Skip to main content

Influence of Stressor-Induced Nervous System Activation on the Intestinal Microbiota and the Importance for Immunomodulation

  • Chapter
  • First Online:
Book cover Microbial Endocrinology: The Microbiota-Gut-Brain Axis in Health and Disease

Part of the book series: Advances in Experimental Medicine and Biology ((MICENDO,volume 817))

Abstract

The body is colonized by a vast population of genetically diverse microbes, the majority of which reside within the intestines to comprise the intestinal microbiota. During periods of homeostasis, these microbes reside within stable climax communities, but exposure to physical, physiological, as well as psychological stressors can significantly impact the structure of the intestinal microbiota. This has been demonstrated in humans and laboratory animals, with the most consistent finding being a reduction in the abundance of bacteria in the genus Lactobacillus. Whether stressor exposure also changes the function of the microbiota, has not been as highly studied. The studies presented in this review suggest that stressor-induced disruption of the intestinal microbiota leads to increased susceptibility to enteric infection and overproduction of inflammatory mediators that can induce behavioral abnormalities, such as anxiety-like behavior. Studies involving germfree mice also demonstrate that the microbiota are necessary for stressor-induced increases in innate immunity to occur. Exposing mice to a social stressor enhances splenic macrophage microbicidal activity, but this effect fails to occur in germfree mice. These studies suggest a paradigm in which stressor exposure alters homeostatic interactions between the intestinal microbiota and mucosal immune system and leads to the translocation of pathogenic, and/or commensal, microbes from the lumen of the intestines to the interior of the body where they trigger systemic inflammatory responses and anxiety-like behavior. Restoring homeostasis in the intestines, either by removing the microbiota or by administering probiotic microorganisms, can ameliorate the stressor effects.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ACTH:

Adrenocorticotrophic hormone

CFU:

Colony forming units

CRH:

Corticotrophin release hormone

DGGE:

Denaturing gradient gel electrophoresis

GABA:

γ-Amino butyric acid

GI:

Gastrointestinal

HPA:

Hypothalamic-pituitary-adrenal

iNOS:

Inducible nitric oxide synthase

mRNA:

Messenger ribonucleic acid

NE:

Norepinephrine

SDR:

Social disruption

SNS:

Sympathetic nervous system

TNF-α:

Tumor necrosis factor alpha

References

  1. Huffnagle GB (2010) The microbiota and allergies/asthma. PLoS Pathog 6(5):e1000549

    Article  PubMed Central  PubMed  Google Scholar 

  2. Allison SD, Martiny JB (2008) Colloquium paper: resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105(Suppl 1):11512–11519

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB (2009) Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun 77(6):2367–2375

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Dethlefsen L, Huse S, Sogin ML, Relman DA (2008) The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 6(11):e280

    Article  PubMed Central  PubMed  Google Scholar 

  5. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3(4):213–223

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Beaumont W (1838) Experiments and observations on the gastric juice and the physiology of digestion. Edinburgh, London

    Google Scholar 

  7. Badgley LE, Spiro HM, Senay EC (1969) Effect of mental arithmetic on gastric secretion. Psychophysiology 5(6):633–637

    Article  CAS  PubMed  Google Scholar 

  8. Holtmann G, Kriebel R, Singer MV (1990) Mental stress and gastric acid secretion. Do personality traits influence the response? Dig Dis Sci 35(8):998–1007

    Article  CAS  PubMed  Google Scholar 

  9. Yang H, Yuan PQ, Wang L, Tache Y (2000) Activation of the parapyramidal region in the ventral medulla stimulates gastric acid secretion through vagal pathways in rats. Neuroscience 95(3):773–779

    Article  CAS  PubMed  Google Scholar 

  10. Tache Y, Martinez V, Million M, Wang L (2001) Stress and the gastrointestinal tract III. Stress-related alterations of gut motor function: role of brain corticotropin-releasing factor receptors. Am J Physiol Gastrointest Liver Physiol 280(2):G173–G177

