Chapter 10 : The Interaction of Bile Salts with Pathogenic and Nonpathogenic Intestinal Bacteria

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This chapter provides an overview of bile composition and conjugation mediated by the normal flora and its aforementioned antimicrobial effects. It discusses known molecular mechanisms behind bile resistance and the role bile has in altering the virulence of enteric pathogens. Fasting and malnourishment have been shown to decrease the amount of bile in the intestine and, consequently, leave individuals vulnerable to bacterial pathogens. Similar to commensal enteric bacteria, pathogenic contains bile salt hydrolases (BSH) genes thought to confer bile resistance and successful colonization and disease manifestation. Probiotics researchers suggest that subsequent limitations to enterohepatic circulation in the presence of unconjugated bile acids cause enhanced fecal loss of bile salts. The chapter talks about the effect of bile on pathogenic bacteria. Adaptability to the harsh effects of bile acids is a critical component of survival for gastrointestinal pathogens. Both conjugated and unconjugated bile salts increased expression of the CmeABC efflux pump, while other antimicrobials, including chloramphenicol, ethidium bromide, and erythromycin, did not affect transcription of cmeABC. Surface plasmon resonance provided evidence that bile salts were capable of inhibiting binding of CmeR to the cmeABC promoter, leading to increased pump expression and elevated bile resistance. Interestingly, the presence of bile salts in culture media enhanced the resistance of to multiple antibiotics, including cefotaxime, novobiocin, and fusidic acid. As long as the integrity of the normal microbial flora is maintained, compounds that are mentioned in the chapter could be manufactured to target known factors contributing to bile resistance.

Citation: Crawford R, Gunn J. 2009. The Interaction of Bile Salts with Pathogenic and Nonpathogenic Intestinal Bacteria, p 183-200. In Jaykus L, Wang H, Schlesinger L (ed), Food-Borne Microbes. ASM Press, Washington, DC. doi: 10.1128/9781555815479.ch10
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Bacterial intestinal pathogens discussed in this chapter that are affected by bile. Listed are microbes known to cause acute or chronic disease in the gallbladder or the intestinal tract. Interactions between invading microorganisms and bile, which is produced in the liver and found in the intestine and gallbladder, affect various genes and virulence properties (listed) that enhance colonization and persistence.

Citation: Crawford R, Gunn J. 2009. The Interaction of Bile Salts with Pathogenic and Nonpathogenic Intestinal Bacteria, p 183-200. In Jaykus L, Wang H, Schlesinger L (ed), Food-Borne Microbes. ASM Press, Washington, DC. doi: 10.1128/9781555815479.ch10
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1. Al-Jabri, A. A.,, M. D. Wigg,, E. Elias,, R. Lamkin,, C. O. Mills, and, J. S. Oxford. 2000. In vitro anti-HIV-1 virucidal activity of tyrosineconjugated tri- and dihydroxy bile salt derivatives. J. Antimicrob. Chemother. 45: 617621.
2. Allen, K. J., and, M. W. Griffiths. 2001. Effect of environmental and chemotactic stimuli on the activity of the Campylobacter jejuni flaA σ 28 promoter. FEMS Microbiol. Lett. 205: 4348.
3. Ananieva, O.,, I. Nilsson,, T. Vorobjova,, R. Uibo, and, T. Wadstrom. 2002. Immune responses to bile-tolerant Helicobacter species in patients with chronic liver diseases, a randomized population group, and healthy blood donors. Clin. Diagn. Lab. Immunol. 9: 11601164.
4. Anderson, L. P. 2001. New Helicobacter species in humans. Dig. Dis. 19: 112115.
5. Apostolov, E.,, W. A. Al-Soud,, I. Nilsson,, I. Kornilovska,, V. Usenko,, V. Lyzogubov,, Y. Gaydar,, T. Wadstrom, and, A. Ljungh. 2005. Helicobacter pylori and other Helicobacter species in gallbladder and liver of patients with chronic cholecystitis detected by immunological and molecular methods. Scand. J. Gastroenterol. 40: 96102.
