Impact of stressor exposure on the interplay between commensal microbiota and host inflammation

Gut Microbes

Volumn 5, Issue 3, 2014, Pages

  Galley, Jeffrey D ^a   Bailey, Michael T ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

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

Author keywords

Anxiety; Bacterial translocation; Brain gut axis; Colitis; Dysbiosis; Lactobacillus; Psychological stress; Social defeat

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; HYDROCORTISONE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; TOLL LIKE RECEPTOR 4;

ACHLORHYDRIA; BACTERIAL OVERGROWTH; BACTERIAL TRANSLOCATION; BEHAVIORAL STRESS; COLITIS; COLON MOTILITY; DENATURING GRADIENT GEL ELECTROPHORESIS; DYSBIOSIS; ENTERITIS; EVOKED RESPONSE; GERMFREE ANIMAL; HOMEOSTASIS; HUMAN; HYPERSENSITIVITY; IMMUNOMODULATION; INFLAMMATION; INTESTINE FLORA; LACTOBACILLUS; NONHUMAN; PHYSIOLOGICAL STRESS; PYROSEQUENCING; REVIEW; STOMACH EMPTYING; STOMACH MOTILITY; STOMACH MUCOSA; ANIMAL; BACTERIUM; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY; PRIMATE; RODENT; SYMBIOSIS;

ANIMALS; BACTERIA; GASTROINTESTINAL TRACT; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION; PRIMATES; RODENTIA; STRESS, PHYSIOLOGICAL; SYMBIOSIS;

EID: 84900838331     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.28683     Document Type: Review

References (66)

