Dietary choice affects Shiga toxin-producing Escherichia coli (STEC) O157:H7 colonization and disease

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 23, 2013, Pages

  Zumbrun, Steven D ^a   Melton Celsa, Angela R ^a   Smith, Mark A ^a   Gilbreath, Jeremy J ^a   Merrell, D Scott ^a   O'Brien, Alison D ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Hct 8; Microbiome; Tubular necrosis

Indexed keywords

BUTYRIC ACID; GLOBOTRIAOSYLCERAMIDE; SHIGA TOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BODY WEIGHT; CONTROLLED STUDY; DIET; DISEASE SEVERITY; ESCHERICHIA COLI INFECTION; FEMALE; HEMOLYTIC UREMIC SYNDROME; HIGH FIBER DIET; INFECTION SENSITIVITY; INGESTION; INTESTINE; MICROFLORA; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; UPREGULATION;

HCT-8; MICROBIOME; TUBULAR NECROSIS;

ANALYSIS OF VARIANCE; ANIMALS; BUTYRATES; CELL LINE; DIETARY FIBER; DISEASE SUSCEPTIBILITY; DNA PRIMERS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI O157; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GASTROINTESTINAL TRACT; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; SHIGA TOXIN; SPECIES SPECIFICITY;

ESCHERICHIA; ESCHERICHIA COLI; MUS;

EID: 84878715402     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1222014110     Document Type: Article

References (76)