6. Atabay, H. I.,, J. E. Corry, and, S. L. On. 1998. Identification of unusual Campylobacter-like isolates from poultry products as Helicobacter pullorum. J. Appl. Microbiol. 84: 10171024.
7. Baranova, N., and, H. Nikaido. 2002. The BaeSR two-component regulatory system activates transcription of the yegMNOB (mgtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. J. Bacteriol. 184: 41684176.
8. Begley, M.,, C. G. M. Gahan, and, C. Hill. 2002. Bile stress response in Listeria monocytogenes L028: adaptation, cross-protection and identification of genetic loci involved in bile resistance. Appl. Environ. Microbiol. 68: 60056012.
9. Begley, M.,, C. G. M. Gahan, and, C. Hill. 2005. The interaction between bacteria and bile. FEMS Microbiol. Rev. 29: 625651.
10. Begley, M.,, R. D. Sleator,, C. G. M. Gahan, and, C. Hill. 2005. Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infect. Immun. 73: 894904.
11. Bina, J.,, J. Zhu,, M. Dziejman,, S. Faruque,, S. Calderwood, and, J. J. Mekalanos. 2004. ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. Proc. Natl. Acad. Sci. USA 101: 28012806.
12. Bina, J. E.,, D. Provenzano,, C. Wang,, X. R. Bina, and, J. J. Mekalanos. 2006. Characterization of the Vibrio cholerae vexAB and vexCD efflux systems. Arch. Microbiol. 186: 171181.
13. Blocker, A.,, K. Komoriya, and, S. Aizawa. 2003. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl. Acad. Sci. USA 100: 30273030.
14. Blum, H. E.,, L. Stowring,, A. Figus,, C. K. Montgomery,, A. T. Haase, and, G. N. Vyas. 1983. Detection of hepatitis B virus DNA in hepatocytes, bile duct epithelium, and vascular elements by in situ hybridization. Proc. Natl. Acad. Sci. USA 80: 66856688.
15. Boggs, J. M. 1987. Lipid intermolecular hydrogen bonding: influence on structural organization and membrane function. Biochim. Biophys. Acta 906: 353404.
16. Bohr, U. R. M.,, D. Kuester,, F. Meyer,, T. Wex,, M. Stillert,, A. Csepregi,, H. Lippert,, A. Roessner, and, P. Malfertheiner. 2007. Low prevalence of Helicobacteraceae in gallstone disease and gallbladder carcinoma in the German population. Clin. Microbiol. Infect. 13: 525531.
17. Bortolini, O.,, A. Medici, and, S. Poli. 1997. Biotransformations on steroid nucleus of bile acids. Steroids 62: 564577.
18. Burnens, A. P.,, J. Stanley, and, J. Nicolet. 1994. Possible association of Helicobacter pullorum with lesions of vibrionic hepatitis in poultry, p. 12591274. In D. G. Newell,, J. M. Ketley, and, R. A. Feldman (ed.), Campylobacters, Helicobacters, and Related Organisms. Plenum Press, New York, NY.
19. Caygill, C. P.,, M. J. Hill,, M. Braddick, and, J. C. Sharp. 1994. Cancer mortality in chronic typhoid and paratyphoid carriers. Lancet 343: 8384.
20. Chakrabarti, S. R.,, K. Chaudhuri,, K. Sen, and, J. Das. 1996. Porins of Vibrio cholerae: purification and characterization of OmpU. J. Bacteriol. 178: 524530.
21. Champion, G. A.,, M. N. Neely,, M. A. Brennan, and, V. J. DiRita. 1997. A branch in the ToxR regulatory cascade of Vibrio cholerae revealed by characterization of toxT mutant strains. Mol. Microbiol. 23: 323331.
22. Chang, K.,, S. V. Sosnovtsev,, G. Belliot,, Y. Kim,, L. J. Saif, and, K. Y. Green. 2004. Bile acids are essential for porcine enteric calicivirus replication in association with down-regulation of signal transducer and activator of transcription 1. Proc. Natl. Acad. Sci. USA 101: 87338738.
23. Chatterjee, A.,, P. K. Dutta, and, R. Chowdhury. 2007. Effect of fatty acids and cholesterol present in bile on expression of virulence factors and motility of Vibrio cholerae. Infect. Immun. 75: 19461953.
