 40 · see citing works
Self-citation
In vivo activity of ceftriaxone (Ro 13-9904), a new broad-spectrum semisynthetic cephalosporin
Beskid, G., Christenson, J. G., Cleeland, R., DeLorenzo, W. F., & Trown, P. W. (1981) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.20.2.159 · Cited by 40 · see citing works
Cocaine-induced neuroadaptations in the dorsal striatum: Glutamate dynamics and behavioral sensitization
Parikh, V., Naughton, S. X., Shi, X., Kelley, L. K., Yegla, B., Tallarida, C. S., Rawls, S. M., & Unterwald, E. M. (2014) · Neurochemistry International · doi:10.1016/j.neuint.2014.05.016 · Cited by 39 · see citing works
Ceftriaxone Protects Astrocytes from MPP+ via Suppression of NF-ΚB/JNK/c-Jun Signaling
Zhang, Y., Zhang, X., & Qu, S. (2015) · Molecular Neurobiology · doi:10.1007/s12035-014-8845-z · Cited by 39 · see citing works
Sequential cocaine-alcohol self-administration produces adaptations in rat nucleus accumbens core glutamate homeostasis that are distinct from those produced by cocaine self-administration alone
Stennett, B., Padovan‐Hernandez, Y., & Knackstedt, L. A. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0452-2 · Cited by 39 · see citing works
Self-citation
Effects of Administered Ethanol and Methamphetamine on Glial Glutamate Transporters in Rat Striatum and Hippocampus
Alshehri, F. S., Althobaiti, Y. S., & Sari, Y. (2016) · Journal of Molecular Neuroscience · doi:10.1007/s12031-016-0859-8 · Cited by 38 · see citing works
The beta-lactam antibiotic, ceftriaxone, inhibits the development of opioid-induced hyperalgesia in mice
Chen, Z., He, Y. Z., & Wang, Z. J. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.12.029 · Cited by 37 · see citing works
Altered astrocytic response to activation in SOD1G93A mice and its implications on amyotrophic lateral sclerosis pathogenesis
Benkler, C., Ben‐Zur, T., Barhum, Y., & Offen, D. (2012) · Glia · doi:10.1002/glia.22428 · Cited by 36 · see citing works
Effects of ceftriaxone on hydrocodone seeking behavior and glial glutamate transporters in P rats
Alshehri, F. S., Hakami, A. Y., Althobaiti, Y. S., & Sari, Y. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.03.043 · Cited by 36 · see citing works
Ceftriaxone reduces alcohol intake in outbred rats while upregulating xCT in the nucleus accumbens core
Stennett, B., Frankowski, J. C., Peris, J., & Knackstedt, L. A. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.07.001 · Cited by 33 · see citing works
Self-citation
Effects of Ceftriaxone on Glial Glutamate Transporters in Wistar Rats Administered Sequential Ethanol and Methamphetamine
Althobaiti, Y. S., Alshehri, F. S., Almalki, A. H., & Sari, Y. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00427 · Cited by 30 · see citing works
Modulation of the expression of genes related to the system of amyloid-beta metabolism in the brain as a novel mechanism of ceftriaxone neuroprotective properties
Tikhonova, M. A., Amstislavskaya, T. G., Belichenko, V. M., Fedoseeva, L. A., Kovalenko, S. P., Pisareva, E. E., Avdeeva, A. S., Kolosova, N. G., Belyaev, N. D., & Aftanas, L. I. (2018) · BMC Neuroscience · doi:10.1186/s12868-018-0412-5 · Cited by 30 · see citing works
Positive effects of ceftriaxone on pentylenetetrazol-induced convulsion model in rats
Uyanıkgil, Y., Özkeşkek, K., Çavuşoğlu, T., Solmaz, V., Tümer, M. K., & Erbaş, O. (2014) · International Journal of Neuroscience · doi:10.3109/00207454.2014.991821 · Cited by 29 · see citing works
Synergistic effects of ceftriaxone and erythropoietin on neuronal and behavioral deficits in an MPTP-induced animal model of Parkinson’s disease dementia
Huang, C.-K., Chang, Y., Amstislavskaya, T. G., Tikhonova, M. A., Lin, C., Hung, C., Lai, T., & Ho, Y. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.08.011 · Cited by 28 · see citing works
Neonatal dexamethasone treatment exacerbates hypoxic-ischemic brain injury
Chang, K. H., Yeh, C.-M., Yeh, C. Y., Huang, C., & Hsu, K. (2013) · Molecular Brain · doi:10.1186/1756-6606-6-18 · Cited by 26 · see citing works
The effects of ceftriaxone on skill learning and motor functional outcome after ischemic cortical damage in rats
