Toxin-mediated effects on the innate mucosal defenses: Implications for enteric vaccines

Infection and Immunity

Volumn 77, Issue 12, 2009, Pages 5206-5215

  Glenn, Gregory M ^a   Francis, David H ^b   Danielsen, E Michael ^c  

^a Intercell USA   (United States)

^b SOUTH DAKOTA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITOXIN; BACTERIAL VACCINE; CHOLERA TOXIN; CYCLIC AMP; ENTERIC VACCINE; ENTEROTOXIN; ESCHERICHIA COLI ENTEROTOXIN; GANGLIOSIDE GM1 ANTIBODY; GLYCOSPHINGOLIPID; HEAT LABILE ENTEROTOXIN; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; LIPID BINDING PROTEIN; TOXIN ANTIBODY; UNCLASSIFIED DRUG;

BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; ENDOCYTOSIS; ENTEROTOXIGENIC ESCHERICHIA COLI; GASTROINTESTINAL INFECTION; HUMAN; INNATE IMMUNITY; INTESTINE CELL; LIPID RAFT; MICROENVIRONMENT; MUCOSAL IMMUNITY; NUTRIENT; PATHOGENICITY; PRIORITY JOURNAL; REGULATORY MECHANISM; SECRETION; SHORT SURVEY; TARGET CELL;

BACTERIAL TOXINS; CHOLERA TOXIN; CHOLERA VACCINES; ENTEROTOXINS; ESCHERICHIA COLI PROTEINS; ESCHERICHIA COLI VACCINES; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; MODELS, BIOLOGICAL;

EID: 72449165391     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00712-09     Document Type: Short Survey

References (99)

1. Allen, K. P., M. M. Randolph, and J. M. Fleckenstein. 2006. Importance of heat-labile enterotoxin in colonization of the adult mouse small intestine by human enterotoxigenic Escherichia coli strains. Infect. Immun. 74:869-875.
2. Berberov, E. M., Y. Zhou, D. H. Francis, M. A. Scott, S. D. Kachman, and R. A. Moxley. 2004. Relative importance of heat-labile enterotoxin in the causation of severe diarrheal disease in the gnotobiotic piglet model by a strain of enterotoxigenic Escherichia coli that produces multiple enterotoxins. Infect. Immun. 72:3914-3924.
3. Bergman, P., L. Johansson, V. Asp, L. Plant, G. H. Gudmundsson, A. B. Jonsson, and B. Agerberth. 2005. Neisseria gonorrhoeae downregulates expression of the human antimicrobial peptide LL-37. Cell. Microbiol. 7:1009-1017.
4. Bourgeois, A. L., J. Halpern, S. Grahek, S. Golub, B. Gustafsson, A.-M. Svennerholm, O. Torres, J. Belkind-Gerson, D. Sanchez, I. Nyquist, G. Wiklund, A. Karnell, J. Kyle, and D. A. Sack. 2007. Vaccination of travelers to Guatemala (GU) and Mexico (MX) with an oral killed vaccine (OKV) for enterotoxigenic E. coli (ETEC): impact of vaccine "take" on risk of ETEC disease and infection with enteric pathogens, poster 33. Presented at the 4th International Conference on Vaccines for Enteric Diseases (VED 2007), Lisbon, Portugal, 25-27 April 2007.
5. Catron, D. M., M. D. Sylvester, Y. Lange, M. Kadekoppala, B. D. Jones, D. M. Monack, S. Falkow, and K. Haldar. 2002. The Salmonella-containing vacuole is a major site of intracellular cholesterol accumulation and recruits the GPI-anchored protein CD55. Cell. Microbiol. 4:315-328.
6. Chakraborty, K., S. Ghosh, H. Koley, A. K. Mukhopadhyay, T. Ramamurthy, D. R. Saha, D. Mukhopadhyay, S. Roychowdhury, T. Hamabata, Y. Takeda, and S. Das. 2008. Bacterial exotoxins downregulate cathelicidin (hCAP-18/ LL-37) and human beta-defensin 1 (HBD-1) expression in the intestinal epithelial cells. Cell. Microbiol. 10:2520-2537.
