Regulation of virulence: the rise and fall of gastrointestinal pathogens

Journal of Gastroenterology

Volumn 51, Issue 3, 2016, Pages 195-205

  Kitamoto, Sho ^a   Nagao Kitamoto, Hiroko ^a   Kuffa, Peter ^a   Kamada, Nobuhiko ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Enteric infection; Host immunity; Microbiota; Virulence factor

Indexed keywords

BICARBONATE; FUCOSE; OXYGEN; SHORT CHAIN FATTY ACID; VIRULENCE FACTOR;

BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; BACTERIAL LOAD; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BILE; COMMENSAL; COMMENSALISM; COMPETITIVE ABILITY; ENVIRONMENTAL FACTOR; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; HUMAN; INTESTINE FLORA; MECHANICAL STIMULATION; MICROBIAL POPULATION DYNAMICS; NONHUMAN; OSMOLALITY; OXYGEN TENSION; PH; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; QUORUM SENSING; REGULATORY MECHANISM; REVIEW; VISCOSITY; ENVIRONMENT; GASTROINTESTINAL TRACT; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MECHANOTRANSDUCTION; METABOLISM; MICROBIOLOGY; ORGANISMAL INTERACTION; PHYSIOLOGY; VIRULENCE;

ENVIRONMENT; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; MECHANOTRANSDUCTION, CELLULAR; MICROBIAL INTERACTIONS; VIRULENCE; VIRULENCE FACTORS;

EID: 84959119769     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-015-1141-5     Document Type: Review

References (62)

1. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65 (Epub 2010/03/06).
2. Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr. 2002;22:283–307 (Epub 2002/06/11).
3. Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331(6015):337–41 (Epub 2011/01/06).
4. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009;31(4):677–89 (Epub 2009/10/17).
5. Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139(3):485–98 (Epub 2009/10/20).
6. Kamada N, Chen GY, Inohara N, et al. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol. 2013;14(7):685–90 (Epub 2013/06/20).
7. Kamada N, Seo SU, Chen GY, et al. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13(5):321–35 (Epub 2013/04/27).
8. Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013;13(11):790–801 (Epub 2013/10/08).
9. Kamada N, Kim YG, Sham HP, et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science. 2012;336(6086):1325–9 (Epub 2012/05/15).
10. Fischbach MA, Sonnenburg JL. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe. 2011;10(4):336–47 (Epub 2011/10/25).
11. May T, Mackie RI, Fahey GC Jr, et al. Effect of fiber source on short-chain fatty acid production and on the growth and toxin production by Clostridium difficile. Scand J Gastroenterol. 1994;29(10):916–22 (Epub 1994/10/01).
12. Van Immerseel F, De Buck J, Pasmans F, 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(3):237–48 (Epub 2003/07/25).
13. Lupp C, Robertson ML, Wickham ME, et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2007;2(2):119–29 (Epub 2007/11/17).
14. Sekirov I, Tam NM, Jogova M, et al. Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun. 2008;76(10):4726–36 (Epub 2008/08/06).
15. Bertin Y, Girardeau JP, Chaucheyras-Durand F, et al. Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content. Environ Microbiol. 2011;13(2):365–77 (Epub 2010/09/21).
16. Perna NT, Plunkett G 3rd, Burland V, et al. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature. 2001;409(6819):529–33 (Epub 2001/02/24).
17. Winter SE, Thiennimitr P, Winter MG, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature. 2010;467(7314):426–9 (Epub 2010/09/25).
18. Ferreyra JA, Wu KJ, Hryckowian AJ, et al. Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe. 2014;16(6):770–7 (Epub 2014/12/17).
19. Sturm A, Heinemann M, Arnoldini M, et al. The cost of virulence: retarded growth of Salmonella Typhimurium cells expressing type III secretion system 1. PLoS Pathog. 2011;7(7):e1002143 (Epub 2011/08/11).
20. Kolling G, Wu M, Guerrant RL. Enteric pathogens through life stages. Front Cell Infect Microbiol. 2012;2:114 (Epub 2012/09/01).
21. Castellani F, Ghidini V, Tafi MC, et al. Fate of pathogenic bacteria in microcosms mimicking human body sites. Microb Ecol. 2013;66(1):224–31 (Epub 2013/05/10).
22. Shin S, Castanie-Cornet MP, Foster JW, et al. An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator. Per. Mol Microbiol. 2001;41(5):1133–50 (Epub 2001/09/14).
23. Abe H, Tatsuno I, Tobe T, et al. Bicarbonate ion stimulates the expression of locus of enterocyte effacement-encoded genes in enterohemorrhagic Escherichia coli O157:H7. Infect Immun. 2002;70(7):3500–9 (Epub 2002/06/18).
24. Caparon MG, Geist RT, Perez-Casal J, et al. Environmental regulation of virulence in group A streptococci: transcription of the gene encoding M protein is stimulated by carbon dioxide. J Bacteriol. 1992;174(17):5693–701 (Epub 1992/09/01).
25. Tauschek M, Yang J, Hocking D, et al. Transcriptional analysis of the grlRA virulence operon from Citrobacter rodentium. J Bacteriol. 2010;192(14):3722–34 (Epub 2010/05/18).
26. Yang J, Tauschek M, Hart E, et al. Virulence regulation in Citrobacter rodentium: the art of timing. Microb Biotechnol. 2010;3(3):259–68 (Epub 2011/01/25).
27. Tan A, Yang J, Tauschek M, et al. Autogenous transcriptional regulation of the regA gene, encoding an AraC-Like, essential virulence regulator in Citrobacter rodentium. J Bacteriol. 2011;193(7):1777–82 (Epub 2011/02/01).
28. Cummings LA, Wilkerson WD, Bergsbaken T, et al. In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted. Mol Microbiol. 2006;61(3):795–809 (Epub 2006/06/29).
29. Cummings LA, Barrett SL, Wilkerson WD, et al. FliC-specific CD4+ T cell responses are restricted by bacterial regulation of antigen expression. J Immunol. 2005;174(12):7929–38 (Epub 2005/06/10).
30. Winter SE, Winter MG, Godinez I, et al. A rapid change in virulence gene expression during the transition from the intestinal lumen into tissue promotes systemic dissemination of Salmonella. PLoS Pathog. 2010;6(8):e1001060 (Epub 2010/09/03).
31. Yoshida T, Cai S, Inouye M. Interaction of EnvZ, a sensory histidine kinase, with phosphorylated OmpR, the cognate response regulator. Mol Microbiol. 2002;46(5):1283–94 (Epub 2002/11/28).
32. Winter SE, Winter MG, Thiennimitr P, et al. The TviA auxiliary protein renders the Salmonella enterica serotype Typhi RcsB regulon responsive to changes in osmolarity. Mol Microbiol. 2009;74(1):175–93 (Epub 2009/08/26).
