Corrigendum to “Behavioural and neurochemical consequences of chronic gut microbiota depletion during adulthood in the rat” [Neuroscience 339 (2016) 463–477] (S0306452216305127)(10.1016/j.neuroscience.2016.10.003);Behavioural and neurochemical consequences of chronic gut microbiota depletion during adulthood in the rat

Neuroscience

Volumn 339, Issue , 2016, Pages 463-477

  Hoban, A E ^a,b   Moloney, R D ^a   Golubeva, A V ^a   McVey Neufeld, K A ^a   O'Sullivan, O ^c   Patterson, E ^c   Stanton, C ^c   Dinan, T G ^a,b   Clarke, G ^a,b   Cryan, J F ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c TEAGASC FOOD RESEARCH CENTRE   (Ireland)

Author keywords

antibiotics; brain monoamines; cognition; depressive like behaviours; gut microbiota; visceral sensitivity

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; BIOLOGICAL MARKER; BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; DOPAMINE; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; NORADRENALIN; SEROTONIN; TRYPTOPHAN; ANTIINFECTIVE AGENT; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR RECEPTOR;

ADULT; ADULTHOOD; AMYGDALA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ANXIETY; ARTICLE; BEHAVIOR; CONTROLLED STUDY; CORPUS STRIATUM; DEPRESSION; FORCED SWIM TEST; GENE EXPRESSION; HIPPOCAMPUS; HOST; HOT PLATE TEST; HYPOTHALAMUS; INTESTINE FLORA; MALE; MEMORY DISORDER; MICROBIAL DIVERSITY; MORRIS WATER MAZE TEST; NEUROCHEMISTRY; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PHYSICAL SENSITIVITY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SPATIAL LEARNING; SPATIAL MEMORY; SPRAGUE DAWLEY RAT; VISCERAL SENSITIVITY; ANIMAL; BLOOD; BRAIN; CECUM; DRUG EFFECTS; FECES; GENE EXPRESSION REGULATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PSYCHOLOGY; VISCERAL PAIN;

ANIMALS; ANTI-BACTERIAL AGENTS; ANXIETY; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CECUM; CORTICOSTERONE; DEPRESSION; FECES; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION REGULATION; MALE; MEMORY DISORDERS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER; SEROTONIN; VISCERAL PAIN;

EID: 84994027713     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2017.01.008     Document Type: Erratum

References (74)