24. Chen, W.,, J. Liu, and, C. Gluud. 2003. Bile acids for viral hepatitis. Cochrane Database Syst. Rev. 2: CD003181.
25. Cheville, A. M.,, K. W. Arnold,, C. Buchreiser,, C. M. Cheng, and, C. W. Casper. 1996. rpoS regulation of acid, heat, and salt tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 62: 18221824.
26. Chowdhury, R.,, G. K. Sahu, and, J. Das. 1996. Stress response in pathogenic bacteria. J. Biosci. 21: 149160.
27. Coleman, J. P., and, L. L. Hudson. 1995. Cloning and characterization of a conjugated bile acid hydrolase gene from Clostridium perfringens. Appl. Environ. Microbiol. 61: 25142520.
28. Crosignani, A.,, K. D. Setchell,, P. Invernizzi,, A. Larghi,, C. M. Rodrigues, and, M. Podda. 1996. Clinical pharmacokinetics of therapeutic bile acids. Clin. Pharmacokinet. 30: 333358.
29. de Jesus, M. C.,, A. A. Urban,, M. E. Marasigan, and, D. E. Barnett Foster. 2005. Acid and bile-salt stress of enteropathogenic Escherichia coli enhances adhesion to epithelial cells and alters glycolipid receptor binding specificity. J. Infect. Dis. 192: 14301440.
30. De Smet, I.,, L. Van Hoorde,, N. De Sayer,, M. Vande Woestyne, and, W. Verstraete. 1994. In vitro study of bile salt hydrolase (BSH) activity of BSH isogenic Lactobacillus plantarum 80 strains and estimation of cholesterol lowering through enhanced BSH activity. Microb. Ecol. Health Dis. 7: 315329.
31. DiGiuseppe, P. A., and, T. J. Silhavy. 2003. Signal detection and target gene induction by the CpxRA two-component system. J. Bacteriol. 185: 24322440.
32. Duret, G., and, A. H. Delcour. 2006. Deoxycholic acid blocks Vibrio cholerae OmpT but not OmpU porin. J. Biol. Chem. 281: 1989919905.
33. Dussurget, O.,, D. Cabanes,, P. Dehoux,, M. Lecuit,, C. Buchrieser,, P. Glaser, and, P. Gossart. 2002. Listeria monocytogenes bile salt hydrolase is a prfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol. Microbiol. 45: 10951106.
34. Edenharder, R. 1984. Dehydroxylation of cholic acid at C12 and epimerization at C5 and C7 by Bacteroides species. J. Steroid Biochem. 21: 413420.
35. Edenharder, R., and, K. Mielek. 1984. Epimerization, oxidation and reduction of bile acids by Eubacterium lentum. Syst. Appl. Microbiol. 5: 287298.
36. Flahaut, S.,, A. Hartke,, J. C. Giard,, A. Benachour,, P. Boutibonnes, and, A. Auffray. 1996. Relationship between stress response towards bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiol. Lett. 138: 4954.
37. Flahaut, S.,, J. Frere,, P. Boutibonnes, and, Y. Auffray. 1996. Comparison of the bile salts and sodium dodecyl sulfate stress responses in Enterococcus faecalis. Appl. Environ. Microbiol. 62: 24162420.
38. Formal, S. B.,, T. L. Hale, and, P. J. Sansonetti. 1983. Invasive enteric pathogens. Rev. Infect. Dis. 5: S702S707.
39. Fox, J. G.,, F. E. Dewhirst,, J. G. Tully,, B. J. Paster,, L. Yan,, N. S. Taylor,, M. J. Collins, Jr.,, P. L. Gorelick, and, J. M. Ward. 1994. Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J. Clin. Microbiol. 32: 12381245.
40. Fox, J. G.,, F. E. Dewhirst,, Z. Shen,, Y. Feng,, N. S. Taylor,, B. J. Paster,, R. L. Ericson,, C. N. Lau,, P. Correa,, J. C. Araya, and, I. Roa. 1998. Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology 114: 755763.