7. Chinnapen, D. J., H. Chinnapen, D. Saslowsky, and W. I. Lencer. 2007. Rafting with cholera toxin: endocytosis and trafficking from plasma membrane to ER. FEMS Microbiol. Lett. 266:129-137.
8. Christiansen, K., and J. Carlsen. 1981. Microvillus membrane vesicles from pig small intestine. Purity and lipid composition. Biochim. Biophys. Acta 647:188-195.
9. Clemens, J. D., D. A. Sack, J. R. Harris, J. Chakraborty, M. R. Khan, B. F. Stanton, B. A. Kay, M. U. Khan, M. Yunus, W. Atkinson, et al. 1986. Field trial of oral cholera vaccines in Bangladesh. Lancet ii:124-127.
10. Clemens, J. D., D. A. Sack, J. R. Harris, J. Chakraborty, P. K. Neogy, B. Stanton, N. Huda, M. U. Khan, B. A. Kay, M. R. Khan, et al. 1988. Cross-protection by B subunit-whole cell cholera vaccine against diarrhea associated with heat-labile toxin-producing enterotoxigenic Escherichia coli: results of a large-scale field trial. J. Infect. Dis. 158:372-377.
11. Clemens, J. D., D. A. Sack, J. R. Harris, F. Van Loon, J. Chakraborty, F. Ahmed, M. R. Rao, M. R. Khan, M. Yunus, N. Huda, et al. 1990. Field trial of oral cholera vaccines in Bangladesh: results from three-year follow-up. Lancet 335:270-273.
12. Clements, J. D. 1990. Construction of a nontoxic fusion peptide for immunization against Escherichia coli strains that produce heat-labile and heatstable enterotoxins. Infect. Immun. 58:1159-1166.
13. Clements, J. D., R. J. Yancey, and R. A. Finkelstein. 1980. Properties of homogeneous heat-labile enterotoxin from Escherichia coli. Infect. Immun. 29:91-97.
14. Coster, T. S., M. K. Wolf, E. R. Hall, F. J. Cassels, D. N. Taylor, C. T. Liu, F. C. Trespalacios, A. DeLorimier, D. R. Angleberger, and C. E. McQueen. 2007. Immune response, ciprofloxacin activity, and gender differences after human experimental challenge by two strains of enterotoxigenic Escherichia coli. Infect. Immun. 75:252-259.
15. Crane, J. K., S. S. Choudhari, T. M. Naeher, and M. E. Duffey. 2006. Mutual enhancement of virulence by enterotoxigenic and enteropathogenic Escherichia coli. Infect. Immun. 74:1505-1515.
16. Cuatrecasas, P. 1973. Interaction of Vibrio cholerae enterotoxin with cell membranes. Biochemistry (Moscow) 12:3547-3558.
17. Danielsen, E. M., and B. van Deurs. 1997. Galectin-4 and small intestinal brush border enzymes form clusters. Mol. Biol. Cell 8:2241-2251.
18. Dickinson, B. L., K. Badizadegan, Z. Wu, J. C. Ahouse, X. Zhu, N. E. Simister, R. S. Blumberg, and W. I. Lencer. 1999. Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J. Clin. Investig. 104:903-911.
19. Duncan, M. J., J. S. Shin, and S. N. Abraham. 2002. Microbial entry through caveolae: variations on a theme. Cell. Microbiol. 4:783-791.
20. Edwards, R. A., and D. M. Schifferli. 1997. Differential regulation of fasA and fasH expression of Escherichia coli 987P fimbriae by environmental cues. Mol. Microbiol. 25:797-809.
21. Farthing, M. J. 2000. Enterotoxins and the enteric nervous system - a fatal attraction. Int. J. Med. Microbiol. 290:491-496.
