Role of the Intestinal Microbiota in Host Responses to Stressor Exposure

International Review of Neurobiology

Volumn 131, Issue , 2016, Pages 1-19

  Mackos, A R ^a   Varaljay, V A ^a   Maltz, R ^a,b   Gur, T L ^c,d   Bailey, M T ^a,d,e  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b NATIONWIDE CHILDREN S HOSPITAL   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^d OHIO STATE UNIVERSITY   (United States)

^e THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Anxiety like behavior; Brain gut microbiota axis; Gut microbiota; Hypothalamic pituitary adrenal axis; Lactobacilli; Psychological stressors; Sympathetic nervous system

Indexed keywords

ANXIETY; BACTERIAL OVERGROWTH; BEHAVIOR DISORDER; BEHAVIORISM; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; MATERNAL STRESS; MENTAL STRESS; MICROBIAL COLONIZATION; MUCOSAL IMMUNITY; NERVE CELL DIFFERENTIATION; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; SOCIAL BEHAVIOR; BRAIN; IMMUNOLOGY; INTESTINE; MICROBIOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

BRAIN; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINES; STRESS, PSYCHOLOGICAL;

EID: 84995776189     PISSN: 00747742     EISSN: 21625514     Source Type: Book Series    
DOI: 10.1016/bs.irn.2016.08.002     Document Type: Chapter

References (71)