1. Huffnagle GB. The microbiota and allergies/asthma. PLoS Pathog 2010; 6:e1000549; PMID:20523892; http://dx.doi.org/10.1371/journal.ppat.1000549
2. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science 2005; 307:1915-20; PMID:15790844; http://dx.doi.org/10.1126/science.1104816
3. Reinhardt C, Bergentall M, Greiner TU, Schaffner F, Ostergren-Lundén G, Petersen LC, Ruf W, Bäckhed F. Tissue factor and PAR1 promote microbiota-induced intestinal vascular remodelling. Nature 2012; 483:627-31; PMID:22407318; http://dx.doi.org/10.1038/nature10893
4. Tomas J, Wrzosek L, Bouznad N, Bouet S, Mayeur C, Noordine ML, Honvo-Houeto E, Langella P, Thomas M, Cherbuy C. Primocolonization is associated with colonic epithelial maturation during conventionalization. FASEB J 2013; 27:645-55; PMID:23118025; http://dx.doi.org/10.1096/fj.12-216861
5. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 2004; 101:15718-23; PMID:15505215; http://dx.doi.org/10.1073/pnas.0407076101
6. Sayin SI, Wahlström A, Felin J, Jäntti S, Marschall HU, Bamberg K, Angelin B, Hyötyläinen T, Orešic M, Bäckhed F. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab 2013; 17:225-35; PMID:23395169; http://dx.doi.org/10.1016/j.cmet.2013.01.003
7. Resta SC. Effects of probiotics and commensals on intestinal epithelial physiology: implications for nutrient handling. J Physiol 2009; 587:4169-74; PMID:19596893; http://dx.doi.org/10.1113/jphysiol.2009.176370
8. Bercik P, Denou E, Collins J, Jackson W, Lu J, Jury J, Deng Y, Blennerhassett P, Macri J, McCoy KD, et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 2011; 141:599-609, e1-3; PMID:21683077; http://dx.doi.org/10.1053/j.gastro.2011.04.052
9. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011; 108:3047-52; PMID:21282636; http://dx.doi.org/10.1073/pnas.1010529108
10. Hansen CH, Nielsen DS, Kverka M, Zakostelska Z, Klimesova K, Hudcovic T, Tlaskalova-Hogenova H, Hansen AK. Patterns of early gut colonization shape future immune responses of the host. PLoS One 2012; 7:e34043; PMID:22479515; http://dx.doi.org/10.1371/journal.pone.0034043
11. El Aidy S, van Baarlen P, Derrien M, Lindenbergh-Kortleve DJ, Hooiveld G, Levenez F, Doré J, Dekker J, Samsom JN, Nieuwenhuis EE, et al. Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunol 2012; 5:567-79; PMID:22617837; http://dx.doi.org/10.1038/mi.2012.32
12. Shichijo K, Ito M, Taniyama K, Sekine I. The role of sympathetic neurons for low susceptibility to stress in gastric lesions. Life Sci 1993; 53:261-7; PMID:8321086; http://dx.doi.org/10.1016/0024-3205(93)90677-U
13. Yang H, Yuan PQ, Wang L, Taché Y. Activation of the parapyramidal region in the ventral medulla stimulates gastric acid secretion through vagal pathways in rats. Neuroscience 2000; 95:773-9; PMID:10670444; http://dx.doi.org/10.1016/S0306-4522(99)00490-X
14. Nakade Y, Tsuchida D, Fukuda H, Iwa M, Pappas TN, Takahashi T. Restraint stress delays solid gastric emptying via a central CRF and peripheral sympathetic neuron in rats. Am J Physiol Regul Integr Comp Physiol 2005; 288:R427-32; PMID:15458973; http://dx.doi.org/10.1152/ajpregu.00499.2004
15. Wang SX, Wu WC. Effects of psychological stress on small intestinal motility and bacteria and mucosa in mice. World J Gastroenterol 2005; 11:2016-21; PMID:15800998
16. Nakade Y, Fukuda H, Iwa M, Tsukamoto K, Yanagi H, Yamamura T, Mantyh C, Pappas TN, Takahashi T. Restraint stress stimulates colonic motility via central corticotropin-releasing factor and peripheral 5-HT3 receptors in conscious rats. Am J Physiol Gastrointest Liver Physiol 2007; 292:G1037-44; PMID:17158256; http://dx.doi.org/10.1152/ajpgi.00419.2006
17. Castagliuolo I, Lamont JT, Qiu B, Fleming SM, Bhaskar KR, Nikulasson ST, Kornetsky C, Pothoulakis C. Acute stress causes mucin release from rat colon: role of corticotropin releasing factor and mast cells. Am J Physiol 1996; 271:G884-92; PMID:8944704
