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Volume 164, Issue 2

Galactooligosaccharide supplementation provides protection against -induced colitis without limiting pathogen burden Free

Abstract

Many enteric pathogens, including and enteropathogenic and enterohemorrhagic , express adhesins that recognize and bind to carbohydrate moieties expressed on epithelial cells. An attractive strategy for inhibiting bacterial adherence employs molecules that mimic these epithelial binding sites. Prebiotic oligosaccharides are non-digestible, fermentable fibres capable of modulating the gut microbiota. Moreover, they may act as molecular decoys that competitively inhibit adherence of pathogens to host cells. In particular, galactooligosaccharides (GOS) and other prebiotic fibres have been shown to inhibit pathogen adherence to epithelial cells . In the present study, we determined the ability of prophylactic GOS administration to reduce enteric pathogen adherence both and as well as protect against intestinal inflammation. GOS supplementation significantly reduced the adherence of the epithelial-adherent murine bacterial pathogen in a dose-dependent manner to the surface of epithelial cells A 1- to 2-log reduction in bacterial adherence was observed at the lowest and highest doses tested, respectively. However, mouse studies revealed that treatment with GOS neither reduced the adherence of to the distal colon nor decreased its dissemination to systemic organs. Despite the absence of adherence inhibition, colonic disease scores for GOS-treated, -infected mice were significantly lower than those of untreated -infected animals (=0.028). Together, these data suggest that GOS has a direct protective effect in ameliorating disease severity following infection through an anti-adherence-independent mechanism.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): anti-adherence , Citrobacter rodentium , conventionally-raised mice , gastrointestinal inflammation and prebiotics
© 2018 The Authors
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2018-02-01
2024-04-23
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References

  1. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 2017; 14:491–502 [View Article][PubMed]
     [Google Scholar]
  2. Gänzle MG. Enzymatic synthesis of galacto-oligosaccharides and other lactose derivatives (hetero-oligosaccharides) from lactose. Int Dairy J 2012; 22:116–122 [View Article]
     [Google Scholar]
  3. Bouhnik Y, Flourié B, D'Agay-Abensour L, Pochart P, Gramet G et al. Administration of transgalacto-oligosaccharides increases fecal bifidobacteria and modifies colonic fermentation metabolism in healthy humans. J Nutr 1997; 127:444–448[PubMed]
     [Google Scholar]
  4. Davis LM, Martínez I, Walter J, Goin C, Hutkins RW. Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS One 2011; 6:e25200 [View Article][PubMed]
     [Google Scholar]
  5. Vulevic J, Juric A, Walton GE, Claus SP, Tzortzis G et al. Influence of galacto-oligosaccharide mixture (B-GOS) on gut microbiota, immune parameters and metabonomics in elderly persons. Br J Nutr 2015; 114:586–595 [View Article][PubMed]
     [Google Scholar]
  6. Azcarate-Peril MA, Ritter AJ, Savaiano D, Monteagudo-Mera A, Anderson C et al. Impact of short-chain galactooligosaccharides on the gut microbiome of lactose-intolerant individuals. Proc Natl Acad Sci USA 2017; 114:E367E375 [View Article][PubMed]
     [Google Scholar]
  7. Wu S, Grimm R, German JB, Lebrilla CB. Annotation and structural analysis of sialylated human milk oligosaccharides. J Proteome Res 2011; 10:856–868 [View Article][PubMed]
     [Google Scholar]
  8. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 2006; 40:235–243 [View Article][PubMed]
     [Google Scholar]
  9. van Immerseel F, de Buck J, Pasmans F, Velge P, Bottreau E et al. Invasion of Salmonella enteritidis in avian intestinal epithelial cells in vitro is influenced by short-chain fatty acids. Int J Food Microbiol 2003; 85:237–248 [View Article][PubMed]
     [Google Scholar]
  10. Holmes E, Li JV, Marchesi JR, Nicholson JK. Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. Cell Metab 2012; 16:559–564 [View Article][PubMed]
     [Google Scholar]
  11. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 2012; 3:289–306 [View Article][PubMed]
     [Google Scholar]
  12. Defoirdt T, Halet D, Sorgeloos P, Bossier P, Verstraete W. Short-chain fatty acids protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii . Aquaculture 2006; 261:804–808 [View Article]
     [Google Scholar]
  13. Tejero-Sariñena S, Barlow J, Costabile A, Gibson GR, Rowland I. In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe 2012; 18:530–538 [View Article][PubMed]
     [Google Scholar]