Kim, S. Y., & Jones, T. A. (2013) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2012-120245 · Cited by 24 · see citing works
Ceftriaxone attenuates acute cocaine‐evoked dopaminergic neurotransmission in the nucleus accumbens of the rat
Barr, J. L., Rasmussen, B. A., Tallarida, C. S., Scholl, J. L., Forster, G. L., Unterwald, E. M., & Rawls, S. M. (2015) · British Journal of Pharmacology · doi:10.1111/bph.13330 · Cited by 23 · see citing works
Ceftriaxone Preconditioning Confers Neuroprotection in Neonatal Rats Through Glutamate Transporter 1 Upregulation
Mimura, K., Tomimatsu, T., Minato, K., Jugder, O., Kinugasa-Taniguchi, Y., Kanagawa, T., Nozaki, M., Yanagihara, I., & Kimura, T. (2011) · Reproductive Sciences · doi:10.1177/1933719111410710 · Cited by 23 · see citing works
Lack of Effect of Ceftriaxone, a GLT-1 Transporter Activator, on Spatial Memory in Mice
Karaman, I., Kizilay-Ozfidan, G., Karadag, C. H., & Ulugol, A. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.04.013 · Cited by 23 · see citing works
Neuroprotective effect of ceftriaxone on the penumbra in a rat venous ischemia model
Inui, T., Alessandri, B., Heimann, A., Nishimura, F., Frauenknecht, K. B. M., Sommer, C., & Kempski, O. S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.018 · Cited by 23 · see citing works
Alterations in Neuronal Survival and Glial Reactions after Axotomy by Ceftriaxone and Minocycline in the Mouse Hypoglossal Nucleus
Yamada, J., & Jinno, S. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.09.051 · Cited by 21 · see citing works
Effectiveness of Ceftriaxone Treatment in Preventing Relapse-like Drinking Behavior Following Long-term Ethanol Dependence in P Rats
Sari, Y. (2014) · Journal of Addiction Research & Therapy · doi:10.4172/2155-6105.1000183 · Cited by 21 · see citing works
Changes in the glutamate biomarker expression in rats vulnerable or resistant to the rewarding effects of cocaine and their reversal by ceftriaxone
Niedzielska, E., Mizera, J., Sadakierska−Chudy, A., Pomierny-Chamioło, L., & Filip, M. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.111945 · Cited by 19 · see citing works
Self-citation
Preclinical rodent toxicity studies for long term use of ceftriaxone
Ratti, E., Berry, J. D., Greenblatt, D. J., Loci, L., Ellrodt, A. S., Shefner, J. M., & Cudkowicz, M. (2015) · Toxicology Reports · doi:10.1016/j.toxrep.2015.09.010 · Cited by 17 · see citing works
The Importance of Preclinical Trial Timing – a Potential Reason for the Disconnect between mouse Studies and Human Clinical Trials in ALS
Kong, Q., Carothers, S., Chang, Y., & Lin, C. G. (2012) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2012.00358.x · Cited by 17 · see citing works
Dynamic interactions of ceftriaxone and environmental variables suppress amphetamine seeking
Garcia, E. J., Arndt, D. L., & Cain, M. E. (2019) · Brain Research · doi:10.1016/j.brainres.2019.01.044 · Cited by 17 · see citing works
Genetic and pharmacological manipulation of glial glutamate transporters does not alter infection-induced seizure activity
Loewen, J. L., Albertini, G., Dahle, E. J., Sato, H., Smolders, I. J., Massie, A., & Wilcox, K. S. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.04.010 · Cited by 16 · see citing works
Effects of ceftriaxone on ischemia/reperfusion injury in rat brain
Altaş, M., Meydan, S., Aras, M., Yılmaz, N., Ulutaş, K. T., Okuyan, H. M., & Nacar, A. (2012) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2012.05.030 · Cited by 13 · see citing works
Ceftriaxone reverses ketamine-induced lasting EEG and astrocyte alterations in juvenile mice
Dodman, K. G., Featherstone, R. E., Bang, J., Liang, Y., & Siegel, S. J. (2015) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2015.07.1198 · Cited by 12 · see citing works
MDMA decreases glutamic acid decarboxylase (GAD) 67-immunoreactive neurons in the hippocampus and increases seizure susceptibility: Role for glutamate
Huff, C., Morano, R. L., Herman, J. P., Yamamoto, B. K., & Gudelsky, G. A. (2016) · NeuroToxicology · doi:10.1016/j.neuro.2016.10.011 · Cited by 12 · see citing works

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1 of the 109 references couldn’t be matched to a known paper.

