دورية أكاديمية

Microbial short-chain fatty acids regulate drug seeking and transcriptional control in a model of cocaine seeking.

التفاصيل البيبلوغرافية
العنوان: Microbial short-chain fatty acids regulate drug seeking and transcriptional control in a model of cocaine seeking.
المؤلفون: Meckel KR; Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.; Department of Biology, Swarthmore College, Swarthmore, PA, 19081, USA., Simpson SS; Department of Psychiatry, University of California San Diego, La Jolla, CA, USA., Godino A; Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA., Peck EG; Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.; Department of Physiology & Pharmacology, Wake Forest University School of Medicine, Atrium Wake Forest Baptist Health, Winston-Salem, NC, 27101, USA., Sens JP; Department of Physiology & Pharmacology, Wake Forest University School of Medicine, Atrium Wake Forest Baptist Health, Winston-Salem, NC, 27101, USA., Leonard MZ; Department of Pharmacology, Vanderbilt University, Nashville, TN, USA., George O; Department of Psychiatry, University of California San Diego, La Jolla, CA, USA., Calipari ES; Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.; Department of Pharmacology, Vanderbilt University, Nashville, TN, USA.; Vanderbilt Brain Institute, Vanderbilt University, 865F Light Hall, 2215 Garland Avenue, Nashville, TN, 37232, USA.; Vanderbilt Center for Addiction Research, Vanderbilt University, Nashville, TN, USA.; Department of Molecular Physiology and Biophysics, Vanderbilt University, Nashville, TN, USA.; Department of Psychiatry and Behavioral Sciences, Vanderbilt University, Nashville, TN, USA., Hofford RS; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.; Department of Physiology & Pharmacology, Wake Forest University School of Medicine, Atrium Wake Forest Baptist Health, Winston-Salem, NC, 27101, USA.; Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA., Kiraly DD; Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA. dkiraly@wakehealth.edu.; Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA. dkiraly@wakehealth.edu.; Department of Physiology & Pharmacology, Wake Forest University School of Medicine, Atrium Wake Forest Baptist Health, Winston-Salem, NC, 27101, USA. dkiraly@wakehealth.edu.; Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA. dkiraly@wakehealth.edu.; Department of Psychiatry, Wake Forest University School of Medicine, Atrium Wake Forest Baptist Health, Winston-Salem, NC, 27101, USA. dkiraly@wakehealth.edu.
المصدر: Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology [Neuropsychopharmacology] 2024 Jan; Vol. 49 (2), pp. 386-395. Date of Electronic Publication: 2023 Aug 02.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 8904907 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1740-634X (Electronic) Linking ISSN: 0893133X NLM ISO Abbreviation: Neuropsychopharmacology Subsets: MEDLINE
أسماء مطبوعة: Publication: 2003- : London : Nature Publishing Group
Original Publication: [New York, NY] : Elsevier, [c1987-
مواضيع طبية MeSH: Cocaine* , Cocaine-Related Disorders*/metabolism, Mice ; Rats ; Male ; Animals ; Rats, Sprague-Dawley ; Drug-Seeking Behavior ; Nucleus Accumbens ; Recurrence ; Self Administration ; Cues ; Extinction, Psychological
مستخلص: Cocaine use disorder represents a public health crisis with no FDA-approved medications for its treatment. A growing body of research has detailed the important connections between the brain and the resident population of bacteria in the gut, the gut microbiome, in psychiatric disease models. Acute depletion of gut bacteria results in enhanced reward in a mouse cocaine place preference model, and repletion of bacterially-derived short-chain fatty acid (SCFA) metabolites reverses this effect. However, the role of the gut microbiome and its metabolites in modulating cocaine-seeking behavior after prolonged abstinence is unknown. Given that relapse prevention is the most clinically challenging issue in treating substance use disorders, studies examining the effects of microbiome manipulations in relapse-relevant models are critical. Here, male Sprague-Dawley rats received either untreated water or antibiotics to deplete the gut microbiome and its metabolites. Rats were trained to self-administer cocaine and subjected to either within-session threshold testing to evaluate motivation for cocaine or 21 days of abstinence followed by a cue-induced cocaine-seeking task to model relapse behavior. Microbiome depletion did not affect cocaine acquisition on an fixed-ratio 1 schedule. However, microbiome-depleted rats exhibited significantly enhanced motivation for low dose cocaine on a within-session threshold task. Similarly, microbiome depletion increased cue-induced cocaine-seeking following prolonged abstinence and altered transcriptional regulation in the nucleus accumbens. In the absence of a normal microbiome, repletion of bacterially-derived SCFA metabolites reversed the behavioral and transcriptional changes associated with microbiome depletion. These findings suggest that gut bacteria, via their metabolites, are key regulators of drug-seeking behaviors, positioning the microbiome as a potential translational research target.
