Effect of Maternal Probiotic Intervention on HPA Axis, Immunity and Gut Microbiota in a Rat Model of Irritable Bowel Syndrome

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Barouei, Javad ^a,b   Moussavi, Mahta ^a,b   Hodgson, Deborah M ^b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; IMMUNOGLOBULIN A; PROBIOTIC AGENT;

AEROBIC BACTERIUM; ANAEROBIC BACTERIUM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COUNT; BIFIDOBACTERIUM ANIMALIS; BLOOD SAMPLING; CLOSTRIDIA; CONTROLLED STUDY; EARLY LIFE STRESS; ENTEROCOCCUS; ESCHERICHIA COLI; FEMALE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; INTESTINE FLORA; IRRITABLE COLON; MALE; MATERNAL DEPRIVATION; NEONATAL STRESS; NEWBORN; NONHUMAN; PROPIONIBACTERIUM; PROPIONIBACTERIUM JENSENII; RAT;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; ANIMALS, NEWBORN; BASE SEQUENCE; BIFIDOBACTERIUM; CORTICOSTERONE; DNA PRIMERS; FEMALE; IMMUNOGLOBULIN A; INTESTINES; MALE; PROBIOTICS; PROPIONIBACTERIUM; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84867422607     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046051     Document Type: Article

References (70)

1. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, et al. (2009) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12: 1559-1566.
2. Gareau MG, Silva MA, Perdue MH, (2008) Pathophysiological mechanisms of stress-induced intestinal damage. Curr Mol Med 8: 274-281.
3. O'Mahony SM, Hyland NP, Dinan TG, Cryan JF, (2011) Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl) 214: 71-88.
4. Barreau F, Ferrier L, Fioramonti J, Bueno L, (2007) New insights in the etiology and pathophysiology of irritable bowel syndrome: contribution of neonatal stress models. Pediatr Res 62: 240-245.
5. O'Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, et al. (2009) Early Life Stress Alters Behavior, Immunity, and Microbiota in Rats: Implications for Irritable Bowel Syndrome and Psychiatric Illnesses. Biol Psychiatry pp. 263-267.
6. Gareau MG, Jury J, MacQueen G, Sherman PM, Perdue MH, (2007) Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 56: 1522-1528.
7. 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.
8. Barreau F, Cartier C, Leveque M, Ferrier L, Moriez R, et al. (2007) Pathways involved in gut mucosal barrier dysfunction induced in adult rats by maternal deprivation: corticotrophin-releasing factor and nerve growth factor interplay. J Physiol 580: 347-356.
9. Soderholm JD, Yates DA, Gareau MG, Yang PC, MacQueen G, et al. (2002) Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. Am J Physiol Gastrointest Liver Physiol 283: G1257-1263.
10. Gareau MG, Jury J, Perdue MH, (2007) Neonatal maternal separation of rat pups results in abnormal cholinergic regulation of epithelial permeability. Am J Physiol Gastrointest Liver Physiol 293: G198-203.
11. Barreau F, Cartier C, Ferrier L, Fioramonti J, Bueno L, (2004) Nerve growth factor mediates alterations of colonic sensitivity and mucosal barrier induced by neonatal stress in rats. Gastroenterology 127: 524-534.
12. Garcia-Rodenas CL, Bergonzelli GE, Nutten S, Schumann A, Cherbut C, et al. (2006) Nutritional approach to restore impaired intestinal barrier function and growth after neonatal stress in rats. J Pediatr Gastroenterol Nutr 43: 16-24.
13. Barreau F, Ferrier L, Fioramonti J, Bueno L, (2004) Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut 53: 501-506.
14. 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: 114-122.
15. Bailey MT, Coe CL, (1999) Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35: 146-155.
16. Schwetz I, McRoberts JA, Coutinho SV, Bradesi S, Gale G, et al. (2005) Corticotropin-releasing factor receptor 1 mediates acute and delayed stress-induced visceral hyperalgesia in maternally separated Long-Evans rats. Am J Physiol Gastrointest Liver Physiol 289: G704-712.
17. Coutinho SV, Plotsky PM, Sablad M, Miller JC, Zhou H, et al. (2002) Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat. Am J Physiol Gastrointest Liver Physiol 282: G307-316.
18. Rosztoczy A, Fioramonti J, Jarmay K, Barreau F, Wittmann T, et al. (2003) Influence of sex and experimental protocol on the effect of maternal deprivation on rectal sensitivity to distension in the adult rat. Neurogastroenterol Motil 15: 679-686.
19. Buddington RK, Williams CH, Kostek BM, Buddington KK, Kullen MJ, (2010) Maternal-to-infant transmission of probiotics: concept validation in mice, rats, and pigs. Neonatology 97: 250-256.
20. Gueimonde M, Sakata S, Kalliomaki M, Isolauri E, Benno Y, et al. (2006) Effect of maternal consumption of lactobacillus GG on transfer and establishment of fecal bifidobacterial microbiota in neonates. J Pediatr Gastroenterol Nutr 42: 166-170.
