Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium

Infection and Immunity

Volumn 78, Issue 4, 2010, Pages 1509-1519

  Bailey, Michael T ^a,b   Dowd, Scot E ^c   Parry, Nicola M A ^d   Galley, Jeffrey D ^a   Schauer, David B ^d,e   Lyte, Mark ^f  

^a OHIO STATE UNIVERSITY   (United States)

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

^c Medical Biofilm Research Institute Lubbock   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e Massachusetts Institute of Technology Cambridge   (United States)

^f TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA;

AMPLICON; ANAEROBIC BACTERIUM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL OVERGROWTH; BACTERIUM CULTURE; CECUM; CITROBACTER RODENTIUM; COLON; COMMENSAL; CONTROLLED STUDY; GENE EXPRESSION; INFECTION SENSITIVITY; INTESTINE FLORA; MALE; MICROBIAL DIVERSITY; MICROBIAL POPULATION DYNAMICS; MOUSE; NONHUMAN; PHYSIOLOGICAL STRESS; PORPHYROMONADACEAE; PRIORITY JOURNAL; PYROSEQUENCING;

ANIMALS; BACTERIA; BIODIVERSITY; CITROBACTER RODENTIUM; COLONY COUNT, MICROBIAL; ENTEROBACTERIACEAE INFECTIONS; GASTROINTESTINAL TRACT; MALE; MICE; STRESS, PHYSIOLOGICAL;

EID: 77950202391     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00862-09     Document Type: Article

References (53)