22. Flores, J., H. L. DuPont, S. A. Lee, J. Belkind-Gerson, M. Paredes, J. A. Mohamed, L. Y. Armitige, D. C. Guo, and P. C. Okhuysen. 2008. Influence of host interleukin-10 polymorphisms on development of traveler's diarrhea due to heat-labile enterotoxin-producing Escherichia coli in travelers from the United States who are visiting Mexico. Clin. Vaccine Immunol. 15:1194-1198.
23. Frech, S. A., H. L. DuPont, A. L. Bourgeois, R. McKenzie, J. Belkind-Gerson, J. F. Figueroa, P. C. Okhuysen, N. H. Guerrero, F. G. Martinez-Sandoval, J. H. M. Melendez-Romero, Z.-D. Jiang, E. J. Asturias, J. Halpern, O. R. Torres, A. S. Hoffman, C. P. Villar, R. N. Kassem, D. C. Flyer, B. H. Andersen, K. Kazempour, S. A. Breisch, and G. M. Glenn. 2008. Use of a patch containing heat-labile toxin from Escherichia coli against travellers' diarrhoea: a phase II, randomized, double-blind, placebo-controlled field trial. Lancet 371:2019-2025.
24. Frey, A., K. T. Giannasca, R. Weltzin, P. J. Giannasca, H. Reggio, W. I. Lencer, and M. R. Neutra. 1996. Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells: implications for microbial attachment and oral vaccine targeting. J. Exp. Med. 184:1045-1059.
25. Galbadage, T., Z. D. Jiang, and H. L. DuPont. 2009. Improvement in detection of enterotoxigenic Escherichia coli in patients with travelers' diarrhea by increasing the number of E. coli colonies tested. Am. J. Trop. Med. Hyg. 80:20-23.
26. Galili, U., E. A. Rachmilewitz, A. Peleg, and I. Flechner. 1984. A unique natural human IgG antibody with anti-alpha-galactosyl specificity. J. Exp. Med. 160:1519-1531.
27. Garner, M. J., R. D. Hayward, and V. Koronakis. 2002. The Salmonella pathogenicity island 1 secretion system directs cellular cholesterol redistribution during mammalian cell entry and intracellular trafficking. Cell. Microbiol. 4:153-165.
28. Glenn, G. M., C. P. Villar, D. C. Flyer, A. L. Bourgeois, R. McKenzie, R. M. Lavker, and S. A. Frech. 2007. Safety and immunogenicity of an ETEC vaccine patch containing heat-labile toxin: use of skin pretreatment to disrupt the stratum corneum. Infect. Immun. 75:2163-2170.
29. Golin-Bisello, F., N. Bradbury, and N. Ameen. 2005. STa and cGMP stimulate CFTR translocation to the surface of villus enterocytes in rat jejunum and is regulated by protein kinase G. Am. J. Physiol. Cell Physiol. 289:C708-C716.
30. Goodwin, M. S., and A. A. Weiss. 1990. Adenylate cyclase toxin is critical for colonization and pertussis toxin is critical for lethal infection by Bordetella pertussis in infant mice. Infect. Immun. 58:3445-3447.
31. Guarner, F., and J. R. Malagelada. 2003. Gut flora in health and disease. Lancet 361:512-519.
32. Gupta, S. K., J. Keck, P. K. Ram, J. A. Crump, M. A. Miller, and E. D. Mintz. 2008. Part III. Analysis of data gaps pertaining to enterotoxigenic Escherichia coli infections in low and medium human development index countries, 1984-2005. Epidemiol. Infect. 136:721-738.
33. Hansen, G. H., S. M. Dalskov, C. R. Rasmussen, L. Immerdal, L. L. Niels- Christiansen, and E. M. Danielsen. 2005. Cholera toxin entry into pig enterocytes occurs via a lipid raft- and clathrin-dependent mechanism. Biochemistry (Moscow) 44:873-882.
34. Hansen, G. H., L. L. Niels-Christiansen, L. Immerdal, and E. M. Danielsen. 2006. Antibodies in the small intestine: mucosal synthesis and deposition of anti-glycosyl IgA, IgM, and IgG in the enterocyte brush border. Am. J. Physiol. Gastrointest. Liver Physiol. 291:G82-G90.