1. Aagaard, K., Ma, J., Antony, K.M., Ganu, R., Petrosino, J., Versalovic, J., The placenta harbors a unique microbiome. Science Translational Medicine, 6(237), 2014, 237ra265, 10.1126/scitranslmed.3008599.
2. Aguilera, M., Vergara, P., Martinez, V., Stress and antibiotics alter luminal and wall-adhered microbiota and enhance the local expression of visceral sensory-related systems in mice. Neurogastroenterology and Motility 25:8 (2013), e515–e529, 10.1111/nmo.12154.
3. Ardissone, A.N., de la Cruz, D.M., Davis-Richardson, A.G., Rechcigl, K.T., Li, N., Drew, J.C. et al., Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS One, 9(3), 2014, e90784, 10.1371/journal.pone.0090784.
4. Bailey, M.T., Influence of stressor-induced nervous system activation on the intestinal microbiota and the importance for immunomodulation. Lyte, M., Cryan, F.J., (eds.) Microbial endocrinology: The microbiota-gut-brain axis in health and disease, 2014, Springer New York, New York, NY, 255–276.
5. Bailey, M.T., Coe, C.L., Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Developmental Psychobiology 35:2 (1999), 146–155.
6. 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, Behavior, and Immunity 25:3 (2011), 397–407, 10.1016/j.bbi.2010.10.023.
7. Bailey, M.T., Dowd, S.E., Parry, N.M., Galley, J.D., Schauer, D.B., Lyte, M., Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infection and Immunity 78:4 (2010), 1509–1519, 10.1128/iai.00862-09.
8. Bailey, M.T., Engler, H., Sheridan, J.F., Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice. Journal of Neuroimmunology 171:1–2 (2006), 29–37, 10.1016/j.jneuroim.2005.09.008.
9. Bailey, M.T., Karaszewski, J.W., Lubach, G.R., Coe, C.L., Lyte, M., In vivo adaptation of attenuated Salmonella typhimurium results in increased growth upon exposure to norepinephrine. Physiology & Behavior 67:3 (1999), 359–364.
10. Barouei, J., Moussavi, M., Hodgson, D.M., Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. PLoS One, 7(10), 2012, e46051, 10.1371/journal.pone.0046051.
11. Bearson, B.L., Bearson, S.M., The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. Microbial Pathogenesis 44:4 (2008), 271–278, 10.1016/j.micpath.2007.10.001.
12. Bergström, A., Skov, T.H., Bahl, M.I., Roager, H.M., Christensen, L.B., Ejlerskov, K.T. et al., Establishment of intestinal microbiota during early life: A longitudinal, explorative study of a large cohort of Danish infants. Applied and Environmental Microbiology 80:9 (2014), 2889–2900, 10.1128/aem.00342-14.
13. 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 http://dx.doi.org/10.1016/j.psyneuen.2015.10.001.
14. Chang, J.Y., Antonopoulos, D.A., Kalra, A., Tonelli, A., Khalife, W.T., Schmidt, T.M. et al., Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. Journal of Infectious Diseases 197:3 (2008), 435–438, 10.1086/525047.
15. Chen, C., Lyte, M., Stevens, M.P., Vulchanova, L., Brown, D.R., Mucosally-directed adrenergic nerves and sympathomimetic drugs enhance non-intimate adherence of Escherichia coli O157:H7 to porcine cecum and colon. European Journal of Pharmacology 539:1–2 (2006), 116–124, 10.1016/j.ejphar.2006.03.081.
16. Costello, E.K., Lauber, C.L., Hamady, M., Fierer, N., Gordon, J.I., Knight, R., Bacterial community variation in human body habitats across space and time. Science 326:5960 (2009), 1694–1697, 10.1126/science.1177486.
17. Cryan, J.F., Dinan, T.G., Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nature Reviews. Neuroscience 13:10 (2012), 701–712, 10.1038/nrn3346.
18. David, L.A., Maurice, C.F., Carmody, R.N., Gootenberg, D.B., Button, J.E., Wolfe, B.E. et al., Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:7484 (2014), 559–563, 10.1038/nature12820.
19. 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. Nature Communications, 6, 2015, 7735, 10.1038/ncomms8735.
20. de Vos, W.M., Microbial biofilms and the human intestinal microbiome. Npj Biofilms and Microbiomes, 1, 2015, 15005, 10.1038/npjbiofilms.2015.5.
21. Donaldson, G.P., Lee, S.M., Mazmanian, S.K., Gut biogeography of the bacterial microbiota. Nature Reviews. Microbiology 14:1 (2016), 20–32, 10.1038/nrmicro3552.
22. Duerkop, B.A., Vaishnava, S., Hooper, L.V., Immune responses to the microbiota at the intestinal mucosal surface. Immunity 31:3 (2009), 368–376.
23. Engler, H., Bailey, M.T., Engler, A., Stiner-Jones, L.M., Quan, N., Sheridan, J.F., Interleukin-1 receptor type 1-deficient mice fail to develop social stress-associated glucocorticoid resistance in the spleen. Psychoneuroendocrinology 33:1 (2008), 108–117, 10.1016/j.psyneuen.2007.10.007.
24. Francino, M.P., Antibiotics and the human gut microbiome: Dysbioses and accumulation of resistances. Frontiers in Microbiology, 6, 2015, 1543, 10.3389/fmicb.2015.01543.
25. Freestone, P.P., Haigh, R.D., Lyte, M., Blockade of catecholamine-induced growth by adrenergic and dopaminergic receptor antagonists in Escherichia coli O157:H7, Salmonella enterica and Yersinia enterocolitica. BMC Microbiology, 7, 2007, 8, 10.1186/1471-2180-7-8.