(© 2023. The Author(s), under exclusive licence to American College of Neuropsychopharmacology.)
References: Substance Abuse and Mental Health Services Administration. Facing Addiction in America: The Surgeon General’s Report on Alcohol, Drugs, and Health. in Facing Addiction in America: The Surgeon General’s Report on Alcohol, Drugs, and Health (ed. U.S. Department of Health and Human Services (HHS), O. of the S. G.) chap. 6 (HHS, 2016). https://www.ncbi.nlm.nih.gov/books/NBK424857/pdf/Bookshelf_NBK424857.pd .
Mews P, Calipari ES. Cross-talk between the epigenome and neural circuits in drug addiction. Prog Brain Res. 2017;235:19–63.
Walker DM, Nestler EJ. Neuroepigenetics and addiction. Handb Clin Neurol. 2018;148:747–65. (PMID: 29478612586835110.1016/B978-0-444-64076-5.00048-X)
Hofford RS, Russo SJ, Kiraly DD. Neuroimmune mechanisms of psychostimulant and opioid use disorders. Eur J Neurosci. 2018. https://doi.org/10.1111/ejn.14143 .
Lucerne KE, Kiraly DD. The role of gut-immune-brain signaling in substance use disorders. Int Rev Neurobiol. 2020. https://doi.org/10.1016/bs.irn.2020.09.005 .
Dinan TG, Cryan JF. Microbes Immunity and Behavior: Psychoneuroimmunology Meets the Microbiome. Neuropsychopharmacology. 2017;42:178–92.
Dinan TG, Cryan JF. Brain-Gut-Microbiota Axis and Mental Health. https://doi.org/10.1097/PSY.0000000000000519 .
Vuong HE, Hsiao EY. Emerging Roles for the Gut Microbiome in Autism Spectrum Disorder. Biol Psychiat. 2017;81:411–23.
Hsiao EY, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell. 2013;155:1451–63. (PMID: 24315484389739410.1016/j.cell.2013.11.024)
Meckel KR, Kiraly DD. A potential role for the gut microbiome in substance use disorders. Psychopharmacology. 2019;236:1513–30. (PMID: 30982128659948210.1007/s00213-019-05232-0)
Kiraly DD, et al. Alterations of the host microbiome affect behavioral responses to cocaine. Sci Rep. 2016;6:1–12. (PMID: 10.1038/srep35455)
Lach G, Schellekens H, Dinan TG, Cryan JF. Anxiety, Depression, and the Microbiome: A Role for Gut Peptides. Neurotherapeutics. 2018;15:36–59.
De Palma G, et al. Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nat Commun. 2015;6:7735. (PMID: 2621867710.1038/ncomms8735)
Savignac HM, Tramullas M, Kiely B, Dinan TG, Cryan JF. Bifidobacteria modulate cognitive processes in an anxious mouse strain. Behav Brain Res. 2015;287:59–72.
Lucerne KE, Osman A, Meckel KR, Kiraly DD. Contributions of neuroimmune and gut-brain signaling to vulnerability of developing substance use disorders. Neuropharmacology. 2021;192:108598. (PMID: 33965398822093410.1016/j.neuropharm.2021.108598)
Hofford RS, et al. Alterations in microbiome composition and metabolic byproducts drive behavioral and transcriptional responses to morphine. Neuropsychopharmacology. 2021. https://doi.org/10.1038/s41386-021-01043-0 .