Sorted by citations

The Interplay between Gut Microbiota and Parkinson’s Disease: Implications on Diagnosis and Treatment
Varesi, A., Campagnoli, L. I. M., Fahmideh, F., Pierella, E., Romeo, M., Ricevuti, G., Nicoletta, M., Chirumbolo, S., & Pascale, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012289 · Cited by 88 · see citing works
N‐acetylcysteine as a new prominent approach for treating psychiatric disorders
Smaga, I., Frankowska, M., & Filip, M. (2021) · British Journal of Pharmacology · doi:10.1111/bph.15456 · Cited by 73 · see citing works
Self-citation
Interactions of neuroimmune signaling and glutamate plasticity in addiction
Gipson, C. D., Rawls, S. M., Scofield, M. D., Siemsen, B. M., Bondy, E. O., & Maher, E. E. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02072-8 · Cited by 67 · see citing works
“Activation of this pathway appears to interact with glutamate signaling in addiction models [228, 278, 280, 297], and as such, the NF-κB pathway may prove critical”
Background
Glial Glutamate Transporter-Mediated Plasticity: System xc-/xCT/SLC7A11 and EAAT1/2 in Brain Diseases
Dahlmanns, M., Dahlmanns, J. K., Savaskan, N. E., Steiner, H. H., & Yakubov, E. (2023) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2803057 · Cited by 52 · see citing works
“Increasing the glutamate transporter EAAT2 expression by gain-of-function gene targeting [101,102] ameliorated this phenotype [100].”
Background
Cellular mechanisms in brain aging: Focus on physiological and pathological aging
Aguilar‐Hernández, L., Alejandre‐Aguilar, R., Morales‐Medina, J. C., Iannitti, T., & Flores, G. (2022) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2022.102210 · Cited by 43 · see citing works
Glutamate homeostasis and dopamine signaling: Implications for psychostimulant addiction behavior
Fischer, K. D., Knackstedt, L. A., & Rosenberg, P. A. (2020) · Neurochemistry International · doi:10.1016/j.neuint.2020.104896 · Cited by 40 · see citing works
Self-citation
Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis
Hong, D., Zhang, C., Wu, W., Lu, X., & Zhang, L. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1133546 · Cited by 38 · see citing works
The Effect of GLT-1 Upregulation on Extracellular Glutamate Dynamics
Wilkie, C. M., Barron, J. C., Brymer, K. J., Barnes, J. R., Nafar, F., & Parsons, M. P. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.661412 · Cited by 36 · see citing works
“LDN also exhibits protective effects in many similar disease models (Kong et al., 2014; Takahashi et al., 2015).”
Background
Regulation of cocaine-related behaviours by estrogen and progesterone
Peart, D. R., Andrade, A. K., Logan, C. N., Knackstedt, L. A., & Murray, J. E. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104584 · Cited by 34 · see citing works
Self-citation
Gut microbiota manipulation as an epilepsy treatment
Iannone, L. F., Gómez-Eguílaz, M., & Caro, C. D. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105897 · Cited by 40 · see citing works
“Moreover, it is well known that also antibiotics modify GM community clearly representing the most direct and effective way of targeting intestinal microbes (Smaga et al., 2020).”
N-acetylcysteine in substance use disorder: a lesson from preclinical and clinical research
Smaga, I., Frankowska, M., & Filip, M. (2021) · Pharmacological Reports · doi:10.1007/s43440-021-00283-7 · Cited by 32 · see citing works
Self-citation
Neuroprotective Effects of Ceftriaxone Involve the Reduction of Aβ Burden and Neuroinflammatory Response in a Mouse Model of Alzheimer’s Disease
Tikhonova, M. A., Amstislavskaya, T. G., Ho, Y., Akopyan, A. A., Tenditnik, M. V., Ovsyukova, M. V., Bashirzade, A. A., Dubrovina, N. I., & Aftanas, L. I. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.736786 · Cited by 33 · see citing works
Gut-microbiota-directed strategies to treat epilepsy: clinical and experimental evidence
Granados, D. M. M., Villasana‐Salazar, B., Lozano‐García, L., Cavalheiro, É. A., & Striano, P. (2021) · Seizure · doi:10.1016/j.seizure.2021.03.009 · Cited by 30 · see citing works
Persistent Neuroadaptations in the Nucleus Accumbens Core Accompany Incubation of Methamphetamine Craving in Male and Female Rats
Funke, J. R., Hwang, E.-K., Wunsch, A. M., Baker, R., Engeln, K. A., Murray, C. H., Milovanovic, M., Caccamise, A. J., & Wolf, M. E. (2023) · eNeuro · doi:10.1523/eneuro.0480-22.2023 · Cited by 27 · see citing works
“, for 5–12d), increases expression of the glutamate transporter GLT-1 and normalizes behavioral and neurochemical effects produced by repeated administration of drugs of abuse (Smaga et al., 2020).”