1. Rangel JM, Sparling PH, Crowe C, Griffin PM, Swerdlow DL (2005) Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg Infect Dis 11(4): 603-609.
2. Scallan E, Griffin PM, Angulo FJ, Tauxe RV, Hoekstra RM (2011) Foodborne illness acquired in the United States - unspecified agents. Emerg Infect Dis 17(1):16-22.
3. USDA ERS (1996) Foodborne Illness Cost Calculator (US Department of Agriculture Economic Research Service, Washington).
4. Tilden J, Jr., et al. (1996) A new route of transmission for Escherichia coli: Infection from dry fermented salami. Am J Public Health 86(8):1142-1145.
5. Bell BP, et al. (1994) A multistate outbreak of Escherichia coli O157:H7-associated bloody diarrhea and hemolytic uremic syndrome from hamburgers: The Washington experience. JAMA 272(17):1349-1353.
6. Tarr PI, Gordon CA, Chandler WL (2005) Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365(9464):1073-1086.
7. Mead PS, et al. (1999) Food-related illness and death in the United States. Emerg Infect Dis 5(5):607-625.
8. Rowe PC, Orrbine E, Lior H, Wells GA, McLaine PN (1993) A prospective study of exposure to verotoxin-producing Escherichia coli among Canadian children with haemolytic uraemic syndrome. The CPKDRC co-investigators. Epidemiol Infect 110(1): 1-7.
9. Team CFER (2007) Investigation of an Escherichia coli O157:H7 Outbreak Associated with Dole Pre-Packaged Spinach (California Department of Public Health Food and Drug Branch, Sacramento, CA).
10. Johnson RP, et al. (1996) Growing concerns and recent outbreaks involving non-O157: H7 serotypes of verotoxigenic Escherichia coli. J Food Prot 59(10):1112-1122.
11. Lieberman E (1972) Hemolytic-uremic syndrome. J Pediatr 80(1):1-16.
12. Barton Behravesh C, et al.; FoodNet Working Group (2011) Deaths associated with bacterial pathogens transmitted commonly through food: Foodborne diseases active surveillance network (FoodNet), 1996-2005. J Infect Dis 204(2):263-267.
13. Frank C, et al.; HUS Investigation Team (2011) Epidemic profile of Shiga-toxinproducing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 365(19): 1771-1780.
14. Ståhl AL, Sartz L, Karpman D (2011) Complement activation on platelet-leukocyte complexes and microparticles in enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome. Blood 117(20):5503-5513.
15. Noris M, Mescia F, Remuzzi G (2012) STEC-HUS, atypical HUS and TTP are all diseases of complement activation. Nat Rev Nephrol 8(11):622-633.
16. Karpman D, et al. (2001) Platelet activation by Shiga toxin and circulatory factors as a pathogenetic mechanism in the hemolytic uremic syndrome. Blood 97(10): 3100-3108.
17. Tsuji S, et al. (2012) Production of nitric oxide is lower in Shiga toxin-stimulated neutrophils of infants compared to those of children or adults. Tohoku J Exp Med 228 (3):247-252.
18. Békássy ZD, et al. (2011) Intestinal damage in enterohemorrhagic Escherichia coli infection. Pediatr Nephrol 26(11):2059-2071.
19. Schüller S, Frankel G, Phillips AD (2004) Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture. Cell Microbiol 6(3):289-301.
20. Mayer CL, Leibowitz CS, Kurosawa S, Stearns-Kurosawa DJ (2012) Shiga toxins and the pathophysiology of hemolytic uremic syndrome in humans and animals. Toxins (Basel) 4(11):1261-1287.
21. Jelacic JK, et al. (2003) Shiga toxin-producing Escherichia coli in Montana: Bacterial genotypes and clinical profiles. J Infect Dis 188(5):719-729.
22. Paton JC, Paton AW (1998) Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 11(3):450-479.
23. Shin IS, et al. (2009) Globotriaosylceramide (Gb3) content in HeLa cells is correlated to Shiga toxin-induced cytotoxicity and Gb3 synthase expression. BMB Reports 42(5): 310-314.
24. Holgersson J, Jovall PA, Breimer ME (1991) Glycosphingolipids of human large intestine: Detailed structural characterization with special reference to blood group compounds and bacterial receptor structures. J Biochem 110(1):120-131.
25. Björk S, Breimer ME, Hansson GC, Karlsson KA, Leffler H (1987) Structures of blood group glycosphingolipids of human small intestine: A relation between the expression of fucolipids of epithelial cells and the ABO, Le and Se phenotype of the donor. J Biol Chem 262(14):6758-6765.
26. Zumbrun SD, et al. (2010) Human intestinal tissue and cultured colonic cells contain globotriaosylceramide synthase mRNA and the alternate Shiga toxin receptor globotetraosylceramide. Infect Immun 78(11):4488-4499.
27. Vanhoutvin SA, et al. (2009) Butyrate-induced transcriptional changes in human colonic mucosa. PLoS ONE 4(8):e6759.
28. Scheppach W (1994) Effects of short chain fatty acids on gut morphology and function. Gut 35(1, Suppl):(Suppl):S35-S38.
29. Hamer HM, et al. (2008) Review article: The role of butyrate on colonic function. Aliment Pharmacol Ther 27(2):104-119.
30. Ohmi K, Kiyokawa N, Takeda T, Fujimoto J (1998) Human microvascular endothelial cells are strongly sensitive to Shiga toxins. Biochem Biophys Res Commun 251(1): 137-141.
31. Hughes AK, Stricklett PK, Schmid D, Kohan DE (2000) Cytotoxic effect of Shiga toxin-1 on human glomerular epithelial cells. Kidney Int 57(6):2350-2359.
32. Hughes AK, Stricklett PK, Kohan DE (1998) Cytotoxic effect of Shiga toxin-1 on human proximal tubule cells. Kidney Int 54(2):426-437.
33. Keusch GT, Acheson DW, Aaldering L, Erban J, Jacewicz MS (1996) Comparison of the effects of Shiga-like toxin 1 on cytokine- and butyrate-treated human umbilical and saphenous vein endothelial cells. J Infect Dis 173(5):1164-1170.
34. McIntyre A, Gibson PR, Young GP (1993) Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut 34(3):386-391.
35. Duncan SH, et al. (2007) Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 73(4):1073-1078.
36. De Filippo C, et al. (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107(33):14691-14696.
37. Bach Knudsen KE, Serena A, Kjaer AK, Jørgensen H, Engberg R (2005) Rye bread enhances the production and plasma concentration of butyrate but not the plasma concentrations of glucose and insulin in pigs. J Nutr 135(7):1696-1704.
