Crohn's Disease-Associated Adherent-Invasive Escherichia coli Adhesion Is Enhanced by Exposure to the Ubiquitous Dietary Polysaccharide Maltodextrin

被引:106
|
作者
Nickerson, Kourtney P. [1 ,2 ]
McDonald, Christine [1 ,2 ]
机构
[1] Cleveland Clin, Lerner Res Inst, Dept Pathobiol, Cleveland, OH 44106 USA
[2] Case Western Reserve Univ, Dept Mol Med, Cleveland Clin Lerner Coll Med, Cleveland, OH 44106 USA
来源
PLOS ONE | 2012年 / 7卷 / 12期
基金
美国国家卫生研究院;
关键词
INFLAMMATORY-BOWEL-DISEASE; GUT MICROBIOME; MUCOSAL FLORA; ILEAL MUCOSA; E; COLI; BIOFILM FORMATION; GROWTH; EPIDEMIOLOGY; DIVERSITY; TRANSPORT;
D O I
10.1371/journal.pone.0052132
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Crohn's disease (CD) is associated with intestinal dysbiosis evidenced by an altered microbiome forming thick biofilms on the epithelium. Additionally, adherent-invasive E. coli (AIEC) strains are frequently isolated from ileal lesions of CD patients indicating a potential role for these strains in disease pathogenesis. The composition and characteristics of the host microbiome are influenced by environmental factors, particularly diet. Polysaccharides added to food as emulsifiers, stabilizers or bulking agents have been linked to bacteria-associated intestinal disorders. The escalating consumption of polysaccharides in Western diets parallels an increased incidence of CD during the latter 20th century. In this study, the effect of a polysaccharide panel on adhesiveness of the CD-associated AIEC strain LF82 was analyzed to determine if these food additives promote disease-associated bacterial phenotypes. Maltodextrin (MDX), a polysaccharide derived from starch hydrolysis, markedly enhanced LF82 specific biofilm formation. Biofilm formation of multiple other E. coli strains was also promoted by MDX. MDX-induced E. coli biofilm formation was independent of polysaccharide chain length indicating a requirement for MDX metabolism. MDX exposure induced type I pili expression, which was required for MDX-enhanced biofilm formation. MDX also increased bacterial adhesion to human intestinal epithelial cell monolayers in a mechanism dependent on type 1 pili and independent of the cellular receptor CEACAM6, suggesting a novel mechanism of epithelial cell adhesion. Analysis of mucosa-associated bacteria from individuals with and without CD showed increased prevalence of malX, a gene essential for MDX metabolism, uniquely in the ileum of CD patients. These findings demonstrate that the ubiquitous dietary component MDX enhances E. coli adhesion and suggests a mechanism by which Western diets rich in specific polysaccharides may promote dysbiosis of gut microbes and contribute to disease susceptibility.
引用
收藏
页数:13
相关论文
共 50 条
  • [31] Crohn's disease-associated adherent-invasive Escherichia coli induce secretion of exosomes with pro-inflammatory activity by intestinal epithelial cells
    Carriere, J.
    Bretin, A.
    Barnich, N.
    Nguyen, H. T. T.
    JOURNAL OF CROHNS & COLITIS, 2015, 9 : S110 - S110
  • [32] Comparison of Crohn's disease-associated adherent-invasive Escherichia coli (AIEC) from France and Hong Kong: results from the Pacific study
    Chevarin, Caroline
    Xu, Zhilu
    Martin, Lucas
    Robin, Frederic
    Beyrouthy, Racha
    Colombel, Jean-Frederic
    Sulakvelidze, Alexander
    Ng, Siew C.
    Bonnet, Richard
    Buisson, Anthony
    Barnich, Nicolas
    GUT MICROBES, 2024, 16 (01)
  • [33] CHIA: A MAJOR PLAYER IN THE VIRULENCE OF CROHN'S DISEASE-ASSOCIATED ADHERENT AND INVASIVE ESCHERICHIA COLI (AIEC)
    Fargeas, Margot
    Faure, Frederic
    Douadi, Clara
    Billard, Elisabeth
    Denizot, Jeremy
    Buisson, Anthony
    Barnich, Nicolas
    GASTROENTEROLOGY, 2024, 166 (05) : S559 - S559
  • [34] Crohn's disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly
    Lapaquette, Pierre
    Glasser, Anne-Lise
    Huett, Alan
    Xavier, Ramnik J.
    Darfeuille-Michaud, Arlette
    CELLULAR MICROBIOLOGY, 2010, 12 (01) : 99 - 113
  • [35] ChiA: a major player in the virulence of Crohn's disease-associated adherent and invasive Escherichia coli (AIEC)
    Fargeas, Margot
    Faure, Frederic
    Douadi, Clara
    Chevarin, Caroline
    Birer, Aurelien
    Sivignon, Adeline
    Rodrigues, Michael
    Denizot, Jeremy
    Billard, Elisabeth
    Barnich, Nicolas
    Buisson, Anthony
    GUT MICROBES, 2024, 16 (01)
  • [36] Bile salts induce long polar fimbriae expression favouring Crohn's disease-associated adherent-invasive Escherichia coli interaction with Peyer's patches
    Chassaing, Benoit
    Etienne-Mesmin, Lucie
    Bonnet, Richard
    Darfeuille-Michaud, Arlette
    ENVIRONMENTAL MICROBIOLOGY, 2013, 15 (02) : 355 - 371
  • [37] uvrY Deletion and Acetate Reduce Gut Colonization of Crohn's Disease-Associated Adherent-Invasive Escherichia coli by Decreasing Expression of Type 1 Fimbriae
    Miki, Tsuyoshi
    Hoshino, Yusuke
    Sudo, Naoki
    Ito, Masahiro
    Haneda, Takeshi
    Okada, Nobuhiko
    INFECTION AND IMMUNITY, 2022, 90 (03)
  • [38] An Intestinal Th17 Subset is Associated with Inflammation in Crohn's Disease and Activated by Adherent-invasive Escherichia coli
    Paroni, Moira
    Leccese, Gabriella
    Ranzani, Valeria
    Moschetti, Giorgia
    Chiara, Matteo
    Perillo, Federica
    Ferri, Sara
    Clemente, Francesca
    Noviello, Daniele
    Conforti, Francesco Simone
    Ferrero, Stefano
    Karnani, Bhavna
    Bosotti, Roberto
    Vasco, Chiara
    Curti, Serena
    Crosti, Maria Cristina
    Gruarin, Paola
    Rossetti, Grazisa
    Conte, Maria Pia
    Vecchi, Maurizio
    Pagani, Massimiliano
    Landini, Paolo
    Facciotti, Federica
    Abrignani, Sergio
    Caprioli, Flavio
    Geginat, Jens
    JOURNAL OF CROHNS & COLITIS, 2023, 17 (12): : 1988 - 2001
  • [39] Animals as putative source of Adherent-Invasive Escherichia coli (AIEC) - a group of pathogens associated with Crohn's disease in humans
    Martinez-Medina, M.
    Garcia-Gil, J.
    Barnich, N.
    Wieler, L. H.
    Ewers, C.
    INTERNATIONAL JOURNAL OF MEDICAL MICROBIOLOGY, 2011, 301 : 118 - 118
  • [40] Bile Salts Induce Long Polar Fimbriae Expression and Favour Crohn's Disease-Associated Adherent-Invasive Escherichia coli Interaction With Peyer's Patches
    Chassaing, Benoit
    Darfeuille-Michaud, Arlette
    GASTROENTEROLOGY, 2012, 142 (05) : S673 - S674