41. Fox, J. G.,, L. L. Yan,, F. E. Dewhirst,, B. J. Paster,, B. Shames,, J. C. Murphy,, A. Hayward,, J. C. Belcher, and, E. N. Mendes. 1995. Helicobacter bilis sp. nov., a novel Helicobacter species isolated from bile, livers, and intestines of aged, inbred mice. J. Clin. Microbiol. 33: 445454.
42. Franklund, C. V.,, S. F. Baron, and, P. B. Hylemon. 1993. Characterization of the baiH gene encoding a bile acid-inducible NADH:flavin oxidoreductase from Eubacterium sp. strain VPI 12708. J. Bacteriol. 175: 30023012.
43. Gahan, C. G. M., and, C. Hill. 1999. The relationship between acid stress responses and virulence in Salmonella typhimurium and Listeria monocytogenes. Int. J. Food Microbiol. 50: 93100.
44. Geijtenbeek, T. B.,, D. Kwon,, R. Torensma,, S. van Vliet,, G. van Duijnhoven,, J. Middel,, I. Cornelissen,, H. Nottet,, V. Kewal-Ramini, and, D. Littman. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587597.
45. Geijtenbeek, T. B.,, R. Torensma,, S. van Vliet,, G. van Duijnhoven,, G. Adema,, Y. van Kooyk, and, C. Figdor. 2000. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100: 578585.
46. Grill, J. P.,, C. Cayuela,, J. M. Antoine, and, F. Schneider. 2000. Isolation and characterization of a Lactobacillus amylovorus mutant depleted in conjugated bile salt hydrolase activity: relation between activity and bile salt resistance. J. Appl. Microbiol. 89: 553563.
47. Grill, J. P.,, S. Perrin, and, F. Schneider. 2000. Bile toxicity to some bifidobacteria strains: role of conjugated bile salt hydrolase and pH. Can. J. Microbiol. 46: 878884.
48. Grkovic, S.,, M. H. Brown, and, R. A. Skurray. 2002. Regulation of bacterial drug export systems. Microbiol. Mol. Biol. Rev. 66: 671701.
49. Gunn, J. S. 2000. Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2: 907913.
50. Gupta, S., and, R. Chowdhury. 1997. Bile affects production of virulence factors and motility of Vibrio cholerae. Infect. Immun. 65: 11311134.
51. Haghjoo, E., and, J. E. Galan. 2007. Identification of a transcriptional regulator that controls intracellular gene expression in Salmonella Typhi. Mol. Microbiol. 64: 15491561.
52. Hale, T. L. 1991. Genetic basis of virulence in Shigella species. Microbiol. Rev. 55: 206224.
53. Hardison, W. G. 1978. Hepatic taurine concentration and dietary taurine as regulators of bile acid conjugation with taurine. Gastroenterology 75: 7175.
54. Hardy, J.,, K. P. Francis,, M. DeBoer,, P. Chu,, K. Gibbs, and, C. H. Contag. 2004. Extracellular replication of Listeria monocytogenes in the murine gallbladder. Science 303: 851853.
55. Haruna, Y.,, T. Kanda,, M. Honda,, T. Takao, and, N. Hayashi. 2001. Detection of hepatitis C virus in the bile and bile duct epithelial cells of hepatitis C virus-infected patients. Hepatology 33: 977980.
56. Herold, B. C.,, R. Kirkpatrick,, D. Marcellino,, A. Travelstead,, V. Pilipenko,, H. Krasa,, J. Bremer,, L. J. Dong, and, M. D. Cooper. 1999. Bile salts. Natural detergents for the prevention of sexually transmitted diseases. Antimicrob. Agents Chemother. 43: 745751.
57. Hofmann, A. F. 1989. Overview of bile secretion, p. 549566. In Handbook of Physiology, section 6, vol. 3. The Gastrointestinal System. Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion. American Physiological Society, Bethesda, MD.
58. Hofmann, A. F. 1998. Bile secretion and the enterohepatic circulation of bile acids, p. 937948. In M. Feldman,, B. F. Scharschmidt, and, M. H. Sleisenger (ed.), Sleisenger and Fordtran’s Gastrointestinal and Liver Disease, 6th ed. W. B. Saunders, Co., Philadelphia, PA.