26. Freestone, P.P., Haigh, R.D., Lyte, M., Specificity of catecholamine-induced growth in Escherichia coli O157:H7, Salmonella enterica and Yersinia enterocolitica. FEMS Microbiology Letters 269:2 (2007), 221–228, 10.1111/j.1574-6968.2006.00619.x.
27. Freestone, P.P., Lyte, M., Neal, C.P., Maggs, A.F., Haigh, R.D., Williams, P.H., The mammalian neuroendocrine hormone norepinephrine supplies iron for bacterial growth in the presence of transferrin or lactoferrin. Journal of Bacteriology 182:21 (2000), 6091–6098.
28. Freestone, P.P., Williams, P.H., Haigh, R.D., Maggs, A.F., Neal, C.P., Lyte, M., Growth stimulation of intestinal commensal Escherichia coli by catecholamines: A possible contributory factor in trauma-induced sepsis. Shock 18:5 (2002), 465–470.
29. 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 Microbiology, 14, 2014, 189, 10.1186/1471-2180-14-189.
30. Galley, J.D., Parry, N.M., Ahmer, B.M.M., Fox, J.G., & Bailey, M.T. The commensal microbiota exacerbate infectious colitis in stressor-exposed mice. Brain, Behavior, and Immunity, under review.
31. Galley, J.D., Yu, Z., Kumar, P., Dowd, S.E., Lyte, M., Bailey, M.T., The structures of the colonic mucosa-associated and luminal microbial communities are distinct and differentially affected by a prolonged murine stressor. Gut Microbes 5:6 (2014), 748–760, 10.4161/19490976.2014.972241.
32. Green, B.T., Lyte, M., Chen, C., Xie, Y., Casey, M.A., Kulkarni-Narla, A. et al., Adrenergic modulation of Escherichia coli O157:H7 adherence to the colonic mucosa. American Journal of Physiology. Gastrointestinal and Liver Physiology 287:6 (2004), G1238–G1246, 10.1152/ajpgi.00471.2003.
33. Gur, T.L., Worly, B.L., Bailey, M.T., Stress and the commensal microbiota: Importance in parturition and infant neurodevelopment. Front Psychiatry, 6, 2015, 5, 10.3389/fpsyt.2015.00005.
34. Hooper, L.V., Gordon, J.I., Commensal host-bacterial relationships in the gut. Science 292:5519 (2001), 1115–1118, 10.1126/science.1058709.
35. Howerton, C.L., Bale, T.L., Prenatal programing: At the intersection of maternal stress and immune activation. Hormones and Behavior 62:3 (2012), 237–242, 10.1016/j.yhbeh.2012.03.007.
36. Jasarevic, E., Howerton, C.L., Howard, C.D., Bale, T.L., Alterations in the vaginal microbiome by maternal stress are associated with metabolic reprogramming of the offspring gut and brain. Endocrinology 156:9 (2015), 3265–3276, 10.1210/en.2015-1177.
37. Koenig, J.E., Spor, A., Scalfone, N., Fricker, A.D., Stombaugh, J., Knight, R. et al., Succession of microbial consortia in the developing infant gut microbiome. Proceedings of the National Academy of Sciences of the United States of America 108:Suppl 1 (2011), 4578–4585, 10.1073/pnas.1000081107.
38. Kostic, A.D., Howitt, M.R., Garrett, W.S., Exploring host-microbiota interactions in animal models and humans. Genes & Development 27:7 (2013), 701–718, 10.1101/gad.212522.112.
39. Lafuse, W.P., Gearinger, R., Fisher, S., Nealer, C., & Bailey, M.T. Exposure to a social stressor induces translocation of commensal lactobacilli to the spleen and priming of the innate immune system. Journal of Immunology, under review.
40. Lederberg, J., McCray, A.T., ‘Ome sweet ‘omics: A genealogical treasury of words. The Scientist, 15, 2001, 8.
41. Lyte, M., Bailey, M.T., Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma. The Journal of Surgical Research 70:2 (1997), 195–201, 10.1006/jsre.1997.5130.
42. Lyte, M., Ernst, S., Catecholamine induced growth of gram negative bacteria. Life Sciences 50:3 (1992), 203–212.
43. Lyte, M., Vulchanova, L., Brown, D.R., Stress at the intestinal surface: Catecholamines and mucosa-bacteria interactions. Cell and Tissue Research 343:1 (2011), 23–32, 10.1007/s00441-010-1050-0.
44. Mackos, A.R., Eubank, T.D., Parry, N.M., Bailey, M.T., Probiotic Lactobacillus reuteri attenuates the stressor-enhanced severity of Citrobacter rodentium infection. Infection and Immunity 81:9 (2013), 3253–3263, 10.1128/iai.00278-13.
45. Mackos, A.R., Galley, J.D., Eubank, T.D., Easterling, R.S., Parry, N.M., Fox, J.G. et al., Social stress-enhanced severity of Citrobacter rodentium-induced colitis is CCL2-dependent and attenuated by probiotic Lactobacillus reuteri. Mucosal Immunology 9:2 (2016), 515–526, 10.1038/mi.2015.81.
46. Maslanik, T., Mahaffey, L., Tannura, K., Beninson, L., Greenwood, B.N., Fleshner, M., The inflammasome and danger associated molecular patterns (DAMPs) are implicated in cytokine and chemokine responses following stressor exposure. Brain, Behavior, and Immunity 28 (2013), 54–62, 10.1016/j.bbi.2012.10.014.
47. Maslanik, T., Tannura, K., Mahaffey, L., Loughridge, A.B., Beninson, L., Ursell, L. et al., Commensal bacteria and MAMPs are necessary for stress-induced increases in IL-1beta and IL-18 but not IL-6, IL-10 or MCP-1. PLoS One, 7(12), 2012, e50636, 10.1371/journal.pone.0050636.