33. Fink RC, Evans MR, Porwollik S, et al. FNR is a global regulator of virulence and anaerobic metabolism in Salmonella enterica serovar Typhimurium (ATCC 14028s). J Bacteriol. 2007;189(6):2262–73 (Epub 2007/01/16).
34. Marteyn B, West NP, Browning DF, et al. Modulation of Shigella virulence in response to available oxygen in vivo. Nature. 2010;465(7296):355–8 (Epub 2010/05/04).
35. Gunn JS. Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2000;2(8):907–13 (Epub 2000/08/30).
36. Chatterjee A, Dutta PK, Chowdhury R. Effect of fatty acids and cholesterol present in bile on expression of virulence factors and motility of Vibrio cholerae. Infect Immun. 2007;75(4):1946–53 (Epub 2007/01/31).
37. Lowden MJ, Skorupski K, Pellegrini M, et al. Structure of Vibrio cholerae ToxT reveals a mechanism for fatty acid regulation of virulence genes. Proc Natl Acad Sci USA. 2010;107(7):2860–5 (Epub 2010/02/06).
38. Gupta S, Chowdhury R. Bile affects production of virulence factors and motility of Vibrio cholerae. Infect Immun. 1997;65(3):1131–4 (Epub 1997/03/01).
39. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001;81(3):1031–64 (Epub 2001/06/28).
40. Binder HJ. Role of colonic short-chain fatty acid transport in diarrhea. Annu Rev Physiol. 2010;72:297–313 (Epub 2010/02/13).
41. Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc. 2003;62(1):67–72 (Epub 2003/05/13).
42. Lawhon SD, Maurer R, Suyemoto M, et al. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol Microbiol. 2002;46(5):1451–64 (Epub 2002/11/28).
43. Robbe C, Capon C, Coddeville B, et al. Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochem J. 2004;384(Pt 2):307–16 (Epub 2004/09/14).
44. Liquori GE, Mastrodonato M, Mentino D, et al. In situ characterization of O-linked glycans of Muc2 in mouse colon. Acta Histochem. 2012;114(7):723–32 (Epub 2012/01/21).
45. Jaswal VM, Babbar HS, Mahmood A. Changes in sialic acid and fucose contents of enterocytes across the crypt-villus axis in developing rat intestine. Biochem Med Metab Biol. 1988;39(1):105–10 (Epub 1988/02/01).
46. Chow WL, Lee YK. Free fucose is a danger signal to human intestinal epithelial cells. Br J Nutr. 2008;99(3):449–54 (Epub 2007/08/19).
47. Pacheco AR, Curtis MM, Ritchie JM, et al. Fucose sensing regulates bacterial intestinal colonization. Nature. 2012;492(7427):113–7 (Epub 2012/11/20).
48. Atarashi K, Tanoue T, Ando M, et al. Th17 Cell Induction by Adhesion of Microbes to Intestinal Epithelial Cells. Cell. 2015;163(2):367–80 (Epub 2015/09/29).
49. Alsharif G, Ahmad S, Islam MS, et al. Host attachment and fluid shear are integrated into a mechanical signal regulating virulence in Escherichia coli O157:H7. Proc Natl Acad Sci USA. 2015;112(17):5503–8 (Epub 2015/04/15).
50. Atuma C, Strugala V, Allen A, et al. The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol Gastrointest Liver Physiol. 2001;280(5):G922–9 (Epub 2001/04/09).
51. Corazziari ES. Intestinal mucus barrier in normal and inflamed colon. J Pediatr Gastroenterol Nutr. 2009;48(Suppl 2):S54–5 (Epub 2009/03/28).
52. Hase CC, Mekalanos JJ. Effects of changes in membrane sodium flux on virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA. 1999;96(6):3183–7 (Epub 1999/03/17).
53. Sifri CD. Healthcare epidemiology: quorum sensing: bacteria talk sense. Clin Infect Dis. 2008;47(8):1070–6 (Epub 2008/09/11).
54. Chan WC, Coyle BJ, Williams P. Virulence regulation and quorum sensing in staphylococcal infections: competitive AgrC antagonists as quorum sensing inhibitors. J Med Chem. 2004;47(19):4633–41 (Epub 2004/09/03).
55. Cheung AL, Bayer AS, Zhang G, et al. Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol Med Microbiol. 2004;40(1):1–9 (Epub 2004/01/22).
56. Wuster A, Babu MM. Conservation and evolutionary dynamics of the agr cell-to-cell communication system across firmicutes. J Bacteriol. 2008;190(2):743–6 (Epub 2007/10/16).
57. Diard M, Garcia V, Maier L, et al. Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature. 2013;494(7437):353–6 (Epub 2013/02/22).
58. Kamada N, Sakamoto K, Seo SU, et al. Humoral immunity in the gut selectively targets phenotypically virulent attaching-and-effacing bacteria for intraluminal elimination. Cell Host Microbe. 2015;17(5):617–27 (Epub 2015/05/06).
59. Collins JW, Keeney KM, Crepin VF, et al. Citrobacter rodentium: infection, inflammation and the microbiota. Nat Rev Microbiol. 2014;12(9):612–23 (Epub 2014/08/05).
60. Bry L, Brenner MB. Critical role of T cell-dependent serum antibody, but not the gut-associated lymphoid tissue, for surviving acute mucosal infection with Citrobacter rodentium, an attaching and effacing pathogen. J Immunol. 2004;172(1):433–41 (Epub 2003/12/23).
61. Maaser C, Housley MP, Iimura M, et al. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect Immun. 2004;72(6):3315–24 (Epub 2004/05/25).
62. Palm NW, de Zoete MR, Cullen TW, et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell. 2014;158(5):1000–10 (Epub 2014/08/30).