Effects of stress on commensal microbes and immune system activity

Advances in Experimental Medicine and Biology

Volumn 874, Issue , 2016, Pages 289-300

  Gur, Tamar L ^a   Bailey, Michael T ^b  

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

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

Author keywords

Gut brain axis; Immunomodulation; Microbiome; Psychosocial stress; Stress

Indexed keywords

GLUCOCORTICOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROBIOTIC AGENT; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ADRENERGIC SYSTEM; BACTERIAL GROWTH; BACTERIAL TRANSLOCATION; BACTERIUM ADHERENCE; BIFIDOBACTERIUM; CATECHOLAMINE RELEASE; COMMENSAL; COMMUNITY STRUCTURE; GROWTH RATE; HORMONE RELEASE; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNE SYSTEM; IMMUNOMODULATION; INNATE IMMUNITY; INTESTINE FLORA; LACTOBACILLUS; MENTAL STRESS; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; SPECIES COMPOSITION; SYMBIONT; ANIMAL; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; GASTROINTESTINAL MICROBIOME; HUMANS; STRESS, PSYCHOLOGICAL;

EID: 84947708201     PISSN: 00652598     EISSN: 22148019     Source Type: Book Series    
DOI: 10.1007/978-3-319-20215-0_14     Document Type: Chapter

References (69)

1. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J (2014) The placenta harbors a unique microbiome. Sci Transl Med 6: 237ra65
2. Allen RG, Lafuse WP, Galley JD, Ali MM, Ahmer BM, Bailey MT (2012a) The intestinal microbiota are necessary for stressor-induced enhancement of splenic macrophage microbicidal activity. Brain Behav Immun 26: 371-382
3. Allen RG, Lafuse WP, Powell ND, Stiner-Jones LM, Webster Marketon JI, Sheridan JF, Bailey MT (2012b) Stressor-induced increase in microbicidal activity of splenic macrophages is dependent upon peroxynitrite production. Infect Immun 80: 3429-3437
4. Avitsur R, Stark JL, Dhabhar FS, Sheridan JF (2002) Social stress alters splenocyte phenotype and function. J Neuroimmunol 132: 66-71
5. Avitsur R, Kavelaars A, Heijnen C, Sheridan JF (2005) Social stress and the regulation of tumor necrosis factor-alpha secretion. Brain Behav Immun 19: 311-317
6. Bailey MT, Coe CL (1999) Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35: 146-155
7. Bailey MT, Karaszewski JW, Lubach GR, Coe CL, Lyte M (1999) In vivo adaptation of attenuated Salmonella typhimurium results in increased growth upon exposure to norepinephrine. Physiol Behav 67: 359-364
8. Bailey MT, Lubach GR, Coe CL (2004) Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 38: 414-421
9. Bailey MT, Engler H, Sheridan JF (2006) Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice. J Neuroimmunol 171: 29-37
10. Bailey MT, Engler H, Powell ND, Padgett DA, Sheridan JF (2007) Repeated social defeat increases the bactericidal activity of splenic macrophages through a Toll-like receptor-dependent pathway. Am J Physiol Regul Integr Comp Physiol 293: R1180-R1190
11. Bailey MT, Kierstein S, Sharma S, Spaits M, Kinsey SG, Tliba O, Amrani Y, Sheridan JF, Panettieri RA, Haczku A (2009a) Social stress enhances allergen-induced airway inflammation in mice and inhibits corticosteroid responsiveness of cytokine production. J Immunol 182: 7888-7896
12. Bailey MT, Kinsey SG, Padgett DA, Sheridan JF, Leblebicioglu B (2009b) Social stress enhances IL-1beta and TNF-alpha production by Porphyromonas gingivalis lipopolysaccharidestimulated CD11b+ cells. Physiol Behav 98: 351-358
13. Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M (2010) Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 78: 1509-1519
14. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M (2011) Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 25: 397-407
15. Bellavance MA, Rivest S (2014) The HPA—immune axis and the immunomodulatory actions of glucocorticoids in the brain. Front Immunol 5: 136
16. Berg RD (1996) The indigenous gastrointestinal microflora. Trends Microbiol 4: 430-435
17. Berg RD (1999) Bacterial translocation from the gastrointestinal tract. Adv Exp Med Biol 473: 11-30
18. Bierhaus A, Wolf J, Andrassy M, Rohleder N, Humpert PM, Petrov D, Ferstl R, VON Eynatten M, Wendt T, Rudofsky G, Joswig M, Morcos M, Schwaninger M, McEwen B, Kirschbaum C, Nawroth PP (2003) A mechanism converting psychosocial stress into mononuclear cell activation. Proc Natl Acad Sci U S A 100: 1920-1925
19. Boudry G, Morise A, Seve B, Huërou-Luron ILE (2011) Effect of milk formula protein content on intestinal barrier function in a porcine model of LBW neonates. Pediatr Res 69: 4-9
20. Brydon L, Steptoe A (2005) Stress-induced increases in interleukin-6 and fibrinogen predict ambulatory blood pressure at 3-year follow-up. J Hypertens 23: 1001-1007
21. Brydon L, Edwards S, Jia H, Mohamed-Ali V, Zachary I, Martin JF, Steptoe A (2005) Psychological stress activates interleukin-1beta gene expression in human mononuclear cells. Brain Behav Immun 19: 540-546
22. Brydon L, Magid K, Steptoe A (2006) Platelets, coronary heart disease, and stress. Brain Behav Immun 20: 113-119
23. Coussons-Read ME, Okun ML, Nettles CD (2007) Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain Behav Immun 21: 343-350
24. Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13: 701-712
25. Digiulio DB (2012) Diversity of microbes in amniotic fluid. Semin Fetal Neonatal Med 17: 2-11
26. Dinan TG, Stanton C, Cryan JF (2013) Psychobiotics: a novel class of psychotropic. Biol Psychiatry 74: 720-726
27. Emeny RT, Zierer A, Lacruz ME, Baumert J, Herder C, Gornitzka G, Koenig W, Thorand B, Ladwig KH, Investigators K (2013) Job strain-associated inflammatory burden and long-term risk of coronary events: findings from the MONICA/KORA Augsburg case-cohort study. Psychosom Med 75: 317-325
28. Engler H, Bailey MT, Engler A, Stiner-Jones LM, Quan N, Sheridan JF (2008) Interleukin-1 receptor type 1-deficient mice fail to develop social stress-associated glucocorticoid resistance in the spleen. Psychoneuroendocrinology 33: 108-117
29. Fernandez MF, Boris S, Barbes C (2003) Probiotic properties of human lactobacilli strains to be used in the gastrointestinal tract. J Appl Microbiol 94: 449-455
30. Freestone PP, Williams PH, Haigh RD, Maggs AF, Neal CP, Lyte M (2002) Growth stimulation of intestinal commensal Escherichia coli by catecholamines: a possible contributory factor in trauma-induced sepsis. Shock 18: 465-470
31. Freestone PP, Sandrini SM, Haigh RD, Lyte M (2008) Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol 16: 55-64
32. Galley JD, Nelson MC, Yu Z, Dowd SE, Walter J, Kumar PS, Lyte M, Bailey MT (2014a) Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol 14: 189
33. Galley JD, Yu Z, Kumar P, Dowd SE, Lyte M, Bailey MT (2014b) The structures of the colonic mucosa-associated and luminal microbial communities are distinct and differentially affected by a prolonged murine stressor. Gut Microbes 5: 748-760
34. Gareau MG, Jury J, Yang PC, Macqueen G, Perdue MH (2006) Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance. Pediatr Res 59: 83-88
35. Goldenberg RL, Hauth JC, Andrews WW (2000) Intrauterine infection and preterm delivery. N Engl J Med 342: 1500-1507
36. Goncalves LF, Chaiworapongsa T, Romero R (2002) Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev 8: 3-13