18. Jarillo-Luna A, Rivera-Aguilar V, Garfias HR, Lara-Padilla E, Kormanovsky A, Campos-Rodríguez R. Effect of repeated restraint stress on the levels of intestinal IgA in mice. Psychoneuroendocrinology 2007; 32:681-92; PMID:17590521; http://dx.doi.org/10.1016/j.psyneuen.2007.04.009
19. Drasar BS, Shiner M, McLeod GM. Studies on the intestinal flora. I. The bacterial flora of the gastrointestinal tract in healthy and achlorhydric persons. Gastroenterology 1969; 56:71-9; PMID:4885396
20. Nieuwenhuijs VB, Verheem A, van Duijvenbode-Beumer H, Visser MR, Verhoef J, Gooszen HG, Akkermans LM. The role of interdigestive small bowel motility in the regulation of gut microflora, bacterial overgrowth, and bacterial translocation in rats. Ann Surg 1998; 228:188-93; PMID:9712563; http://dx.doi.org/10.1097/00000658-199808000-00007
21. Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 2004; 54:1469-76; PMID:15388697; http://dx.doi.org/10.1099/ijs.0.02873-0
22. Bailey MT, Karaszewski JW, Lubach GR, Coe CL, Lyte M. In vivo adaptation of attenuated Salmonella typhimurium results in increased growth upon exposure to norepinephrine. Physiol Behav 1999; 67:359-64; PMID:10497953; http://dx.doi.org/10.1016/S0031-9384(99)00087-6
23. Pullinger GD, Carnell SC, Sharaff FF, van Diemen PM, Dziva F, Morgan E, Lyte M, Freestone PP, Stevens MP. 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 2010; 78:372-80; PMID:19884332; http://dx.doi.org/10.1128/IAI.01203-09
24. Green BT, Lyte M, Chen C, Xie Y, Casey MA, Kulkarni-Narla A, Vulchanova L, Brown DR. Adrenergic modulation of Escherichia coli O157:H7 adherence to the colonic mucosa. Am J Physiol Gastrointest Liver Physiol 2004; 287:G1238-46; PMID:15534374; http://dx.doi.org/10.1152/ajpgi.00471.2003
25. Tannock GW, Savage DC. Influences of dietary and environmental stress on microbial populations in the murine gastrointestinal tract. Infect Immun 1974; 9:591-8; PMID:4593471
26. Bailey MT, Coe CL. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 1999; 35:146-55; PMID:10461128; http://dx.doi.org/10.1002/(SICI)1098-2302(199909)35:2
27. Bailey MT, Lubach GR, Coe CL. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 2004; 38:414-21; PMID:15085020; http://dx.doi.org/10.1097/00005176-200404000-00009
28. Knowles SR, Nelson EA, Palombo EA. Investigating the role of perceived stress on bacterial flora activity and salivary cortisol secretion: a possible mechanism underlying susceptibility to illness. Biol Psychol 2008; 77:132-7; PMID:18023961; http://dx.doi.org/10.1016/j.biopsycho.2007.09.010
29. O'Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF, Dinan TG. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 2009; 65:263-7; PMID:18723164; http://dx.doi.org/10.1016/j.biopsych.2008.06.026
30. Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 2010; 78:1509-19; PMID:20145094; http://dx.doi.org/10.1128/IAI.00862-09
31. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 2011; 25:397-407; PMID:21040780; http://dx.doi.org/10.1016/j.bbi.2010.10.023
32. Roberts CJ, Campbell IC, Troop N. Increases in weight during chronic stress are partially associated with a switch in food choice towards increased carbohydrate and saturated fat intake. Eur Eat Disord Rev 2014; 22:77-82; PMID:24123563; http://dx.doi.org/10.1002/erv.2264
33. Sanghez V, Razzoli M, Carobbio S, Campbell M, McCallum J, Cero C, Ceresini G, Cabassi A, Govoni P, Franceschini P, et al. Psychosocial stress induces hyperphagia and exacerbates diet-induced insulin resistance and the manifestations of the Metabolic Syndrome. Psychoneuroendocrinology 2013; 38:2933-42; PMID:24060458; http://dx.doi.org/10.1016/j.psyneuen.2013.07.022
34. Krahn DD, Gosnell BA, Grace M, Levine AS. CRF antagonist partially reverses CRF-and stress-induced effects on feeding. Brain Res Bull 1986; 17:285-9; PMID:3490298; http://dx.doi.org/10.1016/0361-9230(86)90233-9