1. Allen, K.M., et al. The effect of adolescent testosterone on hippocampal BDNF and TrkB mRNA expression: relationship with cell proliferation. BMC Neurosci, 16, 2015, 4.
2. Arentsen, T., Raith, H., Qian, Y., Forssberg, H., Diaz Heijtz, R., Host microbiota modulates development of social preference in mice. Microb Ecol Health Dis, 26, 2015, 29719.
3. Arrieta, M.-C., Walter, J., Finlay, B.B., Human microbiota-associated mice: a model with challenges. Cell Host Microbe 19 (2016), 575–578.
4. Bercik, P., Verdu, E.F., Foster, J.A., Macri, J., Potter, M., Huang, X., Malinowski, P., Jackson, W., Blennerhassett, P., Neufeld, K.A., Lu, J., Khan, W.I., Corthesy-Theulaz, I., Cherbut, C., Bergonzelli, G.E., Collins, S.M., Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice. Gastroenterology, 139(2102–2112), 2010, e1.
5. Bercik P, Denou E, Collins J, Jackson W, Lu J, Jury J, Deng Y, Blennerhassett P, Macri J, McCoy KD, Verdu EF, Collins SM (2011) The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141:599–609, 609.e1–e3.
6. Bercik, P., Park, A.J., Sinclair, D., Khoshdel, A., Lu, J., Huang, X., Deng, Y., Blennerhassett, P.A., Fahnestock, M., Moine, D., Berger, B., Huizinga, J.D., Kunze, W., McLean, P.G., Bergonzelli, G.E., Collins, S.M., Verdu, E.F., The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil 23 (2011), 1132–1139.
7. Bevins, R.A., Besheer, J., Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study “recognition memory”. Nat Protoc 1 (2006), 1306–1311.
8. Bolnick, D.I., Snowberg, L.K., Hirsch, P.E., Lauber, C.L., Org, E., Parks, B., Lusis, A.J., Knight, R., Caporaso, J.G., Svanbäck, R., Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat Commun, 5, 2014.
9. Borre, Y.E., O'Keeffe, G.W., Clarke, G., Stanton, C., Dinan, T.G., Cryan, J.F., Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med 20 (2014), 509–518.
10. Bravo, J.A., Forsythe, P., Chew, M.V., Escaravage, E., Savignac, H.M., Dinan, T.G., Bienenstock, J., Cryan, J.F., Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci 108 (2011), 16050–16055.
11. Buffington, S.A., Di Prisco, G.V., Auchtung, T.A., Ajami, N.J., Petrosino, J.F., Costa-Mattioli, M., Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 165 (2016), 1762–1775.
12. Caporaso, J.G., et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7 (2010), 335–336.
13. Cho, I., Yamanishi, S., Cox, L., Methé, B.A., Zavadil, J., Li, K., Gao, Z., Mahana, D., Raju, K., Teitler, I., Li, H., Alekseyenko, A.V., Blaser, M.J., Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488 (2012), 621–626.
14. Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R.D., Shanahan, F., Dinan, T.G., Cryan, J.F., The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 18 (2012), 666–673.
15. Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R.D., Shanahan, F., Dinan, T.G., Cryan, J.F., The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 18 (2013), 666–673.
16. Clemente, J.C., Ursell, L.K., Parfrey, L.W., Knight, R., The impact of the gut microbiota on human health: an integrative view. Cell 148 (2012), 1258–1270.
17. Crumeyrolle-Arias, M., Jaglin, M., Bruneau, A., Vancassel, S., Cardona, A., Daugé, V., Naudon, L., Rabot, S., Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats. Psychoneuroendocrinology 42 (2014), 207–217.
18. Cryan, J.F., Dinan, T.G., Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nature Rev Neuros 13:10 (2012), 701–712.
19. De Palma, G., Collins, S.M., Bercik, P., Verdu, E.F., The microbiota-gut-brain axis in gastrointestinal disorders: stressed bugs, stressed brain or both?. J. Physiol. 592 (2014), 2989–2997.
20. Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J.F., Dinan, T.G., Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 170 (2010), 1179–1188.
21. Desbonnet, L., Clarke, G., Shanahan, F., Dinan, T.G., Cryan, J.F., Microbiota is essential for social development in the mouse. Mol Psychiatry 19 (2014), 146–148.
22. Desbonnet, L., Clarke, G., Traplin, A., O'Sullivan, O., Crispie, F., Moloney, R.D., Cotter, P.D., Dinan, T.G., Cryan, J.F., Gut microbiota depletion from early adolescence in mice: implications for brain and behaviour. Brain Behav Immun 48 (2015), 165–173.
23. Distrutti, E., Monaldi, L., Ricci, P., Fiorucci, S., Gut microbiota role in irritable bowel syndrome: new therapeutic strategies. World J Gastroenterol 22 (2016), 2219–2241.
24. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 (2010), 2460–2461.
25. Foster, J.A., McVey Neufeld, K.-A., Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36 (2013), 305–312.
