In Vitro Colonization of the Muscle Extracellular Matrix Components by Escherichia coli O157:H7: The Influence of Growth Medium, Temperature and pH on Initial Adhesion and Induction of Biofilm Formation by Collagens I and III

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Chagnot, Caroline ^a,b   Agus, Allison ^a   Renier, Sandra ^a   Peyrin, Frédéric ^b   Talon, Régine ^a   Astruc, Thierry ^b   Desvaux, Mickaël ^a  

^a CEMAGREF   (France)

^b UR370 QuaPA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGEN TYPE 4; ELASTIN; FIBRONECTIN; LAMININ ALPHA2; SCLEROPROTEIN;

ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BIOFILM; CONTROLLED STUDY; CULTURE MEDIUM; ESCHERICHIA COLI O157; EXTRACELLULAR MATRIX; IN VITRO STUDY; MEMBRANE FORMATION; NONHUMAN; PH; TEMPERATURE SENSITIVITY;

ANIMALS; BIOFILMS; CATTLE; COLLAGEN TYPE I; COLLAGEN TYPE III; CULTURE MEDIA; ELASTIN; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; FIBRONECTINS; HYDROGEN-ION CONCENTRATION; LAMININ; TEMPERATURE;

EID: 84874899386     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059386     Document Type: Article

References (76)