35. Lau C, Simpson C. Animal models for the study of the effect of prolonged stress on lactation in rats. Physiol Behav 2004; 82:193-7; PMID:15276780; http://dx.doi.org/10.1016/j.physbeh.2004.05.004
36. Aguggia JP, Suárez MM, Rivarola MA. Early maternal separation: neurobehavioral consequences in mother rats. Behav Brain Res 2013; 248:25-31; PMID:23567892; http://dx.doi.org/10.1016/j.bbr.2013.03.040
37. Goyal N, Shukla G. Probiotic Lactobacillus rhamnosus GG modulates the mucosal immune response in Giardia intestinalis-infected BALB/c mice. Dig Dis Sci 2013; 58:1218-25; PMID:23263901; http://dx.doi.org/10.1007/s10620-012-2503-y
38. Thomas CM, Hong T, van Pijkeren JP, Hemarajata P, Trinh DV, Hu W, Britton RA, Kalkum M, Versalovic J. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One 2012; 7:e31951; PMID:22384111; http://dx.doi.org/10.1371/journal.pone.0031951
39. Mackos AR, Eubank TD, Parry NM, Bailey MT. Probiotic Lactobacillus reuteri attenuates the stressor-enhanced severity of Citrobacter rodentium infection. Infect Immun 2013; 81:3253-63; PMID:23798531; http://dx.doi.org/10.1128/IAI.00278-13
40. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, Kubo C, Koga Y. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558:263-75; PMID:15133062; http://dx.doi.org/10.1113/jphysiol.2004.063388
41. Padgett DA, Glaser R. How stress influences the immune response. Trends Immunol 2003; 24:444-8; PMID:12909458; http://dx.doi.org/10.1016/S1471-4906(03)00173-X
42. Reber SO, Birkeneder L, Veenema AH, Obermeier F, Falk W, Straub RH, Neumann ID. Adrenal insufficiency and colonic inflammation after a novel chronic psycho-social stress paradigm in mice: implications and mechanisms. Endocrinology 2007; 148:670-82; PMID:17110427; http://dx.doi.org/10.1210/en.2006-0983
43. Barouei J, Moussavi M, Hodgson DM. Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. PLoS One 2012; 7:e46051; PMID:23071537; http://dx.doi.org/10.1371/journal.pone.0046051
44. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010; 170:1179-88; PMID:20696216; http://dx.doi.org/10.1016/j.neuroscience.2010.08.005
45. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, Bisson JF, Rougeot C, Pichelin M, Cazaubiel M, et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 2011; 105:755-64; PMID:20974015; http://dx.doi.org/10.1017/S0007114510004319
46. Bernstein CN, Singh S, Graff LA, Walker JR, Miller N, Cheang M. A prospective population-based study of triggers of symptomatic flares in IBD. Am J Gastroenterol 2010; 105:1994-2002; PMID:20372115; http://dx.doi.org/10.1038/ajg.2010.140
47. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Doré J. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 2009; 15:1183-9; PMID:19235886; http://dx.doi.org/10.1002/ibd.20903
48. Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, Ballet V, Claes K, Van Immerseel F, Verbeke K, et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 2013; PMID:24021287; http://dx.doi.org/10.1136/gutjnl-2013-304833
49. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 2008; 105:16731-6; PMID:18936492; http://dx.doi.org/10.1073/pnas.0804812105
50. Martín R, Chain F, Miquel S, Lu J, Gratadoux JJ, Sokol H, Verdu EF, Bercik P, Bermúdez-Humarán LG, Langella P. The commensal bacterium Faecalibacterium prausnitzii is protective in DNBS-induced chronic moderate and severe colitis models. Inflamm Bowel Dis 2014; 20:417-30; http://dx.doi.org/10.1097/01.MIB.0000440815.76627.64; PMID:24418903
51. Söderholm JD, Yates DA, Gareau MG, Yang PC, MacQueen G, Perdue MH. Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. Am J Physiol Gastrointest Liver Physiol 2002; 283:G1257-63; PMID:12388189
52. Maslanik T, Tannura K, Mahaffey L, Loughridge AB, Benninson L, Ursell L, Greenwood BN, Knight R, Fleshner M. Commensal bacteria and MAMPs are necessary for stress-induced increases in IL-1β and IL-18 but not IL-6, IL-10 or MCP-1. PLoS One 2012; 7:e50636; PMID:23236381; http://dx.doi.org/10.1371/journal.pone.0050636