Background
β-lactam antibiotics to tame down molecular pathways of Alzheimer's disease
Kumari, S., & Deshmukh, R. R. (2021) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2021.173877 · Cited by 24 · see citing works
MC-100093, a Novel β-Lactam Glutamate Transporter-1 Enhancer Devoid of Antimicrobial Properties, Attenuates Cocaine Relapse in Rats
Knackstedt, L. A., Wu, L., Rothstein, J., Vidensky, S., Gordon, J. C., Ramanjulu, M. M., Dunman, P. M., Blass, B. E., Childers, W. E., & Abou-Gharbia, M. A. (2021) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.121.000532 · Cited by 24 · see citing works
Self-citation
Targeting Neuroplasticity in Substance Use Disorders: Implications for Therapeutics
Wolf, M. E. (2024) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-061724-080548 · Cited by 22 · see citing works
“As reviewed elsewhere (42), the antibiotic ceftriaxone restores glutamate homeostasis by normalizing the reductions in xCT and GLT-1 produced by cocaine self-administration and extinction.”
Influential
Rational Design and Acoustic Assembly of Human Cerebral Cortex‐Like Microtissues from hiPSC‐Derived Neural Progenitors and Neurons
Wang, J., Qiao, H., Wang, Z., Zhao, W., Chen, T., Li, B., Zhu, L., Chen, S., Gu, L., Wu, Y., et al. (2023) · Advanced Materials · doi:10.1002/adma.202210631 · Cited by 20 · see citing works
Astrocyte-Synapse Structural Plasticity in Neurodegenerative and Neuropsychiatric Diseases
Badia‐Soteras, A., Mak, A., Blok, T. M., Boers-Escuder, C., van den Oever, M. C., Min, R., Smit, A. B., & Verheijen, M. H. G. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.04.011 · Cited by 18 · see citing works
Ultrasound Neuromodulation: Integrating Medicine and Engineering for Neurological Disease Treatment
Chen, Y., Li, Y., Du, M., Yu, J., Gao, F., Yuan, Z., & Chen, Z. (2021) · BIO Integration · doi:10.15212/bioi-2020-0026 · Cited by 16 · see citing works
“Drug therapy Simplicity, efficiency Drug resistance Epilepsy [5], tremor [6], Alzheimer’s disease [7], depression [8], Parkinson’s disease [9]”
Background
Extrasynaptic therapeutic targets in substance use and stress disorders
Hodebourg, R., Kalivas, P. W., & Kruyer, A. (2021) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2021.10.006 · Cited by 16 · see citing works
Intrusive thinking: Circuit and synaptic mechanisms of a transdiagnostic psychiatric symptom
Kalivas, P. W., Gourley, S. L., & Paulus, M. P. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105196 · Cited by 16 · see citing works
Effects of ceftriaxone on ethanol drinking and GLT-1 expression in ethanol dependence and relapse drinking
Griffin, W. C., Haun, H. L., Ramachandra, V. S., Knackstedt, L. A., Mulholland, P. J., & Becker, H. C. (2021) · Alcohol · doi:10.1016/j.alcohol.2021.01.004 · Cited by 15 · see citing works
Self-citation
Induction of Parkinsonian-Like Changes via Targeted Downregulation of Astrocytic Glutamate Transporter GLT-1 in the Striatum
Ren, C., He, K.-J., Hu, H., Zhang, J.-B., Dong, L.-G., Li, D., Chen, J., Mao, C.-J., Wang, F., & Liu, C.-F. (2021) · Journal of Parkinson s Disease · doi:10.3233/jpd-212640 · Cited by 15 · see citing works
Elevation of Extracellular Glutamate by Blockade of Astrocyte Glutamate Transporters Inhibits Cocaine Reinforcement in Rats via a NMDA-GluN2B Receptor Mechanism
Yang, H.-J., Hempel, B. J., Bi, G.-H., He, Y., Zhang, H.-Y., Gardner, E. L., & Xi, Z.-X. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1432-21.2022 · Cited by 13 · see citing works
Hippocampal region-specific endogenous neuroprotection as an approach in the search for new neuroprotective strategies in ischemic stroke. Fiction or fact?
Beresewicz, M. (2022) · Neurochemistry International · doi:10.1016/j.neuint.2022.105455 · Cited by 12 · see citing works
Neuroinflammation and Neurometabolomic Profiling in Fentanyl Overdose Mouse Model Treated with Novel β-Lactam, MC-100093, and Ceftriaxone
Alasmari, M. S., Alasmari, F. F., AlSharari, S. D., Alasmari, A. F., Ali, N., Ahamad, S. R., Alghamdi, A. M., Kadi, A. A., Hammad, A. M., Ali, Y. S. M., et al. (2024) · Toxics · doi:10.3390/toxics12080604 · Cited by 12 · see citing works
“The astrocytic glutamate transporter 1 (GLT-1) regulates the majority of extracellular glutamate concentrations in the brain [11] and is potentially considered as a target for the treat-ment of neurological diseases and psychiatric disorders involving hyperglutamatergic states [7,12–14].”