  14. Shoaf‐sweeney KD, Hutkins RW. Adherence, anti‐adherence, and oligosaccharides: preventing pathogens from sticking to the host. Adv Food Nutr Res 2008; 55:101–161 [Crossref]
     [Google Scholar]
  15. Quintero M, Maldonado M, Perez-Munoz M, Jimenez R, Fangman T et al. Adherence inhibition of Cronobacter sakazakii to intestinal epithelial cells by prebiotic oligosaccharides. Curr Microbiol 2011; 62:1448–1454 [View Article][PubMed]
     [Google Scholar]
  16. Quintero-Villegas MI, Aam BB, Rupnow J, Sørlie M, Eijsink VG et al. Adherence inhibition of enteropathogenic Escherichia coli by chitooligosaccharides with specific degrees of acetylation and polymerization. J Agric Food Chem 2013; 61:2748–2754 [View Article][PubMed]
     [Google Scholar]
  17. Kisiela D, Laskowska A, Sapeta A, Kuczkowski M, Wieliczko A et al. Functional characterization of the FimH adhesin from Salmonella enterica serovar Enteritidis. Microbiology 2006; 152:1337–1346 [View Article][PubMed]
     [Google Scholar]
  18. Cleary J, Lai LC, Shaw RK, Straatman-Iwanowska A, Donnenberg MS et al. Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 2004; 150:527–538 [View Article][PubMed]
     [Google Scholar]
  19. Shoaf K, Mulvey GL, Armstrong GD, Hutkins RW. Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells. Infect Immun 2006; 74:6920–6928 [View Article][PubMed]
     [Google Scholar]
  20. Neeser JR, Koellreutter B, Wuersch P. Oligomannoside-type glycopeptides inhibiting adhesion of Escherichia coli strains mediated by type 1 pili: preparation of potent inhibitors from plant glycoproteins. Infect Immun 1986; 52:428–436[PubMed]
     [Google Scholar]
  21. Firon N, Ofek I, Sharon N. Interaction of mannose-containing oligosaccharides with the fimbrial lectin of Escherichia coli . Biochem Biophys Res Commun 1982; 105:1426–1432 [View Article][PubMed]
     [Google Scholar]
  22. Rodrigues DM, Sousa AJ, Johnson-Henry KC, Sherman PM, Gareau MG. Probiotics are effective for the prevention and treatment of Citrobacter rodentium-induced colitis in mice. J Infect Dis 2012; 206:99–109 [View Article][PubMed]
     [Google Scholar]
  23. Chao AW, Bhatti M, Dupont HL, Nataro JP, Carlin LG et al. Clinical features and molecular epidemiology of diarrheagenic Escherichia coli pathotypes identified by fecal gastrointestinal multiplex nucleic acid amplification in patients with cancer and diarrhea. Diagn Microbiol Infect Dis 2017; 89:235–240 [View Article][PubMed]
     [Google Scholar]
  24. Izquierdo M, Navarro-Garcia F, Nava-Acosta R, Nataro JP, Ruiz-Perez F et al. Identification of cell surface-exposed proteins involved in the fimbria-mediated adherence of enteroaggregative Escherichia coli to intestinal cells. Infect Immun 2014; 82:1719–1724 [View Article][PubMed]
     [Google Scholar]
  25. Kudva IT, Krastins B, Torres AG, Griffin RW, Sheng H et al. The Escherichia coli O157:H7 cattle immunoproteome includes outer membrane protein A (OmpA), a modulator of adherence to bovine rectoanal junction squamous epithelial (RSE) cells. Proteomics 2015; 15:1829–1842 [View Article][PubMed]
     [Google Scholar]
  26. Kudva IT, Carter MQ, Sharma VK, Stasko JA, Giron JA. Curli temper adherence of Escherichia coli O157:H7 to squamous epithelial cells from the bovine recto-anal junction in a strain-dependent manner. Appl Environ Microbiol 2017; 83:e02594-16 [View Article][PubMed]
     [Google Scholar]
  27. Larzábal M, Zotta E, Ibarra C, Rabinovitz BC, Vilte DA et al. Effect of coiled-coil peptides on the function of the type III secretion system-dependent activity of enterohemorragic Escherichia coli O157:H7 and Citrobacter rodentium . Int J Med Microbiol 2013; 303:9–15 [View Article][PubMed]
     [Google Scholar]
  28. Johnson-Henry KC, Pinnell LJ, Waskow AM, Irrazabal T, Martin A et al. Short-chain fructo-oligosaccharide and inulin modulate inflammatory responses and microbial communities in Caco2-bbe cells and in a mouse model of intestinal injury. J Nutr 2014; 144:1725–1733 [View Article][PubMed]
     [Google Scholar]
  29. Mundy R, Macdonald TT, Dougan G, Frankel G, Wiles S. Citrobacter rodentium of mice and man. Cell Microbiol 2005; 7:1697–1706 [View Article][PubMed]
     [Google Scholar]
  30. Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 1998; 66:5224–5231[PubMed]
     [Google Scholar]
  31. Jergens AE, Dorn A, Wilson J, Dingbaum K, Henderson A et al. Induction of differential immune reactivity to members of the flora of gnotobiotic mice following colonization with Helicobacter bilis or Brachyspira hyodysenteriae . Microbes Infect 2006; 8:1602–1610 [View Article][PubMed]
     [Google Scholar]
  32. Maaser C, Housley MP, Iimura M, Smith JR, Vallance BA et al. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect Immun 2004; 72:3315–3324 [View Article][PubMed]