1. Chase-Topping M, Gally D, Low C, Matthews L, Woolhouse M, (2008) Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nat Rev Microbiol 6: 904-912.
2. Meng J, Doyle MP, (1997) Emerging issues in microbiological food safety. Annu Rev Nutr 17: 255-275.
3. Bavaro MF, (2012) Escherichia coli O157:H7 and other toxigenic strains: the curse of global food distribution. Curr Gastroenterol Rep 14: 317-323.
4. Riley LW, Remis RS, Helgerson SD, McGee HB, Wells JG, et al. (1983) Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308: 681-685.
5. Karch H, Tarr PI, Blelaszewska M, (2005) Enterohaemorrhagic Escherichia coli in human medicine. International Journal of Medical Microbiology 295: 405-418.
6. Karch H, Mellmann A, Bielaszewska M, (2009) Epidemiology and pathogenesis of enterohaemorrhagic Escherichia coli. Berliner Und Munchener Tierarztliche Wochenschrift 122: 417-424.
7. Hermos CR, Janineh M, Han LL, McAdam AJ, (2011) Shiga toxin-producing Escherichia coli in children: diagnosis and clinical manifestations of O157:H7 and non-O157:H7 infection. Journal of Clinical Microbiology 49: 955-959.
8. Gould LH, Demma L, Jones TF, Hurd S, Vugia DJ, et al. (2009) Hemolytic uremic syndrome and death in persons with Escherichia coli O157:H7 infection, foodborne diseases active surveillance network sites, 2000-2006. Clinical Infectious Diseases 49: 1480-1485.
9. Tarr PI, (2009) Shiga toxin-associated hemolytic uremic syndrome and thrombotic thrombocytopenic purpura: distinct mechanisms of pathogenesis. Kidney International 75: S29-S32.
10. Rhoades JR, Duffy G, Koutsoumanis K, (2009) Prevalence and concentration of verocytotoxigenic Escherichia coli, Salmonella enterica and Listeria monocytogenes in the beef production chain: a review. Food Microbiol 26: 357-376.
11. Lonergan EH, Zhang WA, Lonergan SM, (2010) Biochemistry of postmortem muscle - Lessons on mechanisms of meat tenderization. Meat Science 86: 184-195.
12. Wong ARC, Pearson JS, Bright MD, Munera D, Robinson KS, et al. (2011) Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Molecular Microbiology 80: 1420-1438.
13. Farfan MJ, Torres AG, (2012) Molecular mechanisms that mediate colonization of Shiga toxin-producing Escherichia coli strains. Infection and Immunity 80: 903-913.
14. Duffy G, Cummins E, Nally P, O'Brien, Butler F, (2006) A review of quantitative microbial risk assessment in the management of Escherichia coli O157:H7 on beef. Meat Sci 74: 76-88.
15. Chen JR, Rossman ML, Pawar DM, (2007) Attachment of enterohemorrhagic Escherichia coli to the surface of beef and a culture medium. Lwt-Food Science and Technology 40: 249-254.
16. Cabedo L, Sofos JN, Schmidt GR, Smith GC, (1997) Attachment of Escherichia coli O157:H7 and other bacterial cells grown in two media to beef adipose and muscle tissues. Journal of Food Protection 60: 102-106.
17. Rivas L, Dykes GA, Fegan N, (2006) Attachment of Shiga toxigenic Escherichia coli to beef muscle and adipose tissue. Journal of Food Protection 69: 999-1006.
18. Li J, McLandsborough LA, (1999) The effects of the surface charge and hydrophobicity of Escherichia coli on its adhesion to beef muscle. International Journal of Food Microbiology 53: 185-193.
19. Auty M, Duffy G, O'Beirne D, McGovern A, Gleeson E, et al. (2005) In situ localization of Escherichia coli O157: H7 in food by confocal scanning laser microscopy. Journal of Food Protection 68: 482-486.
20. Medina MB, (2001) Binding of collagen I to Escherichia coli O157:H7 and inhibition by carrageenans. Int J Food Microbiol 69: 199-208.
21. Frantz C, Stewart KM, Weaver VM, (2010) The extracellular matrix at a glance. J Cell Sci 123: 4195-4200.
22. Purslow PP, (2005) Intramuscular connective tissue and its role in meat quality. Meat Science 70: 435-447.
23. Purslow PP, (2002) The structure and functional significance of variations in the connective tissue within muscle. Comparative Biochemistry and Physiology a-Molecular and Integrative Physiology 133: 947-966.
24. Thorsteinsdottir S, Deries M, Cachaco AS, Bajanca F, (2011) The extracellular matrix dimension of skeletal muscle development. Developmental Biology 354: 191-207.
25. Chagnot C, Listrat A, Astruc T, Desvaux M, (2012) Bacterial adhesion to animal tissues: protein determinants for recognition of extracellular matrix components. Cell Microbiol 14: 1687-1696.
26. Medina MB, Fratamico PM, (1998) Binding interactions of collagen I, laminin and fibronectin with immobilized Escherichia coli O157: H7 using a surface plasmon resonance biosensor. Biotechnology Techniques 12: 235-240.