BackgroundResult
Sequencing hour-level temporal patterns of polysubstance use among persons who use cocaine, alcohol, and cannabis: A back-translational approach
Fitzgerald, N. D., Liu, Y., Wang, A., Striley, C. W., Setlow, B., Knackstedt, L. A., & Cottler, L. B. (2024) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2024.111272 · Cited by 11 · see citing works
Self-citation
Gut microbiota and Parkinson’s disease: exploring pathogenesis and potential therapeutic strategies from a gut-brain axis perspective
Jin, X., Wei, J., Min, X., Fan, Y., Yuan, Z., Du, Z., Su, Z., Xun, T., Du, Q., Liang, T., et al. (2025) · iScience · doi:10.1016/j.isci.2025.114185 · Cited by 10 · see citing works
“238,242 246–248 However, discrepancies remain between clinical and preclinical antibiotic data, alongside concerns regarding antibiotic-induced gut dysbiosis, antibiotic resistance, and potential adverse effects.”
Ceftriaxone alters the gut microbiome composition and reduces alcohol intake in male and female Sprague–Dawley rats
Duclot, F., Wu, L., Wilkinson, C. S., Kabbaj, M., & Knackstedt, L. A. (2024) · Alcohol · doi:10.1016/j.alcohol.2024.01.006 · Cited by 10 · see citing works
Self-citation
A maternal high-fat diet during pregnancy and lactation disrupts short-term memory functions via altered hippocampal glutamatergic signaling in female rat offspring
Smaga, I., Gawlińska, K., Gawliński, D., Surówka, P., & Filip, M. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114396 · Cited by 10 · see citing works
Self-citation
Effects of novel beta-lactam, MC-100093, and ceftriaxone on astrocytic glutamate transporters and neuroinflammatory factors in nucleus accumbens of C57BL/6 mice exposed to escalated doses of morphine
Sari, Y., Swiss, G. M. S., Alrashedi, F. A., Baeshen, K. A., Alshammari, S. A., AlSharari, S. D., Ali, N., Alasmari, A. F., Alhoshani, A., Alameen, A. A., et al. (2024) · Saudi Pharmaceutical Journal · doi:10.1016/j.jsps.2024.102108 · Cited by 9 · see citing works
“Downregulation of GLT-1 is key factor in the development of dependence and tolerance to drugs of abuse, including opioids (Abulseoud et al., 2022;Smaga et al., 2020).”
Arc and BDNF mediated effects of hippocampal astrocytic glutamate uptake blockade on spatial memory stages
Riboldi, J. G., Correa, J., Renfijes, M. M., Tintorelli, R., & Viola, H. (2024) · Communications Biology · doi:10.1038/s42003-024-06586-8 · Cited by 8 · see citing works
“To do this, we used theantibioticCeftriaxone(CFT),a β -lactamantibiotic,which,administered sub-chronically, induces an upregulation in GLT-1 in Hp and other brain regions 23,31 .”
Ceftriaxone affects ferroptosis and alleviates glial cell activation in Parkinson's disease
Zhi, H., Wang, X., Chen, Y., Cai, Z., Li, J., & Guo, D. (2025) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2025.5526 · Cited by 8 · see citing works
Neurodegeneration, Mitochondria, and Antibiotics
Suarez-Rivero, J. M., López‐Pérez, J., Muela‐Zarzuela, I., Pastor‐Maldonado, C. J., Cilleros-Holgado, P., Gómez-Fernández, D., Álvarez-Córdoba, M., Munuera-Cabeza, M., Talaverón-Rey, M., Povea-Cabello, S., et al. (2023) · Metabolites · doi:10.3390/metabo13030416 · Cited by 8 · see citing works
“reported that a dose of 200 mg/kg of ceftriaxone for a minimum of 2 days restored GLT1 expression [296].”
Background
Unveiling the contribution mechanism and the role of oxygen vacancies in the simultaneous electrochemical sensing of ceftriaxone and diclofenac by CPE/zeolite
Khosravi‐Hamoleh, A., Taban, R., & Cheraghizade, M. (2025) · Materials Research Bulletin · doi:10.1016/j.materresbull.2025.113398 · Cited by 7 · see citing works
Glutamatergic Agents for the Treatment of Cocaine Use Disorder
Hadizadeh, H., Flores, J. M., Mayerson, T. F., Worhunsky, P. D., Potenza, M. N., & Angarita, G. A. (2022) · Current Behavioral Neuroscience Reports · doi:10.1007/s40473-022-00252-1 · Cited by 7 · see citing works
From Stress to Substance Use Disorders: The Expanding Role of Microglia–Astrocyte Crosstalk in Neuroimmune and Glutamate Alterations in the Nucleus Accumbens
Cancela, L. M., Mongi‐Bragato, B., Avalos, M. P., & Bollati, F. A. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms27010385 · Cited by 9 · see citing works
“…NF-κ B transcriptomic profile did not correlate with GLT-1 expression changes in the prefrontal cortex following extinction training after cocaine self-administration [366], suggesting that NF-κ B may exert region-specific regulatory control over GLT-1 expression under conditions of drug exposure.”