59. Hofmann, A. F. 1999. Bile acids: the good, the bad, and the ugly. News Physiol. Sci. 14: 2429.
60. Hofmann, A. F., and, A. Roda. 1984. Physicochemical properties of bile acids and their relationship to biological properties: an overview of the problem. J. Lipid Res. 25: 14771489.
61. Hofmann, A. F., and, K. J. Mysels. 1992. Bile acid solubility and precipitation in vitro and in vivo: the role of conjugation, pH and Ca 2+ ions. J. Lipid Res. 33: 617626.
62. Hu, J.,, M. B. Gardner, and, C. J. Miller. 2000. Simian immunodeficiency virus rapidly penetrates the cervicovaginal mucosa after intravaginal inoculation and infects intraepithelial dendritic cells. J. Virol. 74: 60876095.
63. Hung, D. T., and, J. J. Mekalanos. 2005. Bile acids induce cholera toxin expression in Vibrio cholerae in a ToxT-independent manner. Proc. Natl. Acad. Sci. USA 102: 30283033.
64. Hung, D. T.,, J. Zhu,, D. Sturtevant, and, J. J. Mekalanos. 2006. Bile acids stimulate biofilm formation in Vibrio cholerae. Mol. Microbiol. 59: 193201.
65. Jeong, K. C.,, M. Y. Kang,, C. Heimke,, J. A. Shere,, I. Erol, and, C. W. Kaspar. 2007. Isolation of Escherichia coli O157:H7 from the gallbladder of inoculated and naturally-infected cattle. Vet. Microbiol. 119: 339345.
66. Johnson, L. R. 1998. Bile secretion and gallbladder function, p. 465471. In L. R. Johnson (ed.), Essential Medical Physiology, 2nd ed. Lippincott–Raven, Philadelphia, PA.
67. Kaper, J. B.,, J. G. Morris, and, M. M. Levine. 1995. Cholera. Clin. Microbiol. Rev. 8: 4886.
68. Knarreborg, A.,, R. M. Engberg,, S. K. Jensen, and, B. B. Jensen. 2002. Quantitative determination of bile salt hydrolase activity in bacteria isolated from the small intestine of chickens. Appl. Environ. Microbiol. 68: 64256428.
69. Lacroix, F. J.,, C. Ayoyne,, C. Pinault,, M. Y. Popoff, and, P. Pardon. 1995. Salmonella typhimurium TnphoA mutants with increased sensitivity to biological and chemical detergents. Res. Microbiol. 146: 659670.
70. Lefkowitch, J. H. 1993. Pathological diagnosis of chronic hepatitis C: a multicenter comparative study with chronic hepatitis B. Gastroenterology 104: 595603.
71. Lin, J., and, A. Martinez. 2006. Effect of efflux pump inhibitors on bile resistance and in vivo colonization of Campylobacter jejuni. J. Antimicrob. Chemother. 58: 966972.
72. Lin, J.,, C. Cagliero,, B. Guo,, Y. Barton,, M. Maurel,, S. Payot, and, Q. Zhang. 2005. Bile salts modulate expression of the CmeABC multidrug efflux pump in Campylobacter jejuni. J. Bacteriol. 187: 74177424.
73. Lin, J.,, M. Akiba,, O. Sahin, and, Q. Zhang. 2005. CmeR functions as a transcriptional repressor for the multidrug efflux pump CmeABC in Campylobacter jejuni. Antimicrob. Agents Chemother. 49: 10671075.
74. Lin, J.,, O. Sahin,, L. Overbye Michel, and, Q. Zhang. 2003. Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect. Immun. 71: 42504259.
75. Lomovskaya, O., and, K. Lewis. 1992. Emr, an Escherichia coli locus for multidrug resistance. Proc. Natl. Acad. Sci. USA 89: 89388942.
76. Lomovskaya, O.,, K. Lewis, and, A. Matin. 1995. EmrR is a negative regulator of the Escherichia coli multidrug resistance pump EmrAB. J. Bacteriol. 177: 23282334.