    CAS  PubMed  Google Scholar 

  11. Tache Y, Perdue MH (2004) Role of peripheral CRF signalling pathways in stress-related alterations of gut motility and mucosal function. Neurogastroenterol Motil 16(Suppl 1):137–142

    Article  PubMed  Google Scholar 

  12. O’Malley D, Julio-Pieper M, Gibney SM, Dinan TG, Cryan JF (2010) Distinct alterations in colonic morphology and physiology in two rat models of enhanced stress-induced anxiety and depression-like behaviour. Stress 13(2):114–122

    Article  PubMed  Google Scholar 

  13. Shigeshiro M, Tanabe S, Suzuki T (2012) Repeated exposure to water immersion stress reduces the Muc2 gene level in the rat colon via two distinct mechanisms. Brain Behav Immun 26(7):1061–1065

    Article  CAS  PubMed  Google Scholar 

  14. Drasar BS, Shiner M, McLeod GM (1969) Studies on the intestinal flora. I. The bacterial flora of the gastrointestinal tract in healthy and achlorhydric persons. Gastroenterology 56(1):71–79

    CAS  PubMed  Google Scholar 

  15. Berg RD (1996) The indigenous gastrointestinal microflora. Trends Microbiol 4(11):430–435

    Article  CAS  PubMed  Google Scholar 

  16. Stephen AM, Wiggins HS, Cummings JH (1987) Effect of changing transit time on colonic microbial metabolism in man. Gut 28(5):601–609

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Sonnenburg JL, Xu J, Leip DD et al (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307(5717):1955–1959

    Article  CAS  PubMed  Google Scholar 

  18. Mackenzie DA, Jeffers F, Parker ML et al (2010) Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiology 156(Pt 11):3368–3378

    Article  CAS  PubMed  Google Scholar 

  19. Lyte M (2004) Microbial endocrinology and infectious disease in the 21st century. Trends Microbiol 12(1):14–20

    Article  CAS  PubMed  Google Scholar 

  20. Lyte M, Bailey MT (1997) Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma. J Surg Res 70(2):195–201

    Article  CAS  PubMed  Google Scholar 

  21. Pullinger GD, Carnell SC, Sharaff FF et al (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(1):372–380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Tannock GW, Savage DC (1974) Influences of dietary and environmental stress on microbial populations in the murine gastrointestinal tract. Infect Immun 9(3):591–598

    CAS  PubMed Central  PubMed  Google Scholar 

  23. Everson CA, Toth LA (2000) Systemic bacterial invasion induced by sleep deprivation. Am J Physiol Regul Integr Comp Physiol 278(4):R905–R916

    CAS  PubMed  Google Scholar 

  24. Lizko NN (1987) Stress and intestinal microflora. Nahrung 31(5–6):443–447

    Article  CAS  PubMed  Google Scholar 

  25. Holdeman LV, Good IJ, Moore WE (1976) Human fecal flora: variation in bacterial composition within individuals and a possible effect of emotional stress. Appl Environ Microbiol 31(3):359–375

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Bailey MT, Coe CL (1999) Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35(2):146–155

    Article  CAS  PubMed  Google Scholar 

  27. Bailey MT, Lubach GR, Coe CL (2004) Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 38(4):414–421

    Article  PubMed  Google Scholar 

  28. Sakuma K, Funabashi H, Matsuoka H, Saito M (2013) Potential use of Lactobacillus cell density in feces as a non-invasive bio-indicator for evaluating environmental stress during mouse breeding. Biocontrol Sci 18(2):101–104

    Article  PubMed  Google Scholar 

  29. Aguilera M, Vergara P, Martinez V (2013) Environment-related adaptive changes of gut commensal microbiota do not alter colonic toll-like receptors but modulate the local expression of sensory-related systems in rats. Microb Ecol 66(1):232–243

    Article  CAS  PubMed  Google Scholar 

  30. Knowles SR, Nelson EA, Palombo EA (2008) Investigating the role of perceived stress on bacterial flora activity and salivary cortisol secretion: a possible mechanism underlying susceptibility to illness. Biol Psychol 77(2):132–137