An Eluate of the Medicinal Plant Garcinia kola Displays Strong Antidiabetic and Neuroprotective Properties in Streptozotocin-Induced Diabetic Mice
Etet, P. F. S., Hamza, M. A., El-Tahir, A., Vecchio, L., Osman, S. Y., Satti, G. M. H., Ismail, M. H. A., Farahna, M., NJAMNSHI, A. K., & Adem, A. (2022) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2022/8708961 · Cited by 6 · see citing works
Effects of waterpipe tobacco smoke and ceftriaxone treatment on the expression of endocannabinoid receptors in mesocorticolimbic brain regions
Hammad, A. M., Meknas, S. J., Hall, F. S., Hikmat, S., Sari, Y., Al-Qirim, T. M., Alfaraj, M., & Amawi, H. A. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.04.014 · Cited by 5 · see citing works
Enhancement of the GluN2B subunit of glutamatergic NMDA receptors in rat brain areas after cocaine abstinence
Smaga, I., Wydra, K., Suder, A., Sanak, M., Caffino, L., Fumagalli, F., & Filip, M. (2021) · Journal of Psychopharmacology · doi:10.1177/02698811211048283 · Cited by 5 · see citing works
“During food-training, the animals did not have any amplification in the form of light and sound exposure (Smaga et al., 2020c).”
BackgroundInfluentialSelf-citation
The role of glutamate transporter-1 in firing activity of locus coeruleus neurons and nociception in rats
Nozad, A., Hamidi, N., & Amani, M. (2021) · Experimental Brain Research · doi:10.1007/s00221-021-06065-0 · Cited by 4 · see citing works
“It has been elucidated that CFT, a beta-lactam antibiotic, can selectively induce the GLT1 gene expression in astrocytes as shown in our study (Smaga et al. 2020).”
Result
The need to incorporate polysubstance use in neuropsychopharmacology research: Biological lessons and new opportunities
Joffe, M. E., Ferguson, S. M., Gilpin, N. W., Herman, M. A., Knackstedt, L. A., Randall, P. A., Schindler, A. G., Torregrossa, M. M., & Rinker, J. A. (2025) · Addiction Neuroscience · doi:10.1016/j.addicn.2025.100246 · Cited by 3 · see citing works
“Notably, the antibiotic ceftriaxone, which reliably prevents the reinstatement of cocaine-seeking in dozens of studies [92] is ineffective in cocaine-alcohol polysubstance use [89].”
Self-citation
Ceftriaxone and MC-100093 mitigate fentanyl-induced cardiac injury in mice: Preclinical investigation of its underlying molecular mechanisms
Alasmari, A. F., Alshehri, M. M., Ali, N., Alasmari, F. F., Sari, Y., Childers, W. E., Abou-Gharbia, M. A., Alharbi, M., El-Nagar, D. M., & AL-Qahtani, W. S. (2024) · Saudi Pharmaceutical Journal · doi:10.1016/j.jsps.2024.102148 · Cited by 3 · see citing works
“Moreover, it was documented that ceftriaxone significantly induced xCT expression, which could justify the protective effect of ceftriaxone (Rao et al., 2015, Smaga et al., 2020, Das et al., 2022).”
Background
The interplay between gut microbiome, epigenetics, and substance use disorders: from molecular to clinical perspectives
Sahebi, K., Arianejad, M., Azadi, S., Hosseinpour-Soleimani, F., Kazemi, R., Tajbakhsh, A., & Negahdaripour, M. (2025) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2025.177630 · Cited by 3 · see citing works
Differential Effects of Hippocampal Astrocytic Glutamate Uptake Modulation on Aversive Memory Formation and Expression
Renfijes, M. M., Riboldi, J. G., Correa, J., Iribarne, J., Medina, J. H., & Viola, H. (2025) · Journal of Neurochemistry · doi:10.1111/jnc.70144 · Cited by 2 · see citing works
“This increase is more sensitive and happens earlier in the Hp of the animals than in other brain regions (Smaga et al. 2020).”
Differential Modulation of Glutamate Transporter‐1 by Cocaine and Oxycodone and the Efficacy of MC‐100093 to Reduce Reinstatement of Self‐Administration
Hart, D. W., Alonso‐Caraballo, Y., Hornback, B., Robert, A., Brickner, M. A., Esguerra, M., Childers, W. E., Abou-Gharbia, M. A., & Thomas, M. J. (2025) · Brain and Behavior · doi:10.1002/brb3.70616 · Cited by 2 · see citing works
“Most of the preclinical work with beta-lactams and SUDs has focused on cocaine and other psychostimulants (Smaga et al. 2020).”