21. Schultz M, Gottl C, Young RJ, Iwen P, Vanderhoof JA, (2004) Administration of oral probiotic bacteria to pregnant women causes temporary infantile colonization. J Pediatr Gastroenterol Nutr 38: 293-297.
22. Vanderhoof JA, Iwen P, Hinrichs SH, Bilyeu DV, Young RJ, (1999) Colonization of an Infant with the Probiotic, Lactobacillus GG, by Maternal Transmission. Pediatr Res 45: 118A.
23. Sudo N, (2006) Stress and gut microbiota: Does postnatal microbial colonization programs the hypothalamic-pituitaryadrenal system for stress response? International Congress Series 1287: 350-354.
24. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, et al. (2004) Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 558: 263-275.
25. Blumer N, Sel S, Virna S, Patrascan CC, Zimmermann S, et al. (2007) Perinatal maternal application of Lactobacillus rhamnosus GG suppresses allergic airway inflammation in mouse offspring. Clin Exp Allergy 37: 348-357.
26. Rautava S, Kalliomaki M, Isolauri E, (2002) Probiotics during pregnancy and breast-feeding might confer immunomodulatory protection against atopic disease in the infant. J Allergy Clin Immunol 109: 119-121.
27. Simren M, Ohman L, Olsson J, Svensson U, Ohlson K, et al. (2009) Clinical trial: the effects of a fermented milk containing three probiotic bacteria in patients with irritable bowel syndrome- a randomized, double-blind, controlled study. Aliment Pharmacol Ther 31: 218-227.
28. Kajander K, Myllyluoma E, Rajilic-Stojanovic M, Kyronpalo S, Rasmussen M, et al. (2008) Clinical trial: multispecies probiotic supplementation alleviates the symptoms of irritable bowel syndrome and stabilizes intestinal microbiota. Aliment Pharmacol Ther 27: 48-57.
29. Kotula L (2008) Application of a probiotic bacterium Propionibacterium jensenii 702 for human consumption. PhD Thesis, the University of Newcastle, Newcastle, Australia.
30. Moussavi M, Adams MC, (2010) An in vitro study on bacterial growth interactions and intestinal epithelial cell adhesion characteristics of probiotic combinations. Curr Microbiol 60: 327-335.
31. Walker AK, Nakamura T, Hodgson DM, (2010) Neonatal lipopolysaccharide exposure alters central cytokine responses to stress in adulthood in Wistar rats. Stress 13: 506-515.
32. Malik AC, Reinbold GW, Vedamuthu ER, (1968) An evaluation of the taxonomy of Propionibacterium. Can J Microbiol 14: 1185-1191.
33. Walker AK, Nakamura T, Byrne RJ, Naicker S, Tynan RJ, et al. (2009) Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: implications for the double-hit hypothesis. Psychoneuroendocrinology 34: 1515-1525.
34. Kataoka K, Kibe R, Kuwahara T, Hagiwara M, Arimochi H, et al. (2007) Modifying effects of fermented brown rice on fecal microbiota in rats. Anaerobe 13: 220-227.
35. Atlas RM (2004) Handbook of Microbiological Media. 3 ed. Boca Raton: CRC/Taylor & Francis. pp. 219.
36. Welting O, Van Den Wijngaard RM, De Jonge WJ, Holman R, Boeckxstaens GE, (2005) Assessment of visceral sensitivity using radio telemetry in a rat model of maternal separation. Neurogastroenterol Motil 17: 838-845.
37. Julio-Pieper M, O'Mahony CM, Clarke G, Bravo JA, Dinan TG, et al. (2012) Chronic stress-induced alterations in mouse colonic 5-HT and defecation responses are strain dependent. Stress 15: 218-226.
38. Santos J, Saunders PR, Hanssen NP, Yang PC, Yates D, et al. (1999) Corticotropin-releasing hormone mimics stress-induced colonic epithelial pathophysiology in the rat. Am J Physiol 277: G391-399.
39. Israeli E, Hershcovici T, Berenshtein E, Zannineli G, Wengrower D, et al. (2008) The effect of restraint stress on the normal colon and on intestinal inflammation in a model of experimental colitis. Dig Dis Sci 53: 88-94.
40. Liebl C, Panhuysen M, Putz B, Trumbach D, Wurst W, et al. (2009) Gene expression profiling following maternal deprivation: involvement of the brain Renin-Angiotensin system. Front Mol Neurosci 2: 1.
41. Shanks N, Larocque S, Meaney MJ, (1995) Neonatal endotoxin exposure alters the development of the hypothalamic-pituitary-adrenal axis: early illness and later responsivity to stress. J Neurosci 15: 376-384.
42. Galea LA, McEwen BS, Tanapat P, Deak T, Spencer RL, et al. (1997) Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neurosci 81: 689-697.
43. Lin YL, Lin SY, Wang S, (2012) Prenatal lipopolysaccharide exposure increases anxiety-like behaviors and enhances stress-induced corticosterone responses in adult rats. Brain Behav Immun 26: 459-468.
44. Doremus-Fitzwater TL, Varlinskaya EI, Spear LP, (2009) Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol Behav 97: 484-494.