    Article  PubMed  Google Scholar 

  31. Sartor RB (2006) Microbial and dietary factors in the pathogenesis of chronic, immune-mediated intestinal inflammation. Adv Exp Med Biol 579:35–54

    Article  CAS  PubMed  Google Scholar 

  32. Nocker A, Burr M, Camper AK (2007) Genotypic microbial community profiling: a critical technical review. Microb Ecol 54(2):276–289

    Article  CAS  PubMed  Google Scholar 

  33. O’Mahony SM, Marchesi JR, Scully P et al (2009) Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65(3):263–267

    Article  PubMed  Google Scholar 

  34. 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(4):1509–1519

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. 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(3):397–407

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Buynitsky T, Mostofsky DI (2009) Restraint stress in biobehavioral research: recent developments. Neurosci Biobehav Rev 33(7):1089–1098

    Article  PubMed  Google Scholar 

  37. Dobbs CM, Vasquez M, Glaser R, Sheridan JF (1993) Mechanisms of stress-induced modulation of viral pathogenesis and immunity. J Neuroimmunol 48(2):151–160

    Article  CAS  PubMed  Google Scholar 

  38. Dobbs CM, Feng N, Beck FM, Sheridan JF (1996) Neuroendocrine regulation of cytokine production during experimental influenza viral infection: effects of restraint stress-induced elevation in endogenous corticosterone. J Immunol 157(5):1870–1877

    CAS  PubMed  Google Scholar 

  39. Padgett DA, MacCallum RC, Sheridan JF (1998) Stress exacerbates age-related decrements in the immune response to an experimental influenza viral infection. J Gerontol A Biol Sci Med Sci 53(5):B347–B353

    Article  CAS  PubMed  Google Scholar 

  40. Sartor RB (2012) Gut microbiota: diet promotes dysbiosis and colitis in susceptible hosts. Nat Rev Gastroenterol Hepatol 9(10):561–562

    Article  PubMed  Google Scholar 

  41. Chang JY, Antonopoulos DA, Kalra A et al (2008) Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 197(3):435–438

    Article  PubMed  Google Scholar 

  42. Borenshtein D, McBee ME, Schauer DB (2008) Utility of the Citrobacter rodentium infection model in laboratory mice. Curr Opin Gastroenterol 24(1):32–37

    Article  PubMed  Google Scholar 

  43. Luperchio SA, Schauer DB (2001) Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect 3(4):333–340

    Article  CAS  PubMed  Google Scholar 

  44. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S (2005) Citrobacter rodentium of mice and man. Cell Microbiol 7(12):1697–1706

    Article  CAS  PubMed  Google Scholar 

  45. Eckmann L (2006) Animal models of inflammatory bowel disease: lessons from enteric infections. Ann N Y Acad Sci 1072:28–38

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Google Scholar 

  47. Cameron HL, Perdue MH (2005) Stress impairs murine intestinal barrier function: improvement by glucagon-like peptide-2. J Pharmacol Exp Ther 314(1):214–220

    Article  CAS  PubMed  Google Scholar 

  48. Santos J, Yang PC, Soderholm JD, Benjamin M, Perdue MH (2001) Role of mast cells in chronic stress induced colonic epithelial barrier dysfunction in the rat. Gut 48(5):630–636

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Soderholm JD, Yates DA, Gareau MG, Yang PC, MacQueen G, Perdue MH (2002) Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. Am J Physiol Gastrointest Liver Physiol 283(6):G1257–G1263

    CAS  PubMed  Google Scholar 

  50. Eaton KA, Honkala A, Auchtung TA, Britton RA (2011) Probiotic Lactobacillus reuteri ameliorates disease due to enterohemorrhagic Escherichia coli in germfree mice. Infect Immun 79(1):185–191

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Bohus B, Koolhaas JM, Heijnen CJ, de Boer O (1993) Immunological responses to social stress: dependence on social environment and coping abilities. Neuropsychobiology 28(1–2):95–99