37. Gordon JI, Hooper LV, Mcnevin MS, Wong M, Bry L (1997) Epithelial cell growth and differentiation. III. Promoting diversity in the intestine: conversations between the microflora, epithelium, and diffuse GALT. Am J Physiol 273: G565-G570
38. Goyal N, Rishi P, Shukla G (2013) Lactobacillus rhamnosus GG antagonizes Giardia intestinalis induced oxidative stress and intestinal disaccharidases: an experimental study. World J Microbiol Biotechnol 29: 1049-1057
39. Green BT, Lyte M, Chen C, Xie Y, Casey MA, Kulkarni-Narla A, Vulchanova L, Brown DR (2004) Adrenergic modulation of Escherichia coli O157: H7 adherence to the colonic mucosa. Am J Physiol Gastrointest Liver Physiol 287: G1238-G1246
40. Gur TL, Worly BL, Bailey MT (2015) Stress and the commensal microbiota: importance in parturition and infant neurodevelopment. Front Psychiatry 6: 5
41. Hanke ML, Powell ND, Stiner LM, Bailey MT, Sheridan JF (2012) Beta adrenergic blockade decreases the immunomodulatory effects of social disruption stress. Brain Behav Immun 26: 1150-1159
42. Huth C, Thorand B, Baumert J, Kruse J, Emeny RT, Schneider A, Meisinger C, Ladwig KH (2014) Job strain as a risk factor for the onset of type 2 diabetes mellitus: findings from the MONICA/ KORA Augsburg cohort study. Psychosom Med 76: 562-568
43. Kailasapathy K, Chin J (2000) Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol 78: 80-88
44. Lalles JP (2012) Long term effects of pre- and early postnatal nutrition and environment on the gut. J Anim Sci 90(Suppl 4): 421-429
45. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489: 220-230
46. Lyte M (2004) The biogenic amine tyramine modulates the adherence of Escherichia coli O157: H7 to intestinal mucosa. J Food Prot 67: 878-883
47. Lyte M, Bailey MT (1997) Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma. J Surg Res 70: 195-201
48. Lyte M, Nguyen KT (1997) Alteration of Escherichia coli O157: H7 growth and molecular fingerprint by the neuroendocrine hormone noradrenaline. Microbios 89: 197-213
49. Mackos AR, Eubank TD, Parry NM, Bailey MT (2013) Probiotic Lactobacillus reuteri attenuates the stressor-enhanced severity of Citrobacter rodentium infection. Infect Immun 81: 3253-3263
50. Maslanik T, Tannura K, Mahaffey L, Loughridge AB, Beninson L, Ursell L, Greenwood BN, Knight R, Fleshner M (2012) Commensal bacteria and MAMPs are necessary for stressinduced increases in IL-1beta and IL-18 but not IL-6, IL-10 or MCP-1. PLoS One 7, e50636
51. Mays JW, Bailey MT, Hunzeker JT, Powell ND, Papenfuss T, Karlsson EA, Padgett DA, Sheridan JF (2010) Influenza virus-specific immunological memory is enhanced by repeated social defeat. J Immunol 184: 2014-2025
52. McLaughlin KA, Conron KJ, Koenen KC, Gilman SE (2010) Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: a test of the stress sensitization hypothesis in a population-based sample of adults. Psychol Med 40: 1647-1658
53. Nakade Y, Tsuchida D, Fukuda H, Iwa M, Pappas TN, Takahashi T (2005) Restraint stress delays solid gastric emptying via a central CRF and peripheral sympathetic neuron in rats. Am J Physiol Regul Integr Comp Physiol 288: R427-R432
54. Nakade Y, Fukuda H, Iwa M, Tsukamoto K, Yanagi H, Yamamura T, Mantyh C, Pappas TN, Takahashi T (2007) Restraint stress stimulates colonic motility via central corticotropinreleasing factor and peripheral 5-HT3 receptors in conscious rats. Am J Physiol Gastrointest Liver Physiol 292: G1037-G1044
55. O'Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF, Dinan TG (2009) Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65: 263-267
56. Pullinger GD, Carnell SC, Sharaff FF, VAN Diemen PM, Dziva F, Morgan E, Lyte M, Freestone PP, Stevens MP (2010) Norepinephrine augments Salmonella enterica-induced enteritis in a manner associated with increased net replication but independent of the putative adrenergic sensor kinases QseC and QseE. Infect Immun 78: 372-380
57. Shanahan F (2002) The host-microbe interface within the gut. Best Pract Res Clin Gastroenterol 16: 915-931
58. Shapiro GD, Fraser WD, Frasch MG, Seguin JR (2013) Psychosocial stress in pregnancy and preterm birth: associations and mechanisms. J Perinat Med 41: 631-645
59. Shichijo K, Ito M, Taniyama K, Sekine I (1993) The role of sympathetic neurons for low susceptibility to stress in gastric lesions. Life Sci 53: 261-267
60. Stark JL, Avitsur R, Padgett DA, Campbell KA, Beck FM, Sheridan JF (2001) Social stress induces glucocorticoid resistance in macrophages. Am J Physiol Regul Integr Comp Physiol 280: R1799-R1805
61. Stark JL, Avitsur R, Hunzeker J, Padgett DA, Sheridan JF (2002) Interleukin-6 and the development of social disruption-induced glucocorticoid resistance. J Neuroimmunol 124: 9-15
62. Stepankova R, Sinkora J, Hudcovic T, Kozakova H, Tlaskalova-Hogenova H (1998) Differences in development of lymphocyte subpopulations from gut-associated lymphatic tissue (GALT) of germfree and conventional rats: effect of aging. Folia Microbiol (Praha) 43: 531-534
63. Steptoe A, Hamer M, Chida Y (2007) The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav Immun 21: 901-912
64. Tannock GW, Savage DC (1974) Influences of dietary and environmental stress on microbial populations in the murine gastrointestinal tract. Infect Immun 9: 591-598
65. Thomas CM, Hong T, VAN Pijkeren JP, Hemarajata P, Trinh DV, Hu W, Britton RA, Kalkum M, Versalovic J (2012) Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One 7, e31951
66. Umesaki Y, Setoyama H, Matsumoto S, Okada Y (1993) Expansion of alpha beta T-cell receptorbearing intestinal intraepithelial lymphocytes after microbial colonization in germ-free mice and its independence from thymus. Immunology 79: 32-37
67. Umesaki Y, Okada Y, Matsumoto S, Imaoka A, Setoyama H (1995) Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse. Microbiol Immunol 39: 555-562
68. Wang SX, Wu WC (2005) Effects of psychological stress on small intestinal motility and bacteria and mucosa in mice. World J Gastroenterol 11: 2016-2021
69. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, Siuzdak G (2009) Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A 106: 3698-3703