Implications of the gut microbiota in vulnerability to the social avoidance effects of chronic social defeat in male mice

Brain, Behavior, and Immunity

Volumn 66, Issue , 2017, Pages 45-55

  Szyszkowicz, Joanna Kasia ^a,c   Wong, Alex ^b   Anisman, Hymie ^a,b   Merali, Zul ^a   Audet, Marie Claude ^a,b  

^a UNIVERSITY OF OTTAWA   (Canada)

^b CARLETON UNIVERSITY   (Canada)

^c DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

Animal model; Depressive like behaviors; Gut microbiota; Microbiota gut brain axis; Pro inflammatory cytokine; Social avoidance; Social defeat; Susceptibility resilience

Indexed keywords

CORTICOSTERONE; CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; BRAIN; CECUM; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CYTOKINE PRODUCTION; DEPRESSION; DISEASE ASSOCIATION; DISEASE SEVERITY; FIRMICUTES; FLAVOBACTERIUM; GENE EXPRESSION; IL 1BETA GENE; IL 6 GENE; INTESTINE FLORA; MALE; MICROBIAL POPULATION DYNAMICS; MOUSE; NONHUMAN; PARAPEDOBACTER; PEDOBACTER; PHENOTYPE; PHYLUM; PORPHYROMONAS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SOCIAL AVOIDANCE BEHAVIOR; SOCIAL STRESS; TURICIBACTER; ANIMAL; AVOIDANCE BEHAVIOR; C57BL MOUSE; COMPLICATION; INFLAMMATION; MENTAL STRESS; METABOLISM; MICROBIOLOGY; SOCIAL BEHAVIOR;

ANIMALS; AVOIDANCE LEARNING; BRAIN; CECUM; CYTOKINES; GASTROINTESTINAL MICROBIOME; INFLAMMATION; MALE; MICE, INBRED C57BL; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 85021261151     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2017.06.009     Document Type: Article

References (70)

1. Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., Ferrier, L., et al. Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 37 (2012), 1885–1895.
2. Ait-Belgnaoui, A., Colom, A., Braniste, V., Ramalho, L., Marrot, A., Cartier, C., et al. Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice. Neurogastroenterol. Motil. 26 (2014), 510–520.
3. Allen, R.G., Lafuse, W.P., Galley, J.D., Ali, M.M., Ahmer, B.M., Bailey, M.T., The intestinal microbiota are necessary for stressor-induced enhancement of splenic macrophage microbicidal activity. Brain Behav. Immun. 26 (2012), 371–382.
4. 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.
5. Arentsen, T., Qian, Y., Gkotzis, S., Femenia, T., Wang, T., Udekwu, K., et al. The bacterial peptidoglycan-sensing molecule Pglyrp2 modulates brain development and behavior. Mol. Psychiatry 22 (2017), 257–266.
6. Audet, M.C., Mangano, E.N., Anisman, H., Behavior and pro-inflammatory cytokine variations among submissive and dominant mice engaged in aggressive encounters: moderation by corticosterone reactivity. Front. Behav. Neurosci., 4, 2010, 156.
7. Audet, M.C., Jacobson-Pick, S., Wann, B.P., Anisman, H., Social defeat promotes specific cytokine variations within the prefrontal cortex upon subsequent aggressive or endotoxin challenges. Brain Behav. Immun. 25 (2011), 1197–1205.
8. Bailey, M.T., Dowd, S.E., Galley, J.D., Hufnagle, A.R., Allen, R.G., Lyte, M., Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav. Immun. 25 (2011), 397–407.
9. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006), 864–868.
10. Bharwani, A., Mian, M.F., Foster, J.A., Surette, M.G., Bienenstock, J., Forsythe, P., Structural & functional consequences of chronic psychosocial stress on the microbiome & host. Psychoneuroendocrinology 63 (2016), 217–227.
11. Bharwani, A., Mian, M.F., Surette, M.G., Bienenstock, J., Forsythe, P., Oral treatment with Lactobacillus rhamnosus attenuates behavioural deficits and immune changes in chronic social stress. BMC Med., 15, 2017, 7.
12. Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30 (2014), 2114–2120.
13. Cryan, J.F., Dinan, T.G., Gut microbiota: Microbiota and neuroimmune signalling-Metchnikoff to microglia. Nat. Rev. Gastroenterol. Hepatol. 12 (2015), 494–496.
14. De Palma, G., Blennerhassett, P., Lu, J., Deng, Y., Park, A.J., Green, W., et al. Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nat. Commun., 6, 2015, 7735.
15. 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.
16. Diaz Heijtz, R., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., et al. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. U.S.A. 108 (2011), 3047–3052.
17. Dinan, T.G., Cryan, J.F., Microbes, immunity, and behavior: psychoneuroimmunology meets the microbiome. Neuropsychopharmacology 42 (2017), 178–192.
18. D'Mello, C., Ronaghan, N., Zaheer, R., Dicay, M., Le, T., MacNaughton, W.K., et al. Probiotics improve inflammation-associated sickness behavior by altering communication between the peripheral immune system and the brain. J. Neurosci. 35 (2015), 10821–10830.
19. do Prado, C.H., Narahari, T., Holland, F.H., Lee, H.N., Murthy, S.K., Brenhouse, H.C., Effects of early adolescent environmental enrichment on cognitive dysfunction, prefrontal cortex development, and inflammatory cytokines after early life stress. Dev. Psychobiol. 58 (2016), 482–491.
20. Dowlati, Y., Herrmann, N., Swardfager, W., Liu, H., Sham, L., Reim, E.K., et al. A meta-analysis of cytokines in major depression. Biol. Psychiatry 67 (2010), 446–457.
21. Erny, D., Hrabě de Angelis, A.L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 18 (2015), 965–977.
22. Etxeberria, U., Hijona, E., Aguirre, L., Milagro, F.I., Bujanda, L., Rimando, A.M., et al. Pterostilbene-induced changes in gut microbiota composition in relation to obesity. Mol. Nutr. Food Res., 2016 [Epub ahead of print].
23. Finnell, J.E., Lombard, C.M., Melson, M.N., Singh, N.P., Nagarkatti, M., Nagarkatti, P., et al. The protective effects of resveratrol on social stress-induced cytokine release and depressive-like behavior. Brain Behav. Immun. 59 (2017), 147–157.
24. Franklin, K.B.J., Paxinos, G., A Stereotaxic Atlas of the Mouse Brain. 1997, Academic Press, San Diego, CA.