Hofford RS, et al. Changes in gut microbiome composition drive fentanyl intake and striatal proteomic changes. Preprint at 2022. https://doi.org/10.1101/2022.11.30.518531 .
García-Cabrerizo R, Barros-Santos T, Campos D, Cryan JF. The gut microbiota alone and in combination with a social stimulus regulates cocaine reward in the mouse. Brain Behav Immun. 2023;107:286–91. (PMID: 3634196610.1016/j.bbi.2022.10.020)
Cuesta S, Burdisso P, Segev A, Kourrich S, Sperandio V. Gut colonization by Proteobacteria alters host metabolism and modulates cocaine neurobehavioral responses. Cell Host Microbe. 2022;30:1615–29.e5. (PMID: 36323315966925110.1016/j.chom.2022.09.014)
Wang F, et al. Morphine induces changes in the gut microbiome and metabolome in a morphine dependence model. Sci Rep. 2018;8:3596. (PMID: 29483538582765710.1038/s41598-018-21915-8)
Zhang L, et al. Morphine tolerance is attenuated in germfree mice and reversed by probiotics, implicating the role of gut microbiome. Proc Natl Acad Sci USA. 2019;116:13523–32. (PMID: 31209039661314110.1073/pnas.1901182116)
O’mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behavioural Brain Res. 2015;277:32–48. (PMID: 10.1016/j.bbr.2014.07.027)
Visconti A, et al. Interplay between the human gut microbiome and host metabolism. Nat Commun. 2019;10:1–10. (PMID: 10.1038/s41467-019-12476-z)
Vojinovic D, et al. Relationship between gut microbiota and circulating metabolites in population-based cohorts. Nat Commun. 2019;10:1–7. (PMID: 10.1038/s41467-019-13721-1)
Vuong HE, et al. The maternal microbiome modulates fetal neurodevelopment in mice. Nature. 2020;586:281–6. (PMID: 32968276755419710.1038/s41586-020-2745-3)
Sun J, Chang EB. Exploring gut microbes in human health and disease: Pushing the envelope. Genes Dis. 2014;1:132–9. (PMID: 25642449431000810.1016/j.gendis.2014.08.001)
Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites. Cell. 2016;165:1332–45. (PMID: 2725914710.1016/j.cell.2016.05.041)
Sun J, et al. Antidepressant-like effects of sodium butyrate and its possible mechanisms of action in mice exposed to chronic unpredictable mild stress. Neurosci Lett. 2016;618:159–66. (PMID: 2695723010.1016/j.neulet.2016.03.003)
Erny D, et al. Microbiota-derived acetate enables the metabolic fitness of the brain innate immune system during health and disease. Cell Metab. 2021;33:2260–76.e7. (PMID: 3473165610.1016/j.cmet.2021.10.010)
Erny D, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci. 2015;18:965–77. (PMID: 26030851552886310.1038/nn.4030)
Thion MS, et al. Microbiome Influences Prenatal and Adult Microglia in a Sex-Specific Manner. Cell. 2018;172:500–16.e16. (PMID: 29275859578650310.1016/j.cell.2017.11.042)
Kang M, et al. The effect of gut microbiome on tolerance to morphine mediated antinociception in mice. Sci Rep. 2017;7:1–17.
Lee K, et al. The gut microbiota mediates reward and sensory responses associated with regimen-selective morphine dependence. Neuropsychopharmacology. 2018;1. https://doi.org/10.1038/s41386-018-0211-9 .