    Article  CAS  PubMed  Google Scholar 

  52. de Groot J, van Milligen FJ, Moonen-Leusen BW, Thomas G, Koolhaas JM (1999) A single social defeat transiently suppresses the anti-viral immune response in mice. J Neuroimmunol 95(1–2):143–151

    Article  PubMed  Google Scholar 

  53. Korte SM, Smit J, Bouws GAH, Koolhaas JM, Bohus B (1990) Behavioral and neuroendocrine response to psychosocial stress in male rats: the effects of the 5-HT1A agonistic ipsapirone. Horm Behav 24:554–567

    Article  CAS  PubMed  Google Scholar 

  54. Sgoifo A, Stilli D, de Boer SF, Koolhaas JM, Musso E (1998) Acute social stress and cardiac electrical activity in rats. Aggress Behav 24:287–296

    Article  Google Scholar 

  55. Kinsey SG, Bailey MT, Sheridan JF, Padgett DA, Avitsur R (2007) Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice. Brain Behav Immun 21(4):458–466

    Article  PubMed Central  PubMed  Google Scholar 

  56. Wohleb ES, Hanke ML, Corona AW et al (2011) beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J Neurosci 31(17):6277–6288

    Google Scholar 

  57. Bailey MT, Avitsur R, Engler H, Padgett DA, Sheridan JF (2004) Physical defeat reduces the sensitivity of murine splenocytes to the suppressive effects of corticosterone. Brain Behav Immun 18(5):416–424

    Article  CAS  PubMed  Google Scholar 

  58. Engler H, Engler A, Bailey MT, Sheridan JF (2005) Tissue-specific alterations in the glucocorticoid sensitivity of immune cells following repeated social defeat in mice. J Neuroimmunol 163(1–2):110–119

    Article  CAS  PubMed  Google Scholar 

  59. 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(7):1150–1159

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Avitsur R, Kavelaars A, Heijnen C, Sheridan JF (2005) Social stress and the regulation of tumor necrosis factor-alpha secretion. Brain Behav Immun 19(4):311–317

    Article  CAS  PubMed  Google Scholar 

  61. 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(1):108–117

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. 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(1–2):9–15

    Article  CAS  PubMed  Google Scholar 

  63. Brydon L, Edwards S, Mohamed-Ali V, Steptoe A (2004) Socioeconomic status and stress-induced increases in interleukin-6. Brain Behav Immun 18(3):281–290

    Article  CAS  PubMed  Google Scholar 

  64. 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(5):1001–1007

    Article  CAS  PubMed  Google Scholar 

  65. 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(7):901–912

    Article  CAS  PubMed  Google Scholar 

  66. Avitsur R, Stark JL, Dhabhar FS, Padgett DA, Sheridan JF (2002) Social disruption-induced glucocorticoid resistance: kinetics and site specificity. J Neuroimmunol 124(1–2):54–61

    Article  CAS  PubMed  Google Scholar 

  67. 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(3):R1180–R1190

    Article  CAS  PubMed  Google Scholar 

  68. Bailey MT, Kinsey SG, Padgett DA, Sheridan JF, Leblebicioglu B (2009) Social stress enhances IL-1beta and TNF-alpha production by Porphyromonas gingivalis lipopolysaccharide-stimulated CD11b + cells. Physiol Behav 98(3):351–358

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. 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(6):R1799–R1805

    CAS  PubMed  Google Scholar 

  70. Platt AM, Bain CC, Bordon Y, Sester DP, Mowat AM (2010) An independent subset of TLR expressing CCR2-dependent macrophages promotes colonic inflammation. J Immunol 184(12):6843–6854

    Article  CAS  PubMed  Google Scholar 

  71. Jones SE, Versalovic J (2009) Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol 9:35

    Article  PubMed Central  PubMed  Google Scholar 

  72. Lin YP, Thibodeaux CH, Pena JA, Ferry GD, Versalovic J (2008) Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun. Inflamm Bowel Dis 14(8):1068–1083