35. Hansen, G. H., E. D. Pedersen, L. Immerdal, L. L. Niels-Christiansen, and E. M. Danielsen. 2005. Anti-glycosyl antibodies in lipid rafts of the enterocyte brush border: a possible host defense against pathogens. Am. J. Physiol. Gastrointest. Liver Physiol. 289:G1100-G1107.
36. Harris, A. M., F. Chowdhury, Y. A. Begum, A. I. Khan, A. S. Faruque, A. M. Svennerholm, J. B. Harris, E. T. Ryan, A. Cravioto, S. B. Calderwood, and F. Qadri. 2008. Shifting prevalence of major diarrheal pathogens in patients seeking hospital care during floods in 1998, 2004, and 2007 in Dhaka, Bangladesh. Am. J. Trop. Med. Hyg. 79:708-714.
37. Holmgren, J., I. Lonnroth, J. Mansson, and L. Svennerholm. 1975. Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proc. Natl. Acad. Sci. USA 72:2520-2524.
38. Holmgren, J., I. Lonnroth, and L. Svennerholm. 1973. Tissue receptor for cholera exotoxin: postulated structure from studies with GM1 ganglioside and related glycolipids. Infect. Immun. 8:208-214.
39. Hsiao A. Toscano K. Zhu J. Post-transcriptional cross-talk between pro- and anti-colonization pili biosynthesis systems in Vibrio cholerae Molecular Microbiology 2008 67 4 849-860 DOI 10.1111/j.1365-2958.2007.06091.x 39. Hsiao, A., K. Toscano, and J. Zhu. 2008. Post-transcriptional cross-talk between pro- and anti-colonization pili biosynthesis systems in Vibrio cholerae. Mol. Microbiol. 67:849-860. (Pubitemid 351143688)
40. Hsiao, A., X. Xu, B. Kan, R. V. Kulkarni, and J. Zhu. 2009. Direct regulation by the Vibrio cholerae regulator ToxT to modulate colonization and anticolonization pilus expression. Infect. Immun. 77:1383-1388.
41. Islam, D., L. Bandholtz, J. Nilsson, H. Wigzell, B. Christensson, B. Agerberth, and G. Gudmundsson. 2001. Downregulation of bactericidal peptides in enteric infections: a novel immune escape mechanism with bacterial DNA as a potential regulator. Nat. Med. 7:180-185.
42. Israel E.J. Taylor S. Wu Z. Mizoguchi E. Blumberg R.S. Bhan A. Simister N.E. Expression of the neonatal Fc receptor, FcRn, on human intestinal epithelial cells Immunology 1997 92 1 69-74 42. Israel, E. J., S. Taylor, Z. Wu, E. Mizoguchi, R. S. Blumberg, A. Bhan, and N. E. Simister. 1997. Expression of the neonatal Fc receptor, FcRn, on human intestinal epithelial cells. Immunology 92:69-74. (Pubitemid 27380883)
43. Jang, M. H., M. N. Kweon, K. Iwatani, M. Yamamoto, K. Terahara, C. Sasakawa, T. Suzuki, T. Nochi, Y. Yokota, P. D. Rennert, T. Hiroi, H. Tamagawa, H. Iijima, J. Kunisawa, Y. Yuki, and H. Kiyono. 2004. Intestinal villous M cells: an antigen entry site in the mucosal epithelium. Proc. Natl. Acad. Sci. USA 101:6110-6115.
44. Johnson, A. M., R. S. Kaushik, D. H. Francis, J. M. Fleckenstein, and P. R. Hardwidge. 2009. Heat-labile enterotoxin promotes Escherichia coli adherence to intestinal epithelial cells. J. Bacteriol. 191:178-186.
45. Kaper, J. B., A. Fasano, and M. Trucksis. 1994. Toxins of Vibrio cholerae, p. 145-176. In I. K. Wachsmuth, P. A. Blake, and O. Olsvik (ed.), Vibrio cholerae and cholera: molecular to global perspectives. American Society for Microbiology, Washington, DC.