38. Ramirez-Farias C, et al. (2009) Effect of inulin on the human gut microbiota: Stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr 101(4):541-550.
39. Hopkins MJ, Sharp R, Macfarlane GT (2001) Age and disease related changes in intestinal bacterial populations assessed by cell culture, 16S rRNA abundance, and community cellular fatty acid profiles. Gut 48(2):198-205.
40. Scott KP, Duncan SH, Louis P, Flint HJ (2011) Nutritional influences on the gut microbiota and the consequences for gastrointestinal health. Biochem Soc Trans 39(4):1073-1078.
41. Hermes RG, et al. (2009) Effect of dietary level of protein and fiber on the productive performance and health status of piglets. J Anim Sci 87(11):3569-3577.
42. Holgersson J, Strömberg N, Breimer ME (1988) Glycolipids of human large intestine: Difference in glycolipid expression related to anatomical localization, epithelial/nonepithelial tissue and the ABO, Le and Se phenotypes of the donors. Biochimie 70(11): 1565-1574.
43. Thornton FJ, Barbul A (1997) Healing in the gastrointestinal tract. Surg Clin North Am 77(3):549-573.
44. Roediger WE (1980) Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21(9):793-798.
45. Roediger WE (1990) The starved colon - diminished mucosal nutrition, diminished absorption, and colitis. Dis Colon Rectum 33(10):858-862.
46. Hennings SJ, Hird FJ (1970) Concentrations and metabolism of volatile fatty acids in the fermentative organs of two species of kangaroo and the guinea-pig. Br J Nutr 24(1): 145-155.
47. Firmansyah A, Penn D, Lebenthal E (1989) Isolated colonocyte metabolism of glucose, glutamine, n-butyrate, and beta-hydroxybutyrate in malnutrition. Gastroenterology 97(3):622-629.
48. Van Immerseel F, et al. (2010) Butyric acid-producing anaerobic bacteria as a novel probiotic treatment approach for inflammatory bowel disease. J Med Microbiol 59(Pt 2):141-143.
49. Ahmad MS, et al. (2000) Butyrate and glucose metabolism by colonocytes in experimental colitis in mice. Gut 46(4):493-499.
50. Fernández-Rubio C, et al. (2009) Butyric acid-based feed additives help protect broiler chickens from Salmonella Enteritidis infection. Poult Sci 88(5):943-948.
51. Michiels J, et al. (2012) Effect of organic acids on Salmonella colonization and shedding in weaned piglets in a seeder model. J Food Prot 75(11):1974-1983.
52. Tamura T, Tsuruta N, Hirano K, Yamaguchi K, Oda T (2003) Butyric acid sensitizes Vero cells to ricin-induced apoptosis via accelerated activation of multiple signal transduction pathways. Cell Struct Funct 28(5):475-485.
53. Raa H, et al. (2009) Glycosphingolipid requirements for endosome-to-Golgi transport of Shiga toxin. Traffic 10(7):868-882.
54. Lingwood CA, Khine AA, Arab S (1998) Globotriaosyl ceramide (Gb3) expression in human tumour cells: intracellular trafficking defines a new retrograde transport pathway from the cell surface to the nucleus, which correlates with sensitivity to verotoxin. Acta Biochim Pol 45(2):351-359.
55. Nakanishi N, et al. (2009) Regulation of virulence by butyrate sensing in enterohaemorrhagic Escherichia coli. Microbiology 155(Pt 2):521-530.
56. Robinson CM, Sinclair JF, Smith MJ, O'Brien AD (2006) Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc Natl Acad Sci USA 103(25):9667-9672.
57. Gilbert RA, et al. (2008) Effect of diet on the concentration of complex Shiga toxinproducing Escherichia coli and EHEC virulence genes in bovine faeces, hide and carcass. Int J Food Microbiol 121(2):208-216.
58. Jacewicz MS, et al. (1995) Maturational regulation of globotriaosylceramide, the Shiga-like toxin 1 receptor, in cultured human gut epithelial cells. J Clin Invest 96(3): 1328-1335.
59. Smith MJ, et al. (2009) Monoclonal antibody 11E10, which neutralizes Shiga toxin type 2 (Stx2), recognizes three regions on the Stx2A subunit, blocks the enzymatic action of the toxin in vitro, and alters the overall cellular distribution of the toxin. Infect Immun 77(7):2730-2740.
60. Melton-Celsa AR, O'Brien AD (2000) Handbook of Experimental Pharmacology, eds Aktories K, Just I (Springer, Berlin), pp 385-406.
61. Gentry MK, Dalrymple JM (1980) Quantitative microtiter cytotoxicity assay for Shigella toxin. J Clin Microbiol 12(3):361-366.
62. Mohawk KL, Melton-Celsa AR, Zangari T, Carroll EE, O'Brien AD (2010) Pathogenesis of Escherichia coli O157:H7 strain 86-24 following oral infection of BALB/c mice with an intact commensal flora. Microb Pathog 48(3-4):131-142.
63. Gunzer F, et al. (1998) Construction and characterization of an isogenic slt-ii deletion mutant of enterohemorrhagic Escherichia coli. Infect Immun 66(5):2337-2341.
64. Nutikka A, Binnington-Boyd B, Lingwood CA (2003) Methods for the identification of host receptors for Shiga toxin. Methods Mol Med 73:197-208.
65. Rasband WS (1997-2012) ImageJ (US National Institutes of Health, Bethesda, MD). Available at http://imagej.nih.gov/ij/.
66. Richardson AJ, Calder AG, Stewart CS, Smith A (1989) Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatogrpahy. Lett Appl Microbiol 9(1):5-8.
67. Huber JA, et al. (2007) Microbial population structures in the deep marine biosphere. Science 318(5847):97-100.
68. Huse SM, et al. (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4(11):e1000255.
69. Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12(7):1889-1898.
70. Giardine B, et al. (2005) Galaxy: A platform for interactive large-scale genome analysis. Genome Res 15(10):1451-1455.
71. Schloss PD, et al. (2009) Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537-7541.
72. Friedline CJ, Franklin RB, McCallister SL, Rivera MC (2012) Microbial community diversity of the eastern Atlantic Ocean reveals geographic differences. Biogeosciences Discuss 9:109-150.
73. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261-5267.
74. Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40(3-4):237-264.
75. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131(2):479-491.
76. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32-46.