77. Luo, N.,, O. Sahin,, J. Lin,, L. O. Michel, and, Q. Zhang. 2003. In vivo selection of Campylobacter isolates with high levels of fluoroquinolone resistance associated with gyrA mutations and the function of the CmeABC efflux pump. Antimicrob. Agents Chemother. 47: 390394.
78. Ma, D.,, D. N. Cook,, J. E. Hearst, and, H. Nikaido. 1994. Efflux pumps and drug resistance in gram-negative bacteria. Trends Microbiol. 2: 489493.
79. Macdonald, I. A., and, D. M. Hutchison. 1982. Epimerization versus dehydroxylation of the 7α-hydroxyl-group of primary bile acids: competitive studies with Clostridium absonum and 7α-dehydroxylating bacteria ( Eubacterium sp.). J. Steroid Biochem. 17: 295303.
80. Maurer, K. J.,, A. B. Rogers,, Z. Ge,, A. J. Wiese,, M. C. Carey, and, J. G. Fox. 2006. Helicobacter pylori and cholesterol gallstone formation in C57L/J mice: a prospective study. Am. J. Physiol. Gastrointest. Liver Physiol. 290: G175G182.
81. McPhee, M. S., and, N. J. Greenberger. 1987. Diseases of the gallbladder and bile duct, p. 13581362. In R. T. Harrison (ed.), Harrison’s Principles of Internal Medicine, 11th ed. McGraw-Hill, New York, NY.
82. Merrell, D. S.,, S. M. Butler,, F. Qadri,, N. A. Dolganov,, A. Alam,, M. B. Cohen,, S. B. Calderwood,, G. K. Schoolnik, and, A. Camilli. 2002. Host-induced epidemic spread of the cholera bacterium. Nature 417: 642645.
83. Mohapatra, N. P.,, S. Soni,, B. L. Bell,, R. Warren,, R. K. Ernst,, A. Muszynski,, R. W. Carlson, and, J. S. Gunn. 2007. Identification of an orphan response regulator required for the virulence of Francisella spp. and transcription of pathogenicity island genes. Infect. Immun. 75: 33053314.
84. Mower, H. F.,, R. M. Ray,, R. Shoff,, G. N. Stemmermann,, A. Nomura,, G. A. Glober,, S. Kamiyama,, A. Shimada, and, H. Yamakawa. 1979. Fecal bile acids in two Japanese populations with different colon cancer risks. Cancer Res. 39: 328331.
85. Moxley, R. A. 2004. Escherichia coli O157:H7: an update on intestinal colonization and virulence mechanisms. Anim. Health Res. Rev. 5: 1533.
86. Naarding, M. A.,, A. M. Dirac,, I. S. Ludwig,, D. Speijer,, S. Lindquist,, E. L. Vestman,, M. J. Stax,, T. B. Geijenbeek,, G. Pollakis,, O. Hernell, and, W. A. Paxton. 2006. Bile salt-stimulated lipase from human milk binds DC-SIGN and inhibits human immunodeficiency virus type 1 transfer to CD4 + T cells. Antimicrob. Agents Chemother. 50: 33673374.
87. Naarding, M. A.,, I. S. Ludwig,, F. Groot,, B. Berkhout,, T. B. Geijenbeek,, G. Pollakis, and, W. A. Paxton. 2005. Lewis X component in human milk binds DC-SIGN and inhibits HIV-1 transfer to CD4 + T lymphocytes. J. Clin. Investig. 115: 32563264.
88. Nachamkin, I.,, B. M. Allos, and, T. Ho. 1998. Campylobacter species and Guillain-Barré syndrome. Clin. Microbiol. Rev. 11: 555567.
89. Olive, A. J.,, R. Kenjale,, M. Espina,, D. S. Moore,, W. L. Picking, and, W. D. Picking. 2007. Bile salts stimulate recruitment of IpaB to the Shigella flexneri surface, where it colocalizes with IpaD at the tip of the type III secretion needle. Infect. Immun. 75: 26262629.
90. Opleta, K.,, J. D. Butzner,, E. A. Shaffer, and, D. G. Gall. 1988. The effect of protein-calorie malnutrition on the developing liver. Pediatr. Res. 23: 505508.