46. Kaper, J. B., J. G. Morris, Jr., and M. M. Levine. 1995. Cholera. Clin. Microbiol. Rev. 8:48-86.
47. Karakus, R., K. Caglar, and C. Aybay. 2007. Evaluation of human antibody responses to diphtheria toxin subunits A and B in various age groups. Clin. Microbiol. Infect. 13:1065-1071.
48. Kotloff, K. L., M. B. Sztein, S. S. Wasserman, G. A. Losonsky, S. C. DiLorenzo, and R. I. Walker. 2001. Safety and immunogenicity of oral inactivated whole-cell Helicobacter pylori vaccine with adjuvant among volunteers with or without subclinical infection. Infect. Immun. 69:3581-3590.
49. Lencer, W. I. 2001. Microbes and microbial toxins: paradigms for microbialmucosal toxins. V. cholera: invasion of the intestinal epithelial barrier by a stably folded protein toxin. Am. J. Physiol. Gastrointest. Liver Physiol. 280: G781-G786.
50. Levine, M. M., J. B. Kaper, R. E. Black, and M. L. Clements. 1983. New knowledge on pathogenesis of bacterial enteric infections as applied to vaccine development. Microbiol. Rev. 47:510-550.
51. Levine, M. M., D. R. Nalin, D. L. Hoover, E. J. Bergquist, R. B. Hornick, and C. R. Young. 1979. Immunity to enterotoxigenic Escherichia coli. Infect. Immun. 23:729-736.
52. Levine, M. M., M. B. Rennels, L. Cisneros, T. P. Hughes, D. R. Nalin, and C. R. Young. 1980. Lack of person-to-person transmission of enterotoxigenic Escherichia coli despite close contact. Am. J. Epidemiol. 111:347-355.
53. Linden, S. K., P. Sutton, N. G. Karlsson, V. Korolik, and M. A. McGuckin. 2008. Mucins in the mucosal barrier to infection. Mucosal Immunol. 1:183-197.
54. Lycke, N., U. Karlsson, A. Sjolander, and K. E. Magnusson. 1991. The adjuvant action of cholera toxin is associated with an increased intestinal permeability for luminal antigens. Scand. J. Immunol. 33:691-698.
55. Mañes, S., G. del Real, and A. C. Martinez. 2003. Pathogens: raft hijackers. Nat. Rev. Immunol. 3:557-568.
56. Matson, J. S., J. H. Withey, and V. J. DiRita. 2007. Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect. Immun. 75: 5542-5549.
57. McAuley, J. L., S. K. Linden, C. W. Png, R. M. King, H. L. Pennington, S. J. Gendler, T. H. Florin, G. R. Hill, V. Korolik, and M. A. McGuckin. 2007. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J. Clin. Investig. 117:2313-2324.
58. McKenzie, R., A. L. Bourgeois, S. A. Frech, D. C. Flyer, A. Bloom, K. Kazempour, and G. M. Glenn. 2007. Transcutaneous immunization with the heat-labile toxin (LT) of enterotoxigenic Escherichia coli (ETEC): protective efficacy in a double-blind, placebo-controlled challenge study. Vaccine 25: 3684-3691.
59. 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 417:642-645.
60. Merritt, E. A., S. Sarfaty, F. van den Akker, C. L'Hoir, J. A. Martial, and W. G. Hol. 1994. Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide. Protein Sci. 3:166-175.
