Alterations of the host microbiome affect behavioral responses to cocaine

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Kiraly, Drew D ^a   Walker, Deena M ^a   Calipari, Erin S ^a   Labonte, Benoit ^a   Issler, Orna ^a   Pena, Catherine J ^a   Ribeiro, Efrain A ^a   Russo, Scott J ^a   Nestler, Eric J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; COCAINE; CORTICOSTERONE; DOPAMINE; GLUTAMIC ACID; TRANSCRIPTOME;

ANIMAL; ANIMAL BEHAVIOR; BACTERIUM; BLOOD; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; INTESTINE FLORA; MALE; METABOLISM; MICROFLORA; MOUSE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BEHAVIOR, ANIMAL; COCAINE; CORTICOSTERONE; DOPAMINE; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLUTAMIC ACID; MALE; MICE; MICROBIOTA; TRANSCRIPTOME;

EID: 84992345480     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep35455     Document Type: Article

References (62)

1. Cryan, J. F. and Dinan, T. G. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13, 701-712 (2012).
2. Collins, S. M., Surette, M. and Bercik, P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 10, 735-742 (2012).
3. Diaz Heijtz, R. et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 108, 3047-3052 (2011).
4. Bercik, P. et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141, 599-609, 609.e1 (2011).
5. Zheng, P. et al. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the hosts metabolism. Mol Psychiatry 21, 786-796 (2016).
6. Wong, M. L. et al. Inflammasome signaling affects anxiety- and depressive-like behavior and gut microbiome composition. Mol Psychiatry 21, 797-805 (2016).
7. Clarke, G. et al. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 18, 666-673 (2013).
8. Gacias, M. et al. Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior. elife 5, (2016).
9. Hsiao, E. Y. et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155, 1451-1463 (2013).
10. Tillisch, K. et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144, 1394-1401, 1401.e1 (2013).
11. Akkasheh, G. et al. Clinical and metabolic response to probiotic administration in patients with major depressive disorder: A randomized, double-blind, placebo-controlled trial. Nutrition 32, 315-320 (2016).
12. Murray, C. J. et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. The Lancet 380, 2197-2223 (2012).
13. Volpe, G. E. et al. Associations of cocaine use and HIV infection with the intestinal microbiota, microbial translocation, and inflammation. J Stud Alcohol Drugs 75, 347-357 (2014).
14. Compton, W. M., Conway, K. P., Stinson, F. S. and Grant, B. F. Changes in the prevalence of major depression and comorbid substance use disorders in the United States between 1991-1992 and 2001-2002. Am J Psychiatry 163, 2141-2147 (2006).
15. Peña, C. J., Bagot, R. C., Labonté, B. and Nestler, E. J. Epigenetic signaling in psychiatric disorders. J Mol Biol 426, 3389-3412 (2014).
16. Cohen, A. et al. Virus-mediated shRNA knockdown of prodynorphin in the rat nucleus accumbens attenuates depression-like behavior and cocaine locomotor sensitization. PLoS ONE 9, e97216 (2014).
17. De Palma, G. et al. Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nat Commun 6, 7735 (2015).
18. Desbonnet, L. et al. Gut microbiota depletion from early adolescence in mice: Implications for brain and behaviour. Brain Behav Immun 48, 165-173 (2015).
19. Schéle, E. et al. The gut microbiota reduces leptin sensitivity and the expression of the obesity-suppressing neuropeptides proglucagon (Gcg) and brain-derived neurotrophic factor (Bdnf) in the central nervous system. Endocrinology 154, 3643-3651 (2013).
20. Li, X. and Wolf, M. E. Multiple faces of BDNF in cocaine addiction. Behav Brain Res 279, 240-254 (2015).
21. Fernandes, B. S. et al. Peripheral brain-derived neurotrophic factor (BDNF) as a biomarker in bipolar disorder: a meta-analysis of 52 studies. BMC Med 13, 289 (2015).
22. Crumeyrolle-Arias, M. et al. Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats. Psychoneuroendocrinology 42, 207-217 (2014).
23. Reikvam, D. H. et al. Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression. (2011).
24. Erny, D. et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 18, 965-977 (2015).
25. De Jong, I. E., Steenbergen, P. J. and de Kloet, E. R. Behavioral sensitization to cocaine: cooperation between glucocorticoids and epinephrine. Psychopharmacology (Berl) 204, 693-703 (2009).
26. Neufeld, K. M., Kang, N., Bienenstock, J. and Foster, J. A. Reduced anxiety-like behavior and central neurochemical change in germfree mice. Neurogastroenterol Motil 23, 255-264, e119 (2011).
27. Fröhlich, E. E. et al. Cognitive impairment by antibiotic-induced gut dysbiosis: Analysis of gut microbiota-brain communication. Brain Behav Immun doi: 10.1016/j.bbi.2016.02.020 (2016).
28. Zhang, Y., Limaye, P. B., Renaud, H. J. and Klaassen, C. D. Effect of various antibiotics on modulation of intestinal microbiota and bile acid profile in mice. Toxicol Appl Pharmacol 277, 138-145 (2014).