48. Moles, L., Gómez, M., Heilig, H., Bustos, G., Fuentes, S., de Vos, W. et al., Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One, 8(6), 2013, e66986, 10.1371/journal.pone.0066986.
49. Morgan, X.C., Segata, N., Huttenhower, C., Biodiversity and functional genomics in the human microbiome. Trends in Genetics 29:1 (2013), 51–58 http://dx.doi.org/10.1016/j.tig.2012.09.005.
50. Neu, J., Rushing, J., Cesarean versus vaginal delivery: Long-term infant outcomes and the hygiene hypothesis. Clinics in Perinatology 38:2 (2011), 321–331, 10.1016/j.clp.2011.03.008.
51. O'Mahony, S.M., Clarke, G., Dinan, T.G., Cryan, J.F., Early-life adversity and brain development: Is the microbiome a missing piece of the puzzle?. Neuroscience, 2015, 10.1016/j.neuroscience.2015.09.068 Epub ahead of print.
52. O'Mahony, S.M., Felice, V.D., Nally, K., Savignac, H.M., Claesson, M.J., Scully, P. et al., 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, 10.1016/j.neuroscience.2014.07.054.
53. 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. Biological Psychiatry 65:3 (2009), 263–267, 10.1016/j.biopsych.2008.06.026.
54. Rastall, R.A., Bacteria in the gut: Friends and Foes and how to alter the balance. The Journal of Nutrition 134:8 (2004), 2022S–2026S.
55. Reber, S.O., Siebler, P.H., Donner, N.C., Morton, J.T., Smith, D.G., Kopelman, J.M. et al., Immunization with a heat-killed preparation of the environmental bacterium Mycobacterium vaccae promotes stress resilience in mice. Proceedings of the National Academy of Sciences of the United States of America 113:22 (2016), E3130–E3139, 10.1073/pnas.1600324113.
56. Sakuma, K., Funabashi, H., Matsuoka, H., Saito, M., Potential use of Lactobacillus cell density in feces as a non-invasive bio-indicator for evaluating environmental stress during mouse breeding. Biocontrol Science 18:2 (2013), 101–104.
57. Sandrini, S.M., Shergill, R., Woodward, J., Muralikuttan, R., Haigh, R.D., Lyte, M. et al., Elucidation of the mechanism by which catecholamine stress hormones liberate iron from the innate immune defense proteins transferrin and lactoferrin. Journal of Bacteriology 192:2 (2010), 587–594, 10.1128/jb.01028-09.
58. Sartor, R.B., Mazmanian, S.K., Intestinal microbes in inflammatory bowel diseases. The American Journal of Gastroenterology Supplements 1:1 (2012), 15–21.
59. Sekirov, I., Russell, S.L., Antunes, L.C., Finlay, B.B., Gut microbiota in health and disease. Physiological Reviews 90:3 (2010), 859–904, 10.1152/physrev.00045.2009.
60. Sender, R., Fuchs, S., Milo, R., Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164:3 (2016), 337–340, 10.1016/j.cell.2016.01.013.
61. Spor, A., Koren, O., Ley, R., Unravelling the effects of the environment and host genotype on the gut microbiome. Nature Reviews. Microbiology 9:4 (2011), 279–290, 10.1038/nrmicro2540.
62. Stothart, M.R., Bobbie, C.B., Schulte-Hostedde, A.I., Boonstra, R., Palme, R., Mykytczuk, N.C. et al., Stress and the microbiome: Linking glucocorticoids to bacterial community dynamics in wild red squirrels. Biology Letters, 12(1), 2016, 20150875, 10.1098/rsbl.2015.0875.
63. Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X.N. et al., Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. The Journal of Physiology 558:Pt 1 (2004), 263–275, 10.1113/jphysiol.2004.063388.
64. Tannock, G.W., Savage, D.C., Influences of dietary and environmental stress on microbial populations in the murine gastrointestinal tract. Infection and Immunity 9:3 (1974), 591–598.
65. 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, Behavior, and Immunity 50 (2015), 166–177, 10.1016/j.bbi.2015.06.025.
66. Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R., Gordon, J.I., An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:7122 (2006), 1027–1131, 10.1038/nature05414 http://www.nature.com/nature/journal/v444/n7122/suppinfo/nature05414_S1.html.
67. Van den Abbeele, P., Van de Wiele, T., Verstraete, W., Possemiers, S., The host selects mucosal and luminal associations of coevolved gut microorganisms: A novel concept. FEMS Microbiology Reviews 35:4 (2011), 681–704, 10.1111/j.1574-6976.2011.00270.x.
68. Voreades, N., Kozil, A., Weir, T., Diet and the development of the human intestinal microbiome. Frontiers in Microbiology, 5, 2014, 494.
69. Wohleb, E.S., Powell, N.D., Godbout, J.P., Sheridan, J.F., Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. The Journal of Neuroscience 33:34 (2013), 13820–13833, 10.1523/jneurosci.1671-13.2013.
70. Yap, I.K., Angley, M., Veselkov, K.A., Holmes, E., Lindon, J.C., Nicholson, J.K., Urinary metabolic phenotyping differentiates children with autism from their unaffected siblings and age-matched controls. Journal of Proteome Research 9:6 (2010), 2996–3004, 10.1021/pr901188e.
71. Zheng, P., Chen, J.J., Huang, T., Wang, M.J., Wang, Y., Dong, M.X. et al., A novel urinary metabolite signature for diagnosing major depressive disorder. Journal of Proteome Research 12:12 (2013), 5904–5911, 10.1021/pr400939q.