61. Meyer-Hoffert U. Hornef M.W. Henriques-Normark B. Axelsson L.-G. Midtvedt T. Putsep K. Andersson M. Secreted enteric antimicrobial activity localises to the mucus surface layer Gut 2008 57 6 764-771 DOI 10.1136/gut.2007.141481 61. Meyer-Hoffert, U., M. W. Hornef, B. Henriques-Normark, L. G. Axelsson, T. Midtvedt, K. Putsep, and M. Andersson. 2008. Secreted enteric antimicrobial activity localises to the mucus surface layer. Gut 57:764-771. (Pubitemid 351716969)
62. Michetti, P., C. Kreiss, K. L. Kotloff, N. Porta, J. L. Blanco, D. Bachmann, M. Herranz, P. F. Saldinger, I. Corthesy-Theulaz, G. Losonsky, R. Nichols, J. Simon, M. Stolte, S. Ackerman, T. P. Monath, and A. L. Blum. 1999. Oral immunization with urease and Escherichia coli heat-labile enterotoxin is safe and immunogenic in Helicobacter pylori-infected adults. Gastroenterology 116:804-812.
63. Moon, H. W., S. C. Whipp, and A. L. Baetz. 1971. Comparative effects of enterotoxins from Escherichia coli and Vibrio cholerae on rabbit and swine small intestine. Lab. Investig. 25:133-140.
64. Mukherjee, S., S. Vaishnava, and L. V. Hooper. 2008. Multi-layered regulation of intestinal antimicrobial defense. Cell. Mol. Life Sci. 65:3019-3027.
65. Navaneethan, U., and R. A. Giannella. 2008. Mechanisms of infectious diarrhea. Nat. Clin. Pract. Gastroenterol Hepatol. 5:637-647.
66. Nelson, E. T., J. D. Clements, and R. A. Finkelstein. 1976. Vibrio cholerae adherence and colonization in experimental cholera: electron microscopic studies. Infect. Immun. 14:527-547.
67. Patnaik, B. K., and H. K. Ghosh. 1966. Histopathological studies on experimental cholera. Br. J. Exp. Pathol. 47:210-214.
68. Peltola, H., A. Siitonen, H. Kyronseppa, I. Simula, L. Mattila, P. Oksanen, M. J. Kataja, and M. Cadoz. 1991. Prevention of travellers' diarrhoea by oral B-subunit/whole-cell cholera vaccine. Lancet 338:1285-1289.
69. Pereira, C. M., B. E. Guth, M. E. Sbrogio-Almeida, and B. A. Castilho. 2001. Antibody response against Escherichia coli heat-stable enterotoxin expressed as fusions to flagellin. Microbiology 147:861-867.
70. Pierce, N. F., W. C. Cray, Jr., J. B. Kaper, and J. J. Mekalanos. 1988. Determinants of immunogenicity and mechanisms of protection by virulent and mutant Vibrio cholerae O1 in rabbits. Infect. Immun. 56:142-148.
71. Pierce, N. F., J. B. Kaper, J. J. Mekalanos, and W. C. Cray, Jr. 1985. Role of cholera toxin in enteric colonization by Vibrio cholerae O1 in rabbits. Infect. Immun. 50:813-816.
72. Qadri, F., A. Saha, T. Ahmed, A. Al Tarique, Y. A. Begum, and A. M. Svennerholm. 2007. Disease burden due to enterotoxigenic Escherichia coli in the first 2 years of life in an urban community in Bangladesh. Infect. Immun. 75:3961-3968.
73. Qadri, F., A. M. Svennerholm, A. S. Faruque, and R. B. Sack. 2005. Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin. Microbiol. Rev. 18: 465-483.
74. Rao, M. R., T. F. Wierzba, S. J. Savarino, R. Abu-Elyazeed, N. El-Ghoreb, E. R. Hall, A. Naficy, I. Abdel-Messih, R. W. Frenck, Jr., A. M. Svennerholm, and J. D. Clemens. 2005. Serologic correlates of protection against enterotoxigenic Escherichia coli diarrhea. J. Infect. Dis. 191:562-570.
75. Raymond, B., E. Batsche, F. Boutillon, Y. Z. Wu, D. Leduc, V. Balloy, E. Raoust, C. Muchardt, P. L. Goossens, and L. Touqui. 2009. Anthrax lethal toxin impairs IL-8 expression in epithelial cells through inhibition of histone H3 modification. PLoS Pathog. 5:e1000359.
76. Rosenberger, C. M., J. H. Brumell, and B. B. Finlay. 2000