29. Dudley, M. N. et al. Oral bacitracin vs vancomycin therapy for Clostridium difficile-induced diarrhea. A randomized double-blind trial. Arch Intern Med 146, 1101-1104 (1986).
30. Koh, A., De Vadder, F., Kovatcheva-Datchary, P. and Bäckhed, F. From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites. Cell 165, 1332-1345 (2016).
31. Smith, P. M. et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341, 569-573 (2013).
32. Braniste, V. et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med 6, 263ra158 (2014).
33. Bravo, J. A. et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 108, 16050-16055 (2011).
34. Leclercq, S. et al. Role of intestinal permeability and inflammation in the biological and behavioral control of alcohol-dependent subjects. Brain Behav Immun 26, 911-918 (2012).
35. Leclercq, S. et al. Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci USA 111, E4485-E4493 (2014).
36. Trantham-Davidson, H., LaLumiere, R. T., Reissner, K. J., Kalivas, P. W. and Knackstedt, L. A. Ceftriaxone normalizes nucleus accumbens synaptic transmission, glutamate transport, and export following cocaine self-administration and extinction training. J Neurosci 32, 12406-12410 (2012).
37. Sari, Y., Smith, K. D., Ali, P. K. and Rebec, G. V. Upregulation of GLT1 attenuates cue-induced reinstatement of cocaine-seeking behavior in rats. J Neurosci 29, 9239-9243 (2009).
38. Knackstedt, L. A., Melendez, R. I. and Kalivas, P. W. Ceftriaxone restores glutamate homeostasis and prevents relapse to cocaine seeking. Biol Psychiatry 67, 81-84 (2010).
39. Rothstein, J. D. et al. Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 433, 73-77 (2005).
40. Branchi, I. et al. Early developmental exposure to BDE 99 or Aroclor 1254 affects neurobehavioural profile: interference from the administration route. Neurotoxicology 26, 183-192 (2005).
41. Faith, J. J., McNulty, N. P., Rey, F. E. and Gordon, J. I. Predicting a human gut microbiotas response to diet in gnotobiotic mice. Science 333, 101-104 (2011).
42. Mortha, A. et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343, 1249288 (2014).
43. Zhang, D. et al. Neutrophil ageing is regulated by the microbiome. Nature 525, 528-532 (2015).
44. Hoban, A. E. et al. Regulation of prefrontal cortex myelination by the microbiota. Translational psychiatry 6, e774 (2016).
45. Kennedy, P. J. et al. Class I HDAC inhibition blocks cocaine-induced plasticity by targeted changes in histone methylation. Nat Neurosci 16, 434-440 (2013).
46. Heller, E. A. et al. Targeted Epigenetic Remodeling of the Cdk5 Gene in Nucleus Accumbens Regulates Cocaine- and Stress-Evoked Behavior. J Neurosci 36, 4690-4697 (2016).
47. Romieu, P. et al. Histone deacetylase inhibitors decrease cocaine but not sucrose self-administration in rats. J Neurosci 28, 9342-9348 (2008).
48. Kim, W. Y., Kim, S. and Kim, J. H. Chronic microinjection of valproic acid into the nucleus accumbens attenuates amphetamineinduced locomotor activity. Neurosci Lett 432, 54-57 (2008).
49. Russo, S. J. et al. Nuclear factor kappa B signaling regulates neuronal morphology and cocaine reward. J Neurosci 29, 3529-3537 (2009).
50. Graham, D. L. et al. Tropomyosin-related kinase B in the mesolimbic dopamine system: region-specific effects on cocaine reward. Biol Psychiatry 65, 696-701 (2009).
51. Graham, D. L. et al. Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat Neurosci 10, 1029-1037 (2007).
52. Kelz, M. B. et al. Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401, 272-276 (1999).
53. Boudreau, A. C. and Wolf, M. E. Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J Neurosci 25, 9144-9151 (2005).
54. Wolf, M. E. Regulation of AMPA receptor trafficking in the nucleus accumbens by dopamine and cocaine. Neurotox Res 18, 393-409 (2010).
55. Hyman, S. E., Malenka, R. C. and Nestler, E. J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29, 565-598 (2006).
56. Lobo, M. K. et al. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330, 385-390 (2010).
57. Hikida, T., Kimura, K., Wada, N., Funabiki, K. and Nakanishi, S. Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron 66, 896-907 (2010).
58. Cates, H. M. et al. Threonine 149 phosphorylation enhances FosB transcriptional activity to control psychomotor responses to cocaine. J Neurosci 34, 11461-11469 (2014).
59. Dietz, D. M. et al. Rac1 is essential in cocaine-induced structural plasticity of nucleus accumbens neurons. Nat Neurosci 15, 891-896 (2012).
60. Bagot, R. C. et al. Ventral hippocampal afferents to the nucleus accumbens regulate susceptibility to depression. Nat Commun 6, 7062 (2015).
61. Maze, I. et al. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327, 213-216 (2010).
62. Cahenzli, J., Köller, Y., Wyss, M., Geuking, M. B. and McCoy, K. D. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe 14, 559-570 (2013).