26. Fröhlich, E.E., Farzi, A., Mayerhofer, R., Reichmann, F., Jačan, A., Wagner, B., Zinser, E., Bordag, N., Magnes, C., Fröhlich, E., Kashofer, K., Gorkiewicz, G., Holzer, P., Cognitive impairment by antibiotic-induced gut dysbiosis: analysis of gut microbiota-brain communication. Brain Behav Immun, 2016.
27. Gacias, M., Gaspari, S., Mae-Santos, P., Tamburini, S., Andrade, M., Zang, F., Shen, N., Tolstikov, V., Kiebish, M.A., Dupree, J.L., Zachariou, V., Clemente, J.C., Casaccia, P., Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior. Elife, 5, 2016, e13442.
28. Gareau, M.G., Wine, E., Rodrigues, D.M., Cho, J.H., Whary, M.T., Philpott, D.J., MacQueen, G., Sherman, P.M., Bacterial infection causes stress-induced memory dysfunction in mice. Gut, 2010.
29. Goehler, L.E., Lyte, M., Gaykema, R.P.A., Infection-induced viscerosensory signals from the gut enhance anxiety: implications for psychoneuroimmunology. Brain Behav Immun 21 (2007), 721–726.
30. Gosselin, R.-D., O'Connor, R.M., Tramullas, M., Julio-Pieper, M., Dinan, T.G., Cryan, J.F., Riluzole normalizes early-life stress-induced visceral hypersensitivity in rats: role of spinal glutamate reuptake mechanisms. Gastroenterology 138 (2010), 2418–2425.
31. Grubbs, F.E., Sample criteria for testing outlying observations. Ann Math Stat 21 (1950), 27–58.
32. Heijtz, R.D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M.L., Forssberg, H., Pettersson, S., Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci 108 (2011), 3047–3052.
33. Heimesaat, M.M., Kupz, A., Fischer, A., Nies, D.H., Grass, G., Göbel, U.B., Bereswill, S., Colonization resistance against genetically modified Escherichia coli K12 (W3110) strains is abrogated following broad-spectrum antibiotic treatment and acute ileitis. Eur J Microbiol Immunol (Bp) 3 (2013), 222–228.
34. Hoban, A.E., Stilling, R.M., Ryan, F.J., Shanahan, F., Dinan, T.G., Claesson, M.J., Clarke, G., Cryan, J.F., Regulation of prefrontal cortex myelination by the microbiota. Transl Psychiatry, 6, 2016, e774.
35. Hsiao, E.Y., McBride, S.W., Hsien, S., Sharon, G., Hyde, E.R., McCue, T., Codelli, J.A., Chow, J., Reisman, S.E., Petrosino, J.F., Patterson, P.H., Mazmanian, S.K., Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155 (2013), 1451–1463.
36. Hsiao, E.Y., McBride, S.W., Hsien, S., Sharon, G., Hyde, E.R., McCue, T., Codelli, J.A., Chow, J., Reisman, S.E., Petrosino, J.F., Patterson, P.H., Mazmanian, S.K., Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155 (2013), 1451–1463.
37. Karlsten, R., et al. Effects of intrathecal injection of the adenosine receptor agonists R-phenylisopropyl-adenosine and N-ethylcarboxamide-adenosine on nociception and motor function in the rat. Anesth Analg 71:1 (1990), 60–64.
38. Kelly, J.R., et al. Transferring the blues: depression-associated gut microbiota induces neurobehavioural changes in the rat. J Psychiatr Res, 2016, 94–124.
39. Kundakovic, M., Lim, S., Gudsnuk, K., Champagne, F.A., Sex-specific and strain-dependent effects of early life adversity on behavioral and epigenetic outcomes. Front Psychiatry, 4, 2013, 78.
40. Lee, J.-H., Wood, T.K., Lee, J., Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol 23 (2015), 707–718.
41. Luczynski, P., McVey Neufeld, K.-A., Seira Oriach, C., Clarke, G., Dinan, T.G., Cryan, J.F., Growing up in a bubble: using germ-free animals to assess the influence of the gut microbiota on brain and behaviour. Int J Neuropsychopharmacol, 2016, pyw020.
42. Lundberg, R., Toft, M., August, B., Antibiotic-treated versus germ-free rodents for microbiota transplantation studies. Gut, 2016.
43. Lyte, M., Li, W., Opitz, N., Gaykema, R.P.A., Goehler, L.E., Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium. Physiol Behav 89 (2006), 350–357.
44. Magoč, T., Salzberg, S.L., FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27 (2011), 2957–2963.
45. Markle, J.G.M., et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science, 80, 2013, 339 339:e111–e111.
46. Mayer, E.A., Gut feelings: the emerging biology of gut–brain communication. Nature Rev Neuros 12:8 (2011), 453–466.
47. Mayer, E.A., Padua, D., Tillisch, K., Altered brain-gut axis in autism: comorbidity or causative mechanisms?. BioEssays 36 (2014), 933–939.
48. McVey Neufeld, K.-A., Luczynski, P., Dinan, T.G., Cryan, J.F., Reframing the teenage wasteland: adolescent microbiota-gut-brain axis. Can J Psychiatry 61 (2016), 214–221.
49. Messaoudi, M., Lalonde, R., Violle, N., Javelot, H., Desor, D., Nejdi, A., Bisson, J.-F., Rougeot, C., Pichelin, M., Cazaubiel, M., Cazaubiel, J.-M., Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 105 (2010), 755–764.
50. Möhle, L., Mattei, D., Heimesaat, M.M., Bereswill, S., Fischer, A., Alutis, M., French, T., Hambardzumyan, D., Matzinger, P., Dunay, I.R., Wolf, S.A., Ly6Chi monocytes provide a link between antibiotic-induced changes in gut microbiota and adult hippocampal neurogenesis. Cell Rep 15 (2016), 1945–1956.