25. Fung, T.C., Olson, C.A., Hsiao, E.Y., Interactions between the microbiota, immune and nervous systems in health and disease. Nat. Neurosci. 20 (2017), 145–155.
26. Galley, J.D., Nelson, M.C., Yu, Z., Dowd, S.E., Walter, J., Kumar, P.S., et al. Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol., 14, 2014, 189.
27. Goehler, L.E., Park, S.M., Opitz, N., Lyte, M., Gaykema, R.P., Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav. Immun. 22 (2008), 354–366.
28. Golden, S.A., Covington, H.E. 3rd, Berton, O., Russo, S.J., A standardized protocol for repeated social defeat stress in mice. Nat. Protoc. 6 (2011), 1183–1191.
29. Golubeva, A.V., Crampton, S., Desbonnet, L., Edge, D., O'Sullivan, O., Lomasney, K.W., et al. Prenatal stress-induced alterations in major physiological systems correlate with gut microbiota composition in adulthood. Psychoneuroendocrinology 60 (2015), 58–74.
30. Gur, T.L., Shay, L., Palkar, A.V., Fisher, S., Varaljay, V.A., Dowd, S., et al. Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring. Brain Behav. Immun., 2016 [Epub ahead of print].
31. Hodes, G.E., Pfau, M.L., Leboeuf, M., Golden, S.A., Christoffel, D.J., Bregman, D., et al. Individual differences in the peripheral immune system promote resilience versus susceptibility to social stress. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 16136–16141.
32. Hughes, J.B., Hellmann, J.J., Ricketts, T.H., Bohannan, B.J., Counting the uncountable: statistical approaches to estimating microbial diversity. Appl. Environ. Microbiol. 67 (2001), 4399–4406.
33. Jiang, H., Ling, Z., Zhang, Y., Mao, H., Ma, Z., Yin, Y., et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav. Immun. 48 (2015), 186–194.
34. Kelly, J.R., Borre, Y., O’ Brien, C., Patterson, E., El Aidy, S., Deane, J., et al. Transferring the blues: Depression-associated gut microbiota induces neurobehavioural changes in the rat. J. Psychiatry Res. 82 (2016), 109–118.
35. Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res., 41, 2013, e1.
36. Konikoff, T., Gophna, U., Oscillospira: a central, enigmatic component of the human gut microbiota. Trends Microbiol. 24 (2016), 523–524.
37. Krishnan, V., Nestler, E., The molecular neurobiology of depression. Nature 455 (2008), 894–902.
38. Krishnan, V., Han, M.H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131 (2007), 391–404.
39. Le, S., Josse, J., Husson, F., FactoMineR: an R Package for multivariate analysis. J. Stat. Softw. 25 (2008), 1–18.
40. Liang, S., Wang, T., Hu, X., Luo, J., Li, W., Wu, X., et al. Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress. Neuroscience 310 (2015), 561–577.
41. Liu, W., Crott, J.W., Lyu, L., Pfalzer, A.C., Li, J., Choi, S.W., et al. Diet- and genetically-induced obesity produces alterations in the microbiome, inflammation and Wnt pathway in the intestine of Apc+/1638N mice: comparisons and contrasts. J. Cancer 7 (2016), 1780–1790.
42. Liu, Y.W., Liu, W.H., Wu, C.C., Juan, Y.C., Wu, Y.C., Tsai, H.P., et al. Psychotropic effects of Lactobacillus plantarum PS128 in early life-stressed and naïve adult mice. Brain Res. 1631 (2016), 1–12.
43. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 (2001), 402–408.
44. Löwe, B., Andresen, V., Fraedrich, K., Gappmayer, K., Wegscheider, K., Treszl, A., et al. Psychological outcome, fatigue, and quality of life after infection with shiga toxin-producing Escherichia coli O104. Clin. Gastroenterol. Hepatol. 12 (2014), 1848–1855.
45. Lyte, M., Varcoe, J.J., Bailey, M.T., Anxiogenic effect of subclinical bacterial infection in mice in the absence of overt immune activation. Physiol. Behav. 65 (1998), 63–68.
46. Lyte, M., Li, W., Opitz, N., Gaykema, R.P., 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.
47. Marin, I.A., Goertz, J.E., Ren, T., Rich, S.S., Onengut-Gumuscu, S., Farber, E., et al. Microbiota alteration is associated with the development of stress-induced despair behavior. Sci. Rep., 7, 2017, 43859.
48. McCormack, D., McFadden, D., A review of pterostilbene antioxidant activity and disease modification. Oxid. Med. Cell Longev., 2013, 2013, 575482.
49. 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), 255–264.
50. O'Mahony, S.M., Marchesi, J.R., Scully, P., Codling, C., Ceolho, A.M., Quigley, E.M., et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiatry 65 (2009), 263–267.