     [Google Scholar]
  33. Rathinam VA, Vanaja SK, Waggoner L, Sokolovska A, Becker C et al. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 2012; 150:606–619 [View Article][PubMed]
     [Google Scholar]
  34. Lebeis SL, Bommarius B, Parkos CA, Sherman MA, Kalman D. TLR signaling mediated by MyD88 is required for a protective innate immune response by neutrophils to Citrobacter rodentium . J Immunol 2007; 179:566–577 [View Article][PubMed]
     [Google Scholar]
  35. Kayagaki N, Warming S, Lamkanfi M, vande Walle L, Louie S et al. Non-canonical inflammasome activation targets caspase-11. Nature 2011; 479:117–121 [View Article][PubMed]
     [Google Scholar]
  36. Gibson DL, Ma C, Bergstrom KS, Huang JT, Man C et al. 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 2008; 10:618–631 [View Article][PubMed]
     [Google Scholar]
  37. Dann SM, Spehlmann ME, Hammond DC, Iimura M, Hase K et al. IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens. J Immunol 2008; 180:6816–6826 [View Article][PubMed]
     [Google Scholar]
  38. Alipour M, Lou Y, Zimmerman D, Bording-Jorgensen MW, Sergi C et al. A balanced IL-1β activity is required for host response to Citrobacter rodentium infection. PLoS One 2013; 8:e80656 [View Article][PubMed]
     [Google Scholar]
  39. Hall LJ, Murphy CT, Hurley G, Quinlan A, Shanahan F et al. Natural killer cells protect against mucosal and systemic infection with the enteric pathogen Citrobacter rodentium . Infect Immun 2013; 81:460–469 [View Article][PubMed]
     [Google Scholar]
  40. Wei OL, Hilliard A, Kalman D, Sherman M. Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium . Infect Immun 2005; 73:1978–1985 [View Article][PubMed]
     [Google Scholar]
  41. Medzhitov R, Schneider DS, Soares MP. Disease tolerance as a defense strategy. Science 2012; 335:936–941 [View Article][PubMed]
     [Google Scholar]
  42. Simms EL. Defining tolerance as a norm of reaction. Evol Ecol 2000; 14:563–570 [View Article]
     [Google Scholar]
  43. Schneider DS, Ayres JS. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol 2008; 8:889–895 [View Article][PubMed]
     [Google Scholar]
  44. Smith AD, Yan X, Chen C, Dawson HD, Bhagwat AA. Understanding the host-adapted state of Citrobacter rodentium by transcriptomic analysis. Arch Microbiol 2016; 198:353–362 [View Article][PubMed]
     [Google Scholar]
  45. Petersen A, Heegaard PM, Pedersen AL, Andersen JB, Sørensen RB et al. Some putative prebiotics increase the severity of Salmonella enterica serovar Typhimurium infection in mice. BMC Microbiol 2009; 9:245 [View Article][PubMed]
     [Google Scholar]
  46. Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, van der Meer R. Dietary fructooligosaccharides increase intestinal permeability in rats. J Nutr 2005; 135:837–842[PubMed] [Crossref]
     [Google Scholar]
  47. Cani PD, Possemiers S, van de Wiele T, Guiot Y, Everard A et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009; 58:1091–1103 [View Article][PubMed]
     [Google Scholar]
  48. Neyrinck AM, van Hée VF, Piront N, de Backer F, Toussaint O et al. Wheat-derived arabinoxylan oligosaccharides with prebiotic effect increase satietogenic gut peptides and reduce metabolic endotoxemia in diet-induced obese mice. Nutr Diabetes 2012; 2:e28 [View Article][PubMed]
     [Google Scholar]
  49. Bindels LB, Neyrinck AM, Claus SP, Le Roy CI, Grangette C et al. Synbiotic approach restores intestinal homeostasis and prolongs survival in leukaemic mice with cachexia. Isme J 2016; 10:1456–1470 [View Article][PubMed]
     [Google Scholar]
  50. Krumbeck JA, Maldonado-Gomez MX, Martínez I, Frese SA, Burkey TE et al. In vivo selection to identify bacterial strains with enhanced ecological performance in synbiotic applications. Appl Environ Microbiol 2015; 81:2455–2465 [View Article][PubMed]
     [Google Scholar]
  51. Monteagudo-Mera A, Arthur JC, Jobin C, Keku T, Bruno-Barcena JM et al. High purity galacto-oligosaccharides enhance specific Bifidobacterium species and their metabolic activity in the mouse gut microbiome. Benef Microbes 2016; 7:247–264 [View Article][PubMed]
     [Google Scholar]
  52. Qamar TR, Iqbal S, Syed F, Nasir M, Rehman H et al. Impact of novel prebiotic galacto-oligosaccharides on various biomarkers of colorectal cancer in wister rats. Int J Mol Sci 2017; 18:E1785 [View Article][PubMed]
     [Google Scholar]
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Galactooligosaccharide supplementation provides protection against Citrobacter rodentium-induced colitis without limiting pathogen burden
Microbiology 164, 154 (2018); https://doi.org/10.1099/mic.0.000593
/content/journal/micro/10.1099/mic.0.000593
/content/journal/micro/10.1099/mic.0.000593
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