1. Acosta-Martinez, V., S. Dowd, Y. Sun, and V. Allen. 2008. Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol. Biochem. 40:2762-2770.
2. Antonopoulos, D. A., S. M. Huse, H. G. Morrison, T. M. Schmidt, M. L. Sogin, and V. B. Young. 2009. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect. Immun. 77:2367-2375.
3. Bailey, M., H. Engler, J. Hunzeker, and J. F. Sheridan. 2003. The hypothalamic-pituitary-adrenal axis and viral infection. Viral Immunol. 16:141-157.
4. Bailey, M. T., and C. L. Coe. 1999. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev. Psychobiol. 35:146-155.
5. Bailey, M. T., G. R. Lubach, and C. L. Coe. 2004. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J. Pediatr. Gastroenterol. Nutr. 38:414-421.
6. Barthold, S. W., G. L. Coleman, P. N. Bhatt, G. W. Osbaldiston, and A. M. Jonas. 1976. The etiology of transmissible murine colonic hyperplasia. Lab. Anim. Sci. 26:889-894.
7. Barthold, S. W., G. W. Osbaldiston, and A. M. Jonas. 1977. Dietary, bacterial, and host genetic interactions in the pathogenesis of transmissible murine colonic hyperplasia. Lab. Anim. Sci. 27:938-945.
8. Berkenbosch, F., D. A. Wolvers, and R. Derijk. 1991. Neuroendocrine and immunological mechanisms in stress-induced immunomodulation. J. Steroid Biochem. Mol. Biol. 40:639-647.
9. Borenshtein, D., P. R. Nambiar, E. B. Groff, J. G. Fox, and D. B. Schauer. 2007. Development of fatal colitis in FVB mice infected with Citrobacter rodentium. Infect. Immun. 75:3271-3281.
10. Borenshtein, D., K. A. Schlieper, B. H. Rickman, J. M. Chapman, C. W. Schweinfest, J. G. Fox, and D. B. Schauer. 2009. Decreased expression of colonic Slc26a3 (Dra) and carbonic anhydrase IV as a cause of fatal infectious diarrhea in mice. Infect. Immun. 77:3639-3650.
11. Chang, D. E., D. J. Smalley, D. L. Tucker, M. P. Leatham, W. E. Norris, S. J. Stevenson, A. B. Anderson, J. E. Grissom, D. C. Laux, P. S. Cohen, and T. Conway. 2004. Carbon nutrition of Escherichia coli in the mouse intestine. Proc. Natl. Acad. Sci. U. S. A. 101:7427-7432.
12. Chen, C., D. R. Brown, Y. Xie, B. T. Green, and M. Lyte. 2003. Catecholamines modulate Escherichia coli O157:H7 adherence to murine cecal mucosa. Shock 20:183-188.
13. Chen, C. C., S. Louie, H. N. Shi, and W. A. Walker. 2005. Preinoculation with the probiotic Lactobacillus acidophilus early in life effectively inhibits murine Citrobacter rodentium colitis. Pediatr. Res. 58:1185-1191.
14. Cole, J. R., Q. Wang, E. Cardenas, J. Fish, B. Chai, R. J. Farris, A. S. Kulam-Syed-Mohideen, D. M. McGarrell, T. Marsh, G. M. Garrity, and J. M. Tiedje. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145.
15. Dicksved, J., J. Halfvarson, M. Rosenquist, G. Jarnerot, C. Tysk, J. Apajalahti, L. Engstrand, and J. K. Jansson. 2008. Molecular analysis of the gut microbiota of identical twins with Crohn's disease. ISME J. 2:716-727.
16. Dowd, S. E., T. R. Callaway, R. D. Wolcott, Y. Sun, T. McKeehan, R. G. Hagevoort, and T. S. Edrington. 2008. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 8:125.
17. Dowd, S. E., R. D. Wolcott, Y. Sun, T. McKeehan, E. Smith, and D. Rhoads. 2008. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One 3:e3326.
18. Dowd, S. E., J. Zaragoza, J. R. Rodriguez, M. J. Oliver, and P. R. Payton. 2005. Windows .NET Network Distributed Basic Local Alignment Search Toolkit (W.ND-BLAST). BMC Bioinformatics 6:93.
19. Drossman, D. A. 1998. Presidential address: gastrointestinal illness and the biopsychosocial model. Psychosom. Med. 60:258-267.
20. Everson, C. A., and L. A. Toth. 2000. Systemic bacterial invasion induced by sleep deprivation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278:R905-R916.
21. Gaynes, B. N., and D. A. Drossman. 1999. The role of psychosocial factors in irritable bowel syndrome. Baillieres Best Pract. Res. Clin. Gastroenterol. 13:437-452.
22. Gibson, D. L., C. Ma, K. S. Bergstrom, J. T. Huang, C. Man, and B. A. Vallance. 2008. MyD88 signalling plays a critical role in host defence by controlling pathogen burden and promoting epithelial cell homeostasis during Citrobacter rodentium-induced colitis. Cell. Microbiol. 10:618-631.
23. Gill, S. R., M. Pop, R. T. Deboy, P. B. Eckburg, P. J. Turnbaugh, B. S. Samuel, J. I. Gordon, D. A. Relman, C. M. Fraser-Liggett, and K. E. Nelson. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312:1355-1359.
24. Glavin, G. B., W. P. Pare, T. Sandbak, H. K. Bakke, and R. Murison. 1994. Restraint stress in biomedical research: an update. Neurosci. Biobehav. Rev. 18:223-249.
25. Green, B. T., M. Lyte, C. Chen, Y. Xie, M. A. Casey, A. Kulkarni-Narla, L. Vulchanova, and D. R. Brown. 2004. Adrenergic modulation of Escherichia coli O157:H7 adherence to the colonic mucosa. Am. J. Physiol. Gastrointest. Liver Physiol. 287:G1238-G1246.
26. Green, B. T., M. Lyte, A. Kulkarni-Narla, and D. R. Brown. 2003. Neuro-modulation of enteropathogen internalization in Peyer's patches from porcine jejunum. J. Neuroimmunol. 141:74-82.