51. Orieux, N., Douet, D.G., Le Hénaff, M., Bourdineaud, J.P., Prevalence of Flavobacterium psychrophilum bacterial cells in farmed rainbow trout: characterization of metallothionein A and interleukin1-β genes as markers overexpressed in spleen and kidney of diseased fish. Vet. Microbiol. 162 (2013), 127–135.
52. Pusceddu, M.M., El Aidy, S., Crispie, F., O'Sullivan, O., Cotter, P., Stanton, C., et al. N-3 polyunsaturated fatty acids (PUFAs) reverse the impact of early-life stress on the gut microbiota. PLoS One, 10, 2015, e0139721.
53. Pusceddu, M.M., Kelly, P., Ariffin, N., Cryan, J.F., Clarke, G., Dinan, T.G., N-3 PUFAs have beneficial effects on anxiety and cognition in female rats: effects of early life stress. Psychoneuroendocrinology 58 (2015), 79–90.
54. R Core Team, R: A Language and Environment for Statistical Computing. 2016, R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/.
55. Rea, K., Dinan, T.G., Cryan, J.F., The microbiome: a key regulator of stress and neuroinflammation. Neurobiol. Stress 4 (2016), 23–33.
56. Roque, A., Ochoa-Zarzosa, A., Torner, L., Maternal separation activates microglial cells and induces an inflammatory response in the hippocampus of male rat pups, independently of hypothalamic and peripheral cytokine levels. Brain Behav. Immun. 55 (2016), 39–48.
57. Savignac, H.M., Couch, Y., Stratford, M., Bannerman, D.M., Tzortzis, G., Anthony, D.C., et al. Prebiotic administration normalizes lipopolysaccharide (LPS)-induced anxiety and cortical 5-HT2A receptor and IL1-β levels in male mice. Brain Behav. Immun. 52 (2016), 120–130.
58. Schäffler, H., Herlemann, D.P., Alberts, C., Kaschitzki, A., Bodammer, P., Bannert, K., et al. Mucosa-attached bacterial community in Crohn's disease coheres with the clinical disease activity index. Environ. Microbiol. Rep., 2016 [Epub ahead of print].
59. Schmittgen, T.D., Livak, K.J., Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3 (2008), 1101–1108.
60. Shah, R., Cope, J.L., Nagy-Szakal, D., Dowd, S., Versalovic, J., Hollister, E.B., et al. Composition and function of the pediatric colonic mucosal microbiome in untreated patients with ulcerative colitis. Gut Microbes 7 (2016), 384–396.
61. Stecher, B., The roles of inflammation, nutrient availability and the commensal microbiota in enteric pathogen infection. Microbiol. Spectr. 3 (2015), 1–17.
62. Stewart, A.M., Roy, S., Wong, K., Gaikwad, S., Chung, K.M., Kalueff, A.V., Cytokine and endocrine parameters in mouse chronic social defeat: implications for translational ‘cross-domain’ modeling of stress-related brain disorders. Behav Brain. Res. 276 (2015), 84–91.
63. Tarr, A.J., Galley, J.D., Fisher, S.E., Chichlowski, M., Berg, B.M., Bailey, M.T., The prebiotics 3’Sialyllactose and 6’Sialyllactose diminish stressor-induced anxiety-like behavior and colonic microbiota alterations: evidence for effects on the gut-brain axis. Brain Behav. Immun. 50 (2015), 166–177.
64. Ünal, H.Ü., Akin, E., Aydin, İ., Korkmaz, M., Özel, S., Selçuk, H., et al. Ongoing symptoms after eradication of Helicobacter pylori: psychiatric disorders may accompany. Turk. J. Gastroenterol. 24 (2013), 15–21.
65. Walters, W.A., Xu, Z., Knight, R., Meta-analyses of human gut microbes associated with obesity and IBD. FEBS Lett. 588 (2014), 4223–4233.
66. Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73 (2007), 5261–5267.
67. Weber, M.D., Frank, M.G., Sobesky, J.L., Watkins, L.R., Maier, S.F., Blocking toll-like receptor 2 and 4 signaling during a stressor prevents stress-induced priming of neuroinflammatory responses to a subsequent immune challenge. Brain Behav. Immun. 32 (2013), 112–121.
68. Weber, M.D., Godbout, J.P., Sheridan, J.F., Repeated social defeat, neuroinflammation, and behavior: monocytes carry the signal. Neuropsychopharmacology 42 (2017), 46–61.
69. Wohleb, E.S., Hanke, M.L., Corona, A.W., Powell, N.D., Stiner, L.M., Bailey, M.T., et al. Β-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 31 (2011), 6277–6288.
70. Zheng, P., Zeng, B., Zhou, C., Liu, M., Fang, Z., Xu, X., et al. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host's metabolism. Mol. Psychiatry 21 (2016), 786–796.