27. Medina MB, (2002) Biosensor studies of the binding of extracellular matrix components with immobilized Escherichia coli O157: H7 and inhibition by polysulfated polysaccharides. Biotechnology Letters 24: 77-84.
28. Fratamico PM, Schultz FJ, Benedict RC, Buchanan RL, Cooke PH, (1996) Factors influencing attachment of Escherichia coli O157:H7 to beef tissues and removal using selected sanitizing rinses. Journal of Food Protection 59: 453-459.
29. Brady MJ, Radhakrishnan P, Liu H, Magoun L, Murphy KC, et al. (2011) Enhanced actin pedestal formation by enterohemorrhagic Escherichia coli O157:H7 adapted to the mammalian host. Front Microbiol 2: 226.
30. Xicohtencatl-Cortes J, Monteiro-Neto V, Ledesma MA, Jordan DM, Francetic O, et al. (2007) Intestinal adherence associated with Type 4 pili of enterohemorrhagic Escherichia coli O157:H7. J Clin Invest 117: 3519-3529.
31. Zulfakar SS, White JD, Ross T, Tamplin ML, (2012) Bacterial attachment to immobilized extracellular matrix proteins in vitro. Int J Food Microbiol 157: 210-217.
32. Gobert AP, Vareille M, Glasser AL, Hindre T, de Sablet T, et al. (2007) Shiga toxin produced by enterohemorrhagic Escherichia coli inhibits PI3K/NF-kappaB signaling pathway in globotriaosylceramide-3-negative human intestinal epithelial cells. J Immunol 178: 8168-8174.
33. Perna NT, Plunkett G, Burland V, Mau B, Glasner JD, et al. (2001) Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409: 529-533.
34. Pardee AR, Jacob F, Monod J, (1959) The genetic control and cytoplasmic expression of "Inducibility" in the synthesis of β-galactosidase by Escherichia coli. J Mol Biol 1: 165-178.
35. Guinée PA, Veldkamp J, Jansen WH, (1977) Improved MinCa medium for the detection of K99 antigen in calf enterotoxigenic strains of Escherichia coli. Infect Immun 15: 676-678.
36. Bertani G, (2004) Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J Bacteriol 186: 595-600.
37. Leedle JA, Hespell RB, (1980) Differential carbohydrate media and anaerobic replica plating techniques in delineating carbohydrate-utilizing subgroups in rumen bacterial populations. Appl Environ Microbiol 39: 709-719.
38. Bertin Y, Girardeau JP, Chaucheyras-Durand F, Lyan B, Pujos-Guillot E, et al. (2011) Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content. Environ Microbiol 13: 365-377.
39. Kredel S, Oswald F, Nienhaus K, Deuschle K, Rocker C, et al. (2009) mRuby, a bright monomeric red fluorescent protein for labeling of subcellular structures. PLoS One 4: e4391.
40. Monk IR, Gahan CG, Hill C, (2008) Tools for functional postgenomic analysis of Listeria monocytogenes. Appl Environ Microbiol 74: 3921-3934.
41. Trieu-Cuot P, Carlier C, Poyart-Salmeron C, Courvalin P, (1991) Shuttle vectors containing a multiple cloning site and a lacZ alpha gene for conjugal transfer of DNA from Escherichia coli to Gram-positive bacteria. Gene 102: 99-104.
42. Hennequin C, Forestier C, (2007) Influence of capsule and extended-spectrum beta-lactamases encoding plasmids upon Klebsiella pneumoniae adhesion. Res Microbiol 158: 339-347.
43. Hasman H, Chakraborty T, Klemm P, (1999) Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J Bacteriol 181: 4834-4841.
44. Borucki MK, Peppin JD, White D, Loge F, Call DR, (2003) Variation in biofilm formation among strains of Listeria monocytogenes. Appl Environ Microbiol 69: 7336-7342.
45. Purslow PP, (2010) Muscle fascia and force transmission. J Bodyw Mov Ther 14: 411-417.
46. Durbeej M, (2010) Laminins. Cell Tissue Res 339: 259-268.
47. Voermans NC, Bonnemann CG, Huijing PA, Hamel BC, van Kuppevelt TH, et al. (2008) Clinical and molecular overlap between myopathies and inherited connective tissue diseases. Neuromuscul Disord 18: 843-856.
48. Wells TJ, McNeilly TN, Totsika M, Mahajan A, Gally DL, et al. (2009) The Escherichia coli O157:H7 EhaB autotransporter protein binds to laminin and collagen I and induces a serum IgA response in O157:H7 challenged cattle. Environ Microbiol 11: 1803-1814.
49. Chingcuanco F, Yu Y, Kus JV, Que L, Lackraj T, et al. (2012) Identification of a novel adhesin involved in acid-induced adhesion of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 158: 2399-2407.
50. Collington GK, Booth IW, Knutton S, (1998) Rapid modulation of electrolyte transport in Caco-2 cell monolayers by enteropathogenic Escherichia coli (EPEC) infection. Gut 42: 200-207.
51. Tree JJ, Wolfson EB, Wang D, Roe AJ, Gally DL, (2009) Controlling injection: regulation of Type III secretion in enterohaemorrhagic Escherichia coli. Trends Microbiol 17: 361-370.