Li X, Venniro M, Shaham Y. Translational Research on Incubation of Cocaine Craving. JAMA Psychiat. 2016;73:1115–6. (PMID: 10.1001/jamapsychiatry.2016.2110)
Dong Y, Taylor JR, Wolf ME, Shaham Y. Circuit and Synaptic Plasticity Mechanisms of Drug Relapse. J Neurosci. 2017;37:10867–76. (PMID: 29118216567801910.1523/JNEUROSCI.1821-17.2017)
Lu L, Grimm JW, Dempsey J, Shaham Y. Cocaine seeking over extended withdrawal periods in rats: different time courses of responding induced by cocaine cues versus cocaine priming over the first 6 months. Psychopharmacology. 2004;176:101–8. (PMID: 1507171910.1007/s00213-004-1860-4)
Pickens CL, et al. Neurobiology of the incubation of drug craving. Trends Neurosci. 2011;34:411–20. (PMID: 21764143315266610.1016/j.tins.2011.06.001)
Parvaz MA, Moeller SJ, Goldstein RZ. Incubation of Cue-Induced Craving in Adults Addicted to Cocaine Measured by Electroencephalography. JAMA Psychiat. 2016;73:1127–34. (PMID: 10.1001/jamapsychiatry.2016.2181)
Bercik P, et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology. 2011;141:599–609. (PMID: 2168307710.1053/j.gastro.2011.04.052)
Smith PM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341:569–73. (PMID: 2382889110.1126/science.1241165)
Braniste V, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med. 2014;6:263ra158. (PMID: 25411471439684810.1126/scitranslmed.3009759)
Calipari ES, et al. Granulocyte-colony stimulating factor controls neural and behavioral plasticity in response to cocaine. Nat Commun. 2018;9:9. (PMID: 29339724577042910.1038/s41467-017-01881-x)
Siciliano CA, Jones SR. Cocaine potency at the dopamine transporter tracks discrete motivational states during cocaine self-administration. Neuropsychopharmacology. 2017;42:1893–904. (PMID: 28139678552078110.1038/npp.2017.24)
Oleson EB, Roberts DCS. Behavioral economic assessment of price and cocaine consumption following self-administration histories that produce escalation of either final ratios or intake. Neuropsychopharmacology. 2009;34:796–804. (PMID: 1897192710.1038/npp.2008.195)
Zito KA, Vickers G, Roberts DCS. Disruption of cocaine and heroin self-administration following kainic acid lesions of the nucleus accumbens. Pharmacol, Biochem Behav. 1985;23:1029–36. (PMID: 393605810.1016/0091-3057(85)90110-8)
Salgado S, Kaplitt MG. The nucleus accumbens: A comprehensive review. Stereotact Funct Neurosurg. 2015;93:75–93.
Chu C, et al. The microbiota regulate neuronal function and fear extinction learning. Nature. 2019;574:543–8. (PMID: 31645720681875310.1038/s41586-019-1644-y)
Hoban AE, et al. The microbiome regulates amygdala-dependent fear recall. Mol Psychiat. 2018;23:1134–44. (PMID: 10.1038/mp.2017.100)
Lex A, Gehlenborg N, Strobelt H, Vuillemot R, Pfister H. UpSet: Visualization of Intersecting Sets. IEEE Trans Vis Comput Graph. 2014;20:1983–92. (PMID: 26356912472099310.1109/TVCG.2014.2346248)
Sens JP, Hofford RS, Kiraly DD. Effect of germ-free status on transcriptional profiles in the nucleus accumbens and transcriptomic response to chronic morphine. Mol Cell Neurosci. 2023;103874. https://doi.org/10.1016/j.mcn.2023.103874 .
Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinforma. 2008;9:559. (PMID: 10.1186/1471-2105-9-559)
Lee K, et al. The gut microbiota mediates reward and sensory responses associated with regimen-selective morphine dependence. Neuropsychopharmacology. 2018;43:2606–14. (PMID: 30258112622450610.1038/s41386-018-0211-9)
Hoban AE, et al. Regulation of prefrontal cortex myelination by the microbiota. Transl Psychiatry. 2016;6:e774. (PMID: 27045844487240010.1038/tp.2016.42)
Stilling RM, et al. Microbes & neurodevelopment-Absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala. Brain Behav Immun 2015;50:209–20. (PMID: 2618408310.1016/j.bbi.2015.07.009)
Simpson S, et al. Depletion of the Microbiome Alters the Recruitment of Neuronal Ensembles of Oxycodone Intoxication and Withdrawal. eNeuro. 2020;7:ENEURO.0312-19.2020.