51. Moloney, R.D., Dinan, T.G., Cryan, J.F., Strain-dependent variations in visceral sensitivity: relationship to stress, anxiety and spinal glutamate transporter expression. Genes Brain Behav 14 (2015), 319–329.
52. Moloney, R.D., O'Mahony, S.M., Dinan, T.G., Cryan, J.F., Stress-induced visceral pain: toward animal models of irritable-bowel syndrome and associated comorbidities. Front Psychiatry, 6, 2015, 15.
53. Neufeld, K.M., Kang, N., Bienenstock, J., Foster, J.A., Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil, 23, 2011 255–e119.
54. O'Mahony, S.M., Marchesi, J.R., Scully, P., Codling, C., Ceolho, A.-M., Quigley, E.M.M., Cryan, J.F., Dinan, T.G., Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65 (2009), 263–267.
55. O'Mahony, S.M., Clarke, G., Borre, Y.E., Dinan, T.G., Cryan, J.F., Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res 277 (2014), 32–48.
56. O'Mahony, S.M., Felice, V.D., Nally, K., Savignac, H.M., Claesson, M.J., Scully, P., Woznicki, J., Hyland, N.P., Shanahan, F., Quigley, E.M., Marchesi, J.R., O'Toole, P.W., Dinan, T.G., Cryan, J.F., Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats. Neuroscience 277 (2014), 885–901.
57. Purves-Tyson, T.D., Allen, K., Fung, S., Rothmond, D., Noble, P.L., Handelsman, D.J., Adolescent testosterone influences BDNF and TrkB mRNA and neurotrophin–interneuron marker relationships in mammalian frontal cortex. Schizophr Res 168 (2015), 661–670.
58. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41 (2013), D590–D596.
59. Reigstad, C.S., Salmonson, C.E., Rainey, J.F., Szurszewski, J.H., Linden, D.R., Sonnenburg, J.L., Farrugia, G., Kashyap, P.C., Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells. FASEB J 29 (2015), 1395–1403.
60. Reikvam, D.H., Erofeev, A., Sandvik, A., Grcic, V., Jahnsen, F.L., Gaustad, P., McCoy, K.D., Macpherson, A.J., Meza-Zepeda, L.A., Johansen, F.-E., Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression Heimesaat M, ed. PLoS One, 6, 2011, e17996.
61. Slattery, D.A., Cryan, J.F., Using the rat forced swim test to assess antidepressant-like activity in rodents. Nat Protoc 7 (2012), 1009–1014.
62. Staudacher, H., Whelan, K., Altered gastrointestinal microbiota in irritable bowel syndrome and its modification by diet: probiotics, prebiotics and the low FODMAP diet. Proc Nutr, 2016.
63. Stilling, R.M., Bordenstein, S.R., Dinan, T.G., Cryan, J.F., Friends with social benefits: host–microbe interactions as a driver of brain evolution and development?. Front Cell Infect Microbiol, 4, 2014, 147.
64. Stilling, R.M., Dinan, T.G., Cryan, J.F., Microbial genes, brain & behaviourm – epigenetic regulation of the gut-brain axis. Genes Brain Behav 13 (2014), 69–86.
65. Stilling, R.M., Ryan, F.J., Hoban, A.E., Shanahan, F., Clarke, G., Claesson, M.J., Dinan, T.G., Cryan, J.F., Microbes & neurodevelopment – absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala. Brain Behav Immun, 2015.
66. Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., Koga, Y., Postnatal microbial colonization programs the hypothalamic–pituitary–adrenal system for stress response in mice. J Physiol 558 (2004), 263–275.
67. Taché, Y., Corticotrophin-releasing factor 1 activation in the central amygdale and visceral hyperalgesia. Neurogastroenterol Motil 27 (2015), 1–6.
68. Vázquez-Baeza, Y., Pirrung, M., Gonzalez, A., Knight, R., EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience, 2, 2013, 16.
69. Verdú, E.F., Bercik, P., Verma-Gandhu, M., Huang, X.-X., Blennerhassett, P., Jackson, W., Mao, Y., Wang, L., Rochat, F., Collins, S.M., Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut 55 (2006), 182–190.
70. Vorhees, C.V., Williams, M.T., Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1 (2006), 848–858.
71. Williams, S.C.P., Gnotobiotics. Proc Natl Acad Sci U S A, 111, 2014, 1661.
72. Yano, J.M., Yu, K., Donaldson, G.P., Shastri, G.G., Ann, P., Ma, L., Nagler, C.R., Ismagilov, R.F., Mazmanian, S.K., Hsiao, E.Y., Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161 (2015), 264–276.
73. Zhang, Y., Limaye, P.B., Renaud, H.J., Klaassen, C.D., Effect of various antibiotics on modulation of intestinal microbiota and bile acid profile in mice. Toxicol Appl Pharmacol 277 (2014), 138–145.
74. Zheng, P., Zeng, B., Zhou, C., Liu, M., Fang, Z., Xu, X., Zeng, L., Chen, J., Fan, S., Du, X., Zhang, X., Yang, D., Yang, Y., Meng, H., Li, W., Melgiri, N.D., Licinio, J., Wei, H., Xie, P., Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host's metabolism. Mol Psychiatry 21 (2016), 786–796.