53. Allen RG, Lafuse WP, Galley JD, Ali MM, Ahmer BM, Bailey MT. The intestinal microbiota are necessary for stressor-induced enhancement of splenic macrophage microbicidal activity. Brain Behav Immun 2012; 26:371-82; PMID:22100833; http://dx.doi.org/10.1016/j.bbi.2011.11.002
54. Abrams GD, Bishop JE. Effect of the normal microbial flora on gastrointestinal motility. Proc Soc Exp Biol Med 1967; 126:301-4; PMID:6066182; http://dx.doi.org/10.3181/00379727-126-32430
55. Caenepeel P, Janssens J, Vantrappen G, Eyssen H, Coremans G. Interdigestive myoelectric complex in germ-free rats. Dig Dis Sci 1989; 34:1180-4; PMID:2752868; http://dx.doi.org/10.1007/BF01537265
56. Anitha M, Vijay-Kumar M, Sitaraman SV, Gewirtz AT, Srinivasan S. Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling. Gastroenterology 2012; 143:1006-16, e4; PMID:22732731; http://dx.doi.org/10.1053/j.gastro.2012.06.034
57. Uribe A, Alam M, Johansson O, Midtvedt T, Theodorsson E. Microflora modulates endocrine cells in the gastrointestinal mucosa of the rat. Gastroenterology 1994; 107:1259-69; PMID:7926490; http://dx.doi.org/10.1016/0016-5085(94)90526-6
58. Crouzet L, Gaultier E, Del'Homme C, Cartier C, Delmas E, Dapoigny M, Fioramonti J, Bernalier-Donadille A. The hypersensitivity to colonic distension of IBS patients can be transferred to rats through their fecal microbiota. Neurogastroenterol Motil 2013; 25:e272-82; PMID:23433203; http://dx.doi.org/10.1111/nmo.12103
59. Amaral FA, Sachs D, Costa VV, Fagundes CT, Cisalpino D, Cunha TM, Ferreira SH, Cunha FQ, Silva TA, Nicoli JR, et al. Commensal microbiota is fundamental for the development of inflammatory pain. Proc Natl Acad Sci U S A 2008; 105:2193-7; PMID:18268332; http://dx.doi.org/10.1073/pnas.0711891105
60. Petersson J, Schreiber O, Hansson GC, Gendler SJ, Velcich A, Lundberg JO, Roos S, Holm L, Phillipson M. Importance and regulation of the colonic mucus barrier in a mouse model of colitis. Am J Physiol Gastrointest Liver Physiol 2011; 300:G327-33; PMID:21109593; http://dx.doi.org/10.1152/ajpgi.00422.2010
61. Wrzosek L, Miquel S, Noordine ML, Bouet S, Joncquel Chevalier-Curt M, Robert V, Philippe C, Bridonneau C, Cherbuy C, Robbe-Masselot C, et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol 2013; 11:61; PMID:23692866; http://dx.doi.org/10.1186/1741-7007-11-61
62. Guo S, Gao Q, Jiao Q, Hao W, Gao X, Cao JM. Gastric mucosal damage in water immersion stress: mechanism and prevention with GHRP-6. World J Gastroenterol 2012; 18:3145-55; PMID:22791951; http://dx.doi.org/10.3748/wjg.v18.i24.3145
63. Castagliuolo I, Lamont JT, Qiu B, Fleming SM, Bhaskar KR, Nikulasson ST, Kornetsky C, Pothoulakis C. Acute stress causes mucin release from rat colon: role of corticotropin releasing factor and mast cells. Am J Physiol 1996; 271:G884-92; PMID:8944704
64. Reyna-Garfias H, Miliar A, Jarillo-Luna A, Rivera-Aguilar V, Pacheco-Yepez J, Baeza I, Campos-Rodríguez R. Repeated restraint stress increases IgA concentration in rat small intestine. Brain Behav Immun 2010; 24:110-8; PMID:19748568; http://dx.doi.org/10.1016/j.bbi.2009.09.005
65. Lewis K, Caldwell J, Phan V, Prescott D, Nazli A, Wang A, Soderhölm JD, Perdue MH, Sherman PM, McKay DM. Decreased epithelial barrier function evoked by exposure to metabolic stress and nonpathogenic E. coli is enhanced by TNFα. Am J Physiol Gastrointest Liver Physiol 2008; 294:G669-78; PMID:18187519; http://dx.doi.org/10.1152/ajpgi.00382.2007
66. Allen RG, Lafuse WP, Powell ND, Webster Marketon JI, Stiner-Jones LM, Sheridan JF, Bailey MT. Stressor-induced increase in microbicidal activity of splenic macrophages is dependent upon peroxynitrite production. Infect Immun 2012; 80:3429-37; PMID:22825446; http://dx.doi.org/10.1128/IAI.00714-12