27. Hapfelmeier, S., and W. D. Hardt. 2005. A mouse model for S. typhimurium-induced enterocolitis. Trends Microbiol. 13:497-503.
28. Holdeman, L. V., I. J. Good, and W. E. Moore. 1976. Human fecal flora: variation in bacterial composition within individuals and a possible effect of emotional stress. Appl. Environ. Microbiol. 31:359-375.
29. Itoh, K., K. Maejima, K. Ueda, and K. Fujiwara. 1979. Difference in susceptibility of mice raised under barrier-sustained (SPF) or conventional conditions to infectious megaenteron. Microbiol. Immunol. 23:909-913.
30. Itoh, K., A. Ozaki, T. Yamamoto, and T. Mitsuoka. 1978. An autoclavable stainless steel isolator for small scale gnotobiotic experiments. Jikken Dobutsu 27:13-16. (In Japanese.)
31. Itoh, K., K. Ueda, and K. Fujiwara. 1980. Susceptibility of germ-free mice to infectious megaenteron. Microbiol. Immunol. 24:281-290.
32. Jarillo-Luna, A., V. Rivera-Aguilar, H. R. Garfias, E. Lara-Padilla, A. Kormanovsky, and R. Campos-Rodriguez. 2007. Effect of repeated restraint stress on the levels of intestinal IgA in mice. Psychoneuroendocrinology 32:681-692.
33. Kassinen, A., L. Krogius-Kurikka, H. Makivuokko, T. Rinttila, L. Paulin, J. Corander, E. Malinen, J. Apajalahti, and A. Palva. 2007. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 133:24-33.
34. Knowles, S. R., E. A. Nelson, and E. A. Palombo. 2008. Investigating the role of perceived stress on bacterial flora activity and salivary cortisol secretion: a possible mechanism underlying susceptibility to illness. Biol. Psychol. 77:132-137.
35. Kvetnansky, R., K. Fukuhara, K. Pacak, G. Cizza, D. S. Goldstein, and I. J. Kopin. 1993. Endogenous glucocorticoids restrain catecholamine synthesis and release at rest and during immobilization stress in rats. Endocrinology 133:1411-1419.
36. Lizko, N. N. 1987. Stress and intestinal microflora. Nahrung 31:443-447.
37. Lupp, C., M. L. Robertson, M. E. Wickham, I. Sekirov, O. L. Champion, E. C. Gaynor, and B. B. Finlay. 2007. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2:119-129.
38. Lyte, M. 2004. Microbial endocrinology and infectious disease in the 21st century. Trends Microbiol. 12:14-20.
39. Lyte, M., A. K. Erickson, B. P. Arulanandam, C. D. Frank, M. A. Crawford, and D. H. Francis. 1997. Norepinephrine-induced expression of the K99 pilus adhesin of enterotoxigenic Escherichia coli. Biochem. Biophys. Res. Commun. 232:682-686.
40. Lyte, M., P. P. Freestone, C. P. Neal, B. A. Olson, R. D. Haigh, R. Bayston, and P. H. Williams. 2003. Stimulation of Staphylococcus epidermidis growth and biofilm formation by catecholamine inotropes. Lancet 361:130-135.
41. Lyte, M., and K. T. Nguyen. 1997. Alteration of Escherichia coli O157:H7 growth and molecular fingerprint by the neuroendocrine hormone noradrenaline. Microbios 89:197-213.
42. Nishikawa, J., T. Kudo, S. Sakata, Y. Benno, and T. Sugiyama. 2009. Diversity of mucosa-associated microbiota in active and inactive ulcerative colitis. Scand. J. Gastroenterol. 44:180-186.
43. Nocker, A., M. Burr, and A. K. Camper. 2007. Genotypic microbial community profiling: a critical technical review. Microb. Ecol. 54:276-289.
44. O'Hara, A. M., and F. Shanahan. 2006. The gut flora as a forgotten organ. EMBO Rep. 7:688-693.
45. Plotsky, P. M., and M. J. Meaney. 1993. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res. Mol. Brain Res. 18:195-200.
46. Reyna-Garfias, H., A. Miliar, A. Jarillo-Luna, V. Rivera-Aguilar, J. Pacheco-Yepez, I. Baeza, and R. Campos-Rodriguez. 2010. Repeated restraint stress increases IgA concentration in rat small intestine. Brain Behav. Immun. 24:110-118.
47. Ringel, Y., and D. A. Drossman. 2001. Psychosocial aspects of Crohn's disease. Surg. Clin. North Am. 81:231-252.
48. Schaedler, R. W., and R. J. Dubos. 1962. The fecal flora of various strains of mice. Its bearing on their susceptibility to endotoxin. J. Exp. Med. 115:1149-1160.
49. Schauer, D. B., and S. Falkow. 1993. The eae gene of Citrobacter freundii biotype 4280 is necessary for colonization in transmissible murine colonic hyperplasia. Infect. Immun. 61:4654-4661.
50. Turnbaugh, P. J., M. Hamady, T. Yatsunenko, B. L. Cantarel, A. Duncan, R. E. Ley, M. L. Sogin, W. J. Jones, B. A. Roe, J. P. Affourtit, M. Egholm, B. Henrissat, A. C. Heath, R. Knight, and J. I. Gordon. 2009. A core gut microbiome in obese and lean twins. Nature 457:480-484.
51. Vaarala, O., M. A. Atkinson, and J. Neu. 2008. The "perfect storm" for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes 57:2555-2562.
52. Vallance, B. A., W. Deng, K. Jacobson, and B. B. Finlay. 2003. Host susceptibility to the attaching and effacing bacterial pathogen Citrobacter rodentium. Infect. Immun. 71:3443-3453.
53. van der Waaij, D., J. M. Berghuis-de Vries, and L. Lekkerkerk. 1971. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. (Lond.) 69:405-411.