91. Paumgartner, G., and, T. Sauerbruch. 1991. Gallstones: pathogenesis. Lancet 338: 11171121.
92. Pearce, M. C.,, C. Jenkins,, L. Vali,, A. W. Smith,, H. I. Knight,, T. Cheasty,, H. R. Smith,, G. J. Gunn,, M. E. J. Woolhouse,, S. G. B. Amyes, and, G. Frankel. 2004. Temporal shedding pattern and virulence factors of Escherichia coli O157 serogroups O26, O103, O111, O145, and O157 in a cohort of beef calves and their dams. Appl. Environ. Microbiol. 70: 17081716.
93. Pope, L. M.,, K. E. Reed, and, S. M. Payne. 1995. Increased protein secretion and adherence to HeLa cells by Shigella spp. following growth in the presence of bile salts. Infect. Immun. 63: 36423648.
94. Pope, M.,, S. Gezelter,, N. Gallo,, L. Hoffman, and, R. M. Steinman. 1995. Low levels of HIV-1 infection in cutaneous dendritic cells promote extensive viral replication upon binding to memory CD4 + T cells. J. Exp. Med. 182: 20452056.
95. Prouty, A. M., and, J. S. Gunn. 2000. Salmonella enterica serovar Typhimurium invasion is repressed in the presence of bile. Infect. Immun. 68: 67636769.
96. Prouty, A. M., and, J. S. Gunn. 2003. Comparative analysis of Salmonella enterica serovar Typhimurium biofilm formation on gallstones and on glass. Infect. Immun. 71: 71547158.
97. Prouty, A. M.,, I. E. Brodsky,, J. Manos,, R. Belas,, S. Falkow, and, J. S. Gunn. 2004. Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol. Med. Microbiol. 41: 177185.
98. Prouty, A. M.,, I. E. Brodsky,, S. Falkow, and, J. S. Gunn. 2004. Bile-salt-mediated induction of antimicrobial and bile resistance in Salmonella typhimurium. Microbiology 150: 775783.
99. Prouty, A. M.,, J. C. Van Velkinburgh, and, J. S. Gunn. 2002. Salmonella enterica serovar Typhimurium resistance to bile: identification and characterization of the tolQRA cluster. J. Bacteriol. 184: 12701276.
100. Prouty, A. M.,, W. H. Schwesinger, and, J. S. Gunn. 2002. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect. Immun. 70: 26402649.
101. Provenzano, D., and, K. E. Klose. 2000. Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proc. Natl. Acad. Sci. USA 97: 1022010224.
102. Provenzano, D.,, D. A. Schuhmacher,, J. L. Barker, and, K. E. Klose. 2000. The virulence regulatory protein ToxR mediates enhanced bile resistance in Vibrio cholerae and other pathogenic Vibrio species. Infect. Immun. 68: 14911497.
103. Putman, M.,, H. W. van Veen, and, W. N. Konings. 2000. Molecular properties of bacterial multidrug transporters. Microbiol. Mol. Biol. Rev. 64: 672693.
104. Ramos-Morales, F.,, A. I. Prieto,, C. R. Beuzon,, D. W. Holden, and, J. Casadesus. 2003. Role for Salmonella enterica enterobacterial common antigen in bile resistance and virulence. J. Bacteriol. 185: 53285332.
105. Reed, R. P.,, F. O. Wegerhoff, and, A. D. Rothberg. 1996. Bacteraemia in malnourished African children. Ann. Trop. Paediatr. 16: 6168.
106. Rivera-Amill, V.,, B. J. Kim,, J. Seshu, and, M. E. Konkel. 2001. Secretion of the virulence-associated Campylobacter invasion antigens from Campylobacter jejuni requires a stimulatory signal. J. Infect. Dis. 183: 16071616.
107. Schlech, W. F. 2000. Foodborne listeriosis. Clin. Infect. Dis. 31: 770775.
108. Schuhmacher, D. A., and, K. E. Klose. 1999. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 181: 15081514.
109. Shimeles, D., and, S. Lulseged. 1994. Clinical profile and pattern of infection in Ethiopian children with severe protein-energy malnutrition. East Afr. Med. J. 71: 264267.