Influential
Beta-lactam Antibiotic Cefepime Attenuates Lipopolysaccharide-induced Pain and Depression By Modulating Inflammatory Response and Astroglial Glutamate Transporter in Mice
Khan, A., Ronan, P. J., & Rahman, S. (2026) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-026-10279-w · Cited by 4 · see citing works
“…antibiotics have been shown to inhibit neuroinflammatory responses by reducing the microglial activation and release of proinflammatory cytokines, thus offering neuroprotection in various experimental models (Nizzardo et al. 2011 ; Yimer et al. 2019; Nath et al. 2020 ; Smaga et al. 2020 ).”
Targeting TLR4 in Parkinson's disease: mechanisms and therapeutic prospects
Dong, S., Lu, J., Wu, L., Wang, S., 宫玉波, Hu, J., Liu, Y., & Chen, X. (2026) · International Immunopharmacology · doi:10.1016/j.intimp.2026.116780 · Cited by 2 · see citing works
Fabrication and Characterization of Ibuprofen and Ceftriaxone loaded Electrospun Cellulose Acetate Nanofiber Layers as a Model of Targeted Drug Delivery System
Satriawan, N. E., Khotib, J., Nasir, M., & Zaidan, A. H. (2023) · ALCHEMY Journal of Chemistry · doi:10.18860/al.v10i2.15502 · Cited by 2 · see citing works
Ceftriaxone Inhibits Conditioned Fear and Compulsive-like Repetitive Marble Digging without Central Nervous System Side Effects Typical of Diazepam—A Study on DBA2/J Mice and a High-5HT Subline of Wistar–Zagreb 5HT Rats
Poljak, L., Miše, B., Čičin‐Šain, L., & Tvrdeić, A. (2024) · Biomedicines · doi:10.3390/biomedicines12081711 · Cited by 2 · see citing works
“The amygdala [47] and hippocampus [48] are involved in OCD and PTSD. Ceftriaxone is most effective as a GLT1 expression enhancer to prevent hyperglutamate states [15].”
Background
Differential Effects of Intrahippocampal Administration of Ceftriaxone on Morphine Dependence and Withdrawal Syndrome in Rats
Saeedi, N., Giahi, M., suha, A. J., Azizi, H., Janahmadi, M., & Hosseinmardi, N. (2024) · ACS Omega · doi:10.1021/acsomega.4c05331 · Cited by 2 · see citing works
Intravenous administration of Tat-NR2B9c peptide, a PSD95 inhibitor, attenuates reinstatement of cocaine-seeking behavior in rats
Smaga, I., Wydra, K., Witek, K., Surówka, P., Suder, A., Pieniążek, R., Caffino, L., Fumagalli, F., Sanak, M., & Filip, M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113537 · Cited by 2 · see citing works
Self-citation
Neural correlates of β-lactam exposure in intensive care unit patients: an observational, prospective cohort study
Zalta, A., Trébuchon, A., Daquin, G., Velly, L. J., Léone, M., Blin, O. J., Lagarde, S., & Guilhaumou, R. (2025) · Journal of Neurology · doi:10.1007/s00415-025-13067-3 · Cited by 1 · see citing works
GLUTAMATE AS A TARGET THERAPY FOR ALCOHOL DEPENDENCE DISORDER
Najim, S. M., Sadeq, Z. A., & Sabri, L. A. (2023) · Military Medical Science Letters · doi:10.31482/mmsl.2023.002 · Cited by 1 · see citing works
Effects of Beta Lactams on Behavioral Outcomes of Substance Use Disorders: A Meta-Analysis of Preclinical Studies
Alasmari, M. S., Almohammed, O. A., Hammad, A. M., Altulayhi, K. A., Alkadi, B. K., Alasmari, A. F., Alqahtani, F., Sari, Y., & Alasmari, F. F. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.11.014 · Cited by 1 · see citing works
Mesenchymal stem cells as a promising therapy for alcohol use disorder
Gallardo, J., Berríos‐Cárcamo, P., & Ezquer, F. E. (2024) · International review of neurobiology · doi:10.1016/bs.irn.2024.07.002 · Cited by 1 · see citing works
Individual differences in cocaine seeking during voluntary abstinence predicts cocaine relapse and the circuitry mediating relapse
Padovan‐Hernandez, Y., Rojas, G., Wu, L., & Knackstedt, L. A. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06270-x · Cited by 1 · see citing works
Self-citation
Linking Polysubstance Use, Glutamate, and the Nucleus Accumbens
Knackstedt, L. A. (2022) · Springer eBooks · doi:10.1007/978-3-030-67928-6_153-1
Self-citation
Linking Polysubstance Use, Glutamate, and the Nucleus Accumbens
Knackstedt, L. A. (2022) · Springer eBooks · doi:10.1007/978-3-030-92392-1_153
Self-citation
The Role of Beta-Lactam Antibiotics in Reactive Oxygen Species Generation and Therapeutic Implications
Basu, S., Valente, M., & Banik, B. K. (2025) · Current Medicinal Chemistry · doi:10.2174/0109298673367879250820164456
Histological and electrophysiological effects of sulbactam and valproate in the PTZ-induced epileptic rat model