Dalile B, Van Oudenhove L, Vervliet B, Verbeke K. The role of short-chain fatty acids in microbiota-gut-brain communication. Nat Rev Gastroenterol Hepatol. 2019;16:461–78. (PMID: 3112335510.1038/s41575-019-0157-3)
Frost G, et al. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun. 2014;5:3611. (PMID: 2478130610.1038/ncomms4611)
Waldecker M, Kautenburger T, Daumann H, Busch C, Schrenk D. Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon. J Nutr Biochem. 2008;19:587–93. (PMID: 1806143110.1016/j.jnutbio.2007.08.002)
Mews P, et al. Alcohol metabolism contributes to brain histone acetylation. Nature. 2019;574:717–21. (PMID: 31645761690708110.1038/s41586-019-1700-7)
Mews P, et al. Acetyl-CoA synthetase regulates histone acetylation and hippocampal memory. Nature. 2017;546:381–6. (PMID: 28562591550551410.1038/nature22405)
Macfabe DF. Short-chain fatty acid fermentation products of the gut microbiome: implications in autism spectrum disorders. Microb Ecol Health Dis. 2012;23.
MacFabe DF, et al. Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders. Behav Brain Res. 2007;176:149–69. (PMID: 1695052410.1016/j.bbr.2006.07.025)
Nankova BB, Agarwal R, MacFabe DF, La Gamma EF. Enteric bacterial metabolites propionic and butyric acid modulate gene expression, including CREB-dependent catecholaminergic neurotransmission, in PC12 cells-possible relevance to autism spectrum disorders. PLoS One. 2014;9:e103740. (PMID: 25170769414935910.1371/journal.pone.0103740)
Rabelo FLA, et al. Inhibition of ERK1/2 and CREB phosphorylation by caspase-dependent mechanism enhances apoptosis in a fibrosarcoma cell line treated with butyrate. Biochem Biophys Res Commun. 2003;303:968–72. (PMID: 1267050610.1016/S0006-291X(03)00454-6)
Mally P, et al. Stereospecific regulation of tyrosine hydroxylase and proenkephalin genes by short-chain fatty acids in rat PC12 cells. Pediatr Res. 2004;55:847–54. (PMID: 1473935710.1203/01.PDR.0000119365.21770.45)
Parab S, Nankova BB, La Gamma EF. Differential regulation of the tyrosine hydroxylase and enkephalin neuropeptide transmitter genes in rat PC12 cells by short chain fatty acids: concentration-dependent effects on transcription and RNA stability. Brain Res. 2007;1132:42–50. (PMID: 1717427910.1016/j.brainres.2006.11.013)
Shah P, Nankova BB, Parab S, La Gamma EF. Short chain fatty acids induce TH gene expression via ERK-dependent phosphorylation of CREB protein. Brain Res. 2006;1107:13–23. (PMID: 1685438710.1016/j.brainres.2006.05.097)
معلومات مُعتمدة: K01 DA050906 United States DA NIDA NIH HHS; T32 MH065215 United States MH NIMH NIH HHS; F99 NS124187 United States NS NINDS NIH HHS; DP1 DA051551 United States DA NIDA NIH HHS; R01 DA056592 United States DA NIDA NIH HHS
المشرفين على المادة: I5Y540LHVR (Cocaine)
تواريخ الأحداث: Date Created: 20230801 Date Completed: 20231218 Latest Revision: 20240501
رمز التحديث: 20240501
مُعرف محوري في PubMed: PMC10724273
DOI: 10.1038/s41386-023-01661-w
PMID: 37528220
قاعدة البيانات: MEDLINE
الوصف
تدمد:1740-634X
DOI:10.1038/s41386-023-01661-w