110. Sjovall, J. 1959. Dietary glycine and taurine on bile acid conjugation on man; bile acids and steroids 75. Proc. Soc. Exp. Biol. Med. 100( 4) : 676678.
111. Sleator, R. D.,, H. H. Wemekamp-Kamphuis,, C. G. M. Gahan,, T. Abee, and, C. Hill. 2005. A PrfA-regulated bile exclusion system (BilE) is a novel virulence factor in Listeria monocytogenes. Mol. Microbiol. 55: 11831195.
112. Slutsker, L.,, S. F. Altekruse, and, D. L. Swerdlow. 1998. Foodborne diseases. Emerging pathogens and trends. Infect. Dis. Clin. N. Am. 12: 199216.
113. Stanley, J. 1994. Helicobacter pullorum sp. nov.—genotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiology 140: 34413449.
114. Stintzi, A.,, D. Marlow,, K. Palyada,, H. Naikare,, R. Panciera,, L. Whitworth, and, C. Clarke. 2005. Use of genomewide expression profiling and mutagenesis to study the intestinal lifestyle of Campylobacter jejuni. Infect. Immun. 73: 17971810.
115. Stoffregen, W. C.,, J. F. Pohlenz, and, E. A. Dean-Nystrom. 2004. Escherichia coli O157:H7 in the gallbladders of experimentally infected calves. J. Vet. Diagn. Investig. 16: 7983.
116. Tauxe, R. V. 2002. Emerging foodborne pathogens. Int. J. Food Microbiol. 78: 3141.
117. Thanassi, D. G.,, L. W. Cheng, and, H. Nikaido. 1997. Active efflux of bile salts by Escherichia coli. J. Bacteriol. 179: 25122518.
118. Tiwari, S. K.,, A. A. Khan,, M. Ibrahim,, M. A. Habeeb, and, C. M. Habibullah. 2006. Helicobacter pylori and other Helicobacter species DNA in human bile samples from patients with various hepato-biliary diseases. World J. Gastroenterol. 12: 21812186.
119. Torres, A. G.,, C. B. Tutt,, L. Duval,, V. Popov,, A. B. Nasr,, J. Michalski, and, I. C. Scaletsky. 2007. Bile salts induce expression of the afimbrial LDA adhesin of atypical enteropathogenic Escherichia coli. Cell. Microbiol. 9: 10391049.
120. Trabulsi, L. R.,, R. Keller, and, T. A. Tardelli Gomes. 2002. Typical and atypical enteropathogenic Escherichia coli. Emerg. Infect. Dis. 8: 508513.
121. Van Eldere, J.,, P. Celis,, G. De Pauw,, E. Lesaffre, and, H. Eyssen. 1996. Tauroconjugation of cholic acid stimulates 7α-dehydroxylation by fecal bacteria. Appl. Environ. Microbiol. 62: 656661.
122. Van Velkinburgh, J. C., and, J. S. Gunn. 1999. PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect. Immun. 67: 16141622.
123. Vazquez-Boland, J. A.,, M. Kuhn,, P. Berche,, T. Chakraborty,, G. Dominguez-Bernal,, W. Goebel,, B. Gonzalez-Zorn,, J. Wehland, and, J. Kreft. 2001. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14: 584640.
124. Ward, J. M.,, J. G. Fox,, M. R. Anver,, D. C. Haines,, C. V. George,, M. J. Collins,, P. L. Gorelick,, K. Nagashima,, M. A. Gonda, and, R. V. Gilden. 1994. Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J. Natl. Cancer Inst. 86: 12221227.
125. Welton, J. C.,, J. S. Marr, and, S. M. Friedman. 1979. Association between hepatobiliary cancer and typhoid carrier state. Lancet i: 791794.
126. Xu, Q.,, M. Dziejman, and, J. J. Mekalanos. 2003. Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro. Proc. Natl. Acad. Sci. USA 100: 12861291.
127. Zgurskaya, H. I., and, H. Nikaido. 1999. Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proc. Natl. Acad. Sci. USA 96: 71907195.

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