45. Reul JM, Stec I, Wiegers GJ, Labeur MS, Linthorst AC, et al. (1994) Prenatal immune challenge alters the hypothalamic-pituitary-adrenocortical axis in adult rats. J Clin Invest 93: 2600-2607.
46. Dunn AJ (2008) The HPA Axis and the Immune System: A perspective. In: Del Rey A, Chrousos GP, Besedovsky H, editors. The Hypothalamus-Pituitary-Adrenal Axis. Amsterdam: Elsevier. pp. 1-16.
47. Conley ME, Delacroix DL, (1987) Intravascular and mucosal immunoglobulin A: two separate but related systems of immune defense? Ann Intern Med 106: 892-899.
48. Morton HC, Brandtzaeg P, (2001) CD89: the human myeloid IgA Fc receptor. Arch Immunol Ther Exp (Warsz) 49: 217-229.
49. Otten MA, van Egmond M, (2004) The Fc receptor for IgA (FcalphaRI, CD89). Immunol Lett 92: 23-31.
50. van Egmond M, van Garderen E, van Spriel AB, Damen CA, van Amersfoort ES, et al. (2000) FcalphaRI-positive liver Kupffer cells: reappraisal of the function of immunoglobulin A in immunity. Nat Med 6: 680-685.
51. Woof JM, Kerr MA, (2006) The function of immunoglobulin A in immunity. J Pathol 208: 270-282.
52. Levast B, de Monte M, Chevaleyre C, Melo S, Berri M, et al. (2010) Ultra-early weaning in piglets results in low serum IgA concentration and IL17 mRNA expression. Vet Immunol Immunopathol 137: 261-268.
53. Tejada-Simon MV, Lee JH, Ustunol Z, Pestka JJ, (1999) Ingestion of yoghurt containing Lactobacillus acidophilus and Bifidobacterium to potentiate immunoglobulin A responses to cholera toxin in mice. J Dairy Sci 82: 649-660.
54. Herias MV, Hessle C, Telemo E, Midtvedt T, Hanson LA, et al. (1999) Immunomodulatory effects of Lactobacillus plantarum colonizing the intestine of gnotobiotic rats. Clin Exp Immunol 116: 283-290.
55. Ohland CL, Macnaughton WK, (2010) Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol 298: G807-819.
56. Macpherson AJ, Uhr T, (2004) Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303: 1662-1665.
57. Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, et al. (2000) A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288: 2222-2226.
58. Suzuki K, Meek B, Doi Y, Muramatsu M, Chiba T, et al. (2004) Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc Natl Acad Sci U S A 101: 1981-1986.
59. Wira CR, Sandoe CP, Steele MG, (1990) Glucocorticoid regulation of the humoral immune system. I. In vivo effects of dexamethasone on IgA and IgG in serum and at mucosal surfaces. J Immunol 144: 142-146.
60. Campos-Rodriguez R, Quintanar-Stephano A, Jarillo-Luna RA, Oliver-Aguillon G, Ventura-Juarez J, et al. (2006) Hypophysectomy and neurointermediate pituitary lobectomy reduce serum immunoglobulin M (IgM) and IgG and intestinal IgA responses to Salmonella enterica serovar Typhimurium infection in rats. Infect Immun 74: 1883-1889.
61. Kirjavainen PV, Gibson GR, (1999) Healthy gut microflora and allergy: factors influencing development of the microbiota. Ann Med 31: 288-292.
62. Inoue R, Ushida K, (2003) Development of the intestinal microbiota in rats and its possible interactions with the evolution of the luminal IgA in the intestine. FEMS Microbiol Ecol 45: 147-153.
63. Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, et al. (2010) Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 78: 1509-1519.
64. Eutamene H, Lamine F, Chabo C, Theodorou V, Rochat F, et al. (2007) Synergy between Lactobacillus paracasei and Its Bacterial Products to Counteract Stress-Induced Gut Permeability and Sensitivity Increase in Rats. J Nutr 137: 1901-1908.
65. Layton A, McKay L, Williams D, Garrett V, Gentry R, et al. (2006) Development of Bacteroides 16S rRNA gene TaqMan-based real-time PCR assays for estimation of total, human, and bovine fecal pollution in water. Appl Environ Microbiol 72: 4214-4224.
66. Furet JP, Firmesse O, Gourmelon M, Bridonneau C, Tap J, et al. (2009) Comparative assessment of human and farm animal faecal microbiota using real-time quantitative PCR. FEMS Microbiol Ecol 68: 351-362.
67. Delroisse JM, Boulvin AL, Parmentier I, Dauphin RD, Vandenbol M, et al. (2008) Quantification of Bifidobacterium spp. and Lactobacillus spp. in rat fecal samples by real-time PCR. Microbiol Res 163: 663-670.
68. Rinttila T, Kassinen A, Malinen E, Krogius L, Palva A, (2004) Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97: 1166-1177.
69. Huijsdens XW, Linskens RK, Mak M, Meuwissen SG, Vandenbroucke-Grauls CM, et al. (2002) Quantification of bacteria adherent to gastrointestinal mucosa by real-time PCR. J Clin Microbiol 40: 4423-4427.
70. Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, et al. (2002) Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68: 5445-5451.