52. Abu-Ali GS, Ouellette LM, Henderson ST, Whittam TS, Manning SD, (2010) Differences in adherence and virulence gene expression between two outbreak strains of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 156: 408-419.
53. House B, Kus JV, Prayitno N, Mair R, Que L, et al. (2009) Acid-stress-induced changes in enterohaemorrhagic Escherichia coli O157:H7 virulence. Microbiology 155: 2907-2918.
54. Hirakawa H, Kodama T, Takumi-Kobayashi A, Honda T, Yamaguchi A, (2009) Secreted indole serves as a signal for expression of Type III secretion system translocators in enterohaemorrhagic Escherichia coli O157:H7. Microbiology 155: 541-550.
55. Nakanishi N, Tashiro K, Kuhara S, Hayashi T, Sugimoto N, et al. (2009) Regulation of virulence by butyrate sensing in enterohaemorrhagic Escherichia coli. Microbiology 155: 521-530.
56. Ando H, Abe H, Sugimoto N, Tobe T, (2007) Maturation of functional Type III secretion machinery by activation of anaerobic respiration in enterohaemorrhagic Escherichia coli. Microbiology 153: 464-473.
57. Anand SK, Griffiths MW, (2003) Quorum sensing and expression of virulence in Escherichia coli O157:H7. Int J Food Microbiol 85: 1-9.
58. Desvaux M, Petitdemange H, (2002) Sporulation of Clostridium cellulolyticum while grown in cellulose-batch and cellulose-fed continuous cultures on a mineral-salt based medium. Microb Ecol 43: 271-279.
59. Payot S, Guedon E, Desvaux M, Gelhaye E, Petitdemange E, (1999) Effect of dilution rate, cellobiose and ammonium availabilities on Clostridium cellulolyticum sporulation. Appl Microbiol Biotechnol 52: 670-674.
60. Torres AG, Perna NT, Burland V, Ruknudin A, Blattner FR, et al. (2002) Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol Microbiol 45: 951-966.
61. Desvaux M, Parham NJ, Henderson IR, (2003) Le système de sécrétion de Type V chez les bactéries Gram-négatives. Biofutur 237: 34-37.
62. Henderson IR, Desvaux M, (2004) Type V secretion pathway: a premium source source of virulence factors? Drug Discov Today 9: 241.
63. Desvaux M, Petitdemange H, (2001) Flux analysis of the metabolism of Clostridium cellulolyticum grown in cellulose-fed continuous culture on a chemically defined medium under ammonium-limited conditions. Appl Environ Microbiol 67: 3846-3851.
64. Guedon E, Payot S, Desvaux M, Petitdemange H, (2000) Relationships between cellobiose catabolism, enzyme levels, and metabolic intermediates in Clostridium cellulolyticum grown in a synthetic medium. Biotechnol Bioeng 67: 327-335.
65. Desvaux M, (2004) Mapping of carbon flow distribution in the central metabolic pathways of Clostridium cellulolyticum: Direct comparison of bacterial metabolism with a soluble versus an insoluble carbon source. J Microbiol Biotechnol 14: 1200-1210.
66. Desvaux M, (2006) Unravelling carbon metabolism in anaerobic cellulolytic bacteria. Biotechnol Prog 22: 1229-1238.
67. Farfan MJ, Cantero L, Vidal R, Botkin DJ, Torres AG, (2011) Long polar fimbriae of enterohemorrhagic Escherichia coli O157:H7 bind to extracellular matrix proteins. Infect Immun 79: 3744-3750.
68. Totsika M, Wells TJ, Beloin C, Valle J, Allsopp LP, et al. (2012) Molecular characterization of the EhaG and UpaG trimeric autotransporter proteins from pathogenic Escherichia coli. Appl Environ Microbiol 78: 2179-2189.
69. Wells TJ, Sherlock O, Rivas L, Mahajan A, Beatson SA, et al. (2008) EhaA is a novel autotransporter protein of enterohemorrhagic Escherichia coli O157:H7 that contributes to adhesion and biofilm formation. Environ Microbiol 10: 589-604.
70. Desvaux M, Cooper LM, Filenko NA, Scott-Tucker A, Turner SM, et al. (2006) The unusual extended signal peptide region of the Type V secretion system is phylogenetically restricted. FEMS Microbiol Lett 264: 22-30.
71. Xicohtencatl-Cortes J, Monteiro-Neto V, Saldana Z, Ledesma MA, Puente JL, et al. (2009) The Type 4 pili of enterohemorrhagic Escherichia coli O157:H7 are multipurpose structures with pathogenic attributes. J Bacteriol 191: 411-421.
72. Ricard-Blum S, (2011) The collagen family. Cold Spring Harb Perspect Biol 3: a004978.
73. Bonifait L, Grignon L, Grenier D, (2008) Fibrinogen induces biofilm formation by Streptococcus suis and enhances its antibiotic resistance. Appl Environ Microbiol 74: 4969-4972.
74. Henderson B, Nair S, Pallas J, Williams MA, (2011) Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins. FEMS Microbiol Rev 35: 147-200.
75. Vercellotti GM, McCarthy JB, Lindholm P, Peterson PK, Jacob HS, et al. (1985) Extracellular matrix proteins (fibronectin, laminin, and type IV collagen) bind and aggregate bacteria. Am J Pathol 120: 13-21.
76. Frank JF, (2001) Microbial attachment to food and food contact surfaces. Adv Food Nutr Res 43: 319-370.