    Article  PubMed  Google Scholar 

  73. Thomas CM, Hong T, van Pijkeren JP et al (2012) Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One 7(2):e31951

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Spinler JK, Taweechotipatr M, Rognerud CL, Ou CN, Tumwasorn S, Versalovic J (2008) Human-derived probiotic Lactobacillus reuteri demonstrate antimicrobial activities targeting diverse enteric bacterial pathogens. Anaerobe 14(3):166–171

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. Sudo N, Chida Y, Aiba Y et al (2004) Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 558(Pt 1):263–275

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. Padgett DA, Glaser R (2003) How stress influences the immune response. Trends Immunol 24(8):444–448

    Article  CAS  PubMed  Google Scholar 

  77. Reber SO, Peters S, Slattery DA et al (2011) Mucosal immunosuppression and epithelial barrier defects are key events in murine psychosocial stress-induced colitis. Brain Behav Immun 25(6):1153–1161

    Article  CAS  PubMed  Google Scholar 

  78. Lyte M (2011) Probiotics function mechanistically as delivery vehicles for neuroactive compounds: microbial endocrinology in the design and use of probiotics. Bioessays 33(8):574–581

    Article  CAS  PubMed  Google Scholar 

  79. Kiecolt-Glaser JK, Preacher KJ, MacCallum RC, Atkinson C, Malarkey WB, Glaser R (2003) Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc Natl Acad Sci U S A 100(15):9090–9095

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. Brydon L, Edwards S, Jia H et al (2005) Psychological stress activates interleukin-1beta gene expression in human mononuclear cells. Brain Behav Immun 19(6):540–546

    Article  CAS  PubMed  Google Scholar 

  81. Maslanik T, Tannura K, Mahaffey L et al (2012) 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):e50636

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  82. Maslanik T, Mahaffey L, Tannura K, Beninson L, Greenwood BN, Fleshner M (2013) The inflammasome and danger associated molecular patterns (DAMPs) are implicated in cytokine and chemokine responses following stressor exposure. Brain Behav Immun 28:54–62

    Article  CAS  PubMed  Google Scholar 

  83. Fleshner M (2013) Stress-evoked sterile inflammation, danger associated molecular patterns (DAMPs), microbial associated molecular patterns (MAMPs) and the inflammasome. Brain Behav Immun 27(1):1–7

    Article  CAS  PubMed  Google Scholar 

  84. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN (2010) Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med 16(2):228–231

    Article  CAS  PubMed  Google Scholar 

  85. Allen RG, Lafuse WP, Galley JD, Ali MM, Ahmer BM, Bailey MT (2012) The intestinal microbiota are necessary for stressor-induced enhancement of splenic macrophage microbicidal activity. Brain Behav Immun 26(3):371–382

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  86. Allen RG, Lafuse WP, Powell ND et al (2012) Stressor-induced increase in microbicidal activity of splenic macrophages is dependent upon peroxynitrite production. Infect Immun 80(10):3429–3437

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  87. Ahrne S, Hagslatt ML (2011) Effect of lactobacilli on paracellular permeability in the gut. Nutrients 3(1):104–117

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  88. 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(1–2):29–37

    Article  CAS  PubMed  Google Scholar 

  89. Ando T, Brown RF, Berg RD, Dunn AJ (2000) Bacterial translocation can increase plasma corticosterone and brain catecholamine and indoleamine metabolism. Am J Physiol Regul Integr Comp Physiol 279(6):R2164–R2172

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael T. Bailey .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer New York

About this chapter

Cite this chapter

Bailey, M.T. (2014). Influence of Stressor-Induced Nervous System Activation on the Intestinal Microbiota and the Importance for Immunomodulation. In: Lyte, M., Cryan, J. (eds) Microbial Endocrinology: The Microbiota-Gut-Brain Axis in Health and Disease. Advances in Experimental Medicine and Biology(), vol 817. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-0897-4_12

Download citation

Publish with us

Policies and ethics