Hsieh, Y.-J., Chang, F., Liu, C., Hsiao, Y., Liao, W., Tsai, R., Prabawanti, C., Lin, C., Hung, C., & Ho, Y. (2025) · Epilepsy Research · doi:10.1016/j.eplepsyres.2025.107676
MC-100093, a synthetic beta-lactam compound, and ceftriaxone modulate nicotine consumption, neuroinflammation and glutamatergic transporters in a nicotine self-administration mouse model
Alotaibi, J. A., Alasmari, F. F., Albaker, A. B., Alrashedi, F. A., Mohany, M., Alshammari, M. A., Alasmari, A. F., Al-Rejaie, S. S., Childers, W. E., Abou-Gharbia, M. A., et al. (2025) · Psychopharmacology · doi:10.1007/s00213-025-06986-6
Marine-Derived Bioactive Compounds: Promising Agents for the Prophylaxis and Treatment of Neuronal Infections
Lushington, H., Pathak, S., Nadar, R. M., Dhanasekaran, M., & Palekkodan, J. (2026) · Nutritional neurosciences · doi:10.1007/978-981-95-5791-2_10
Ceftriaxone has a similar effect on astrocytic and neuronal GLT-1 distribution after mild traumatic brain injury
Naumenko, Y., Olifirov, B., Yuryshinetz, I., & Pivneva, T. A. (2026) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2026.153895
Novel circUnc79 regulates morphine-induced reward memory via the miR-149-3p/EAAT2 axis and glutamatergic plasticity
Yang, X., Gao, F., Yang, Z., Yu, D., Chen, J., 姚震, Liao, Q., Yang, J., Liu, J., Gu, B., et al. (2026) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2026.06.004
“Unlike systemic agents with limited specificity 62,63 , circUnc79-based approaches could selectively normalize glutamate dynamics in addiction circuits via the ceRNA mechanism.”
Astrocytic α7 nicotinic acetylcholine receptors play an essential role in regulating glutamate dynamics and memory flexibility in the hippocampus
Tropea, M. R., Melone, M., Piacentini, R., Spiezio, A. D., Tore, M., Trovato, R. C., Vacanti, V., Bragina, L., Puliatti, G., Albini, M., et al. (2026) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2026.102943
Pharmacological actions of novel beta-lactam and non-beta lactam compounds on major astrocytic glutamate transporters in the brain and liver of male C57BL/6 mice exposed chronically to hydrocodone
Wong, W., Mohammed, A. S., Childers, W. E., Abou-Gharbia, M. A., & Sari, Y. (2026) · Neurotherapeutics · doi:10.1016/j.neurot.2026.e01071
Long-term ceftriaxone exposure modulates neuroplasticity in hippocampus
Giahi, M., Saeedi, N., Tavassoli, Z., Rostami, F., Janahmadi, M., & Hosseinmardi, N. (2026) · Journal of Neurophysiology · doi:10.1152/jn.00547.2025

Ceftriaxone as a Novel Therapeutic Agent for Hyperglutamatergic States: Bridging the Gap Between Preclinical Results and Clinical Translation
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Ceftriaxone pretreatment confers neuroprotection in rats with acute glaucoma and reduces the score of seizures induced by pentylenotetrazole in mice
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Antibiotic ceftriaxone up-regulates expression of glial glutamate transporter GLT-1 in cultured rat astrocytes and provides neuroprotection
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Authors: Smaga, I., Fierro, D., Mesa, J., Filip, M., & Knackstedt, L. A.
Affiliations: Maj Institute of Pharmacology (PL)
University of Florida (US)
Corresponding author: Knackstedt, Lori A
ORCID: Smaga, Irena
Mesa, Javier
Knackstedt, Lori A
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2020-08
Volume: 115
Pages: 116-130
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2020.05.016
PMC: PMC7483567
OpenAlex: W3032088217
Cited by: 69
References: 109
Citations by year: 2026: 8 · 2025: 13 · 2024: 10 · 2023: 10 · 2022: 12 · 2021: 15 · 2020: 1
FWCI: 1.31
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Drug Abuse (DA033436)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Keywords: ceftriaxone, beta-lactam antibiotics, GLT-1, glutamate transporters, substance use disorders, neurological disease models, glutamate homeostasis, transporter trafficking, tau pathology, amyloid-beta, neuronal cell death, hippocampus, drug repurposing
MeSH terms: Animals, Anti-Bacterial Agents, Ceftriaxone, Rodentia, Amyloid beta-Peptides, Glutamic Acid, Substance-Related Disorders, Excitatory Amino Acid Transporter 2

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Molecular changes evoked by the beta-lactam antibiotic ceftriaxone across rodent models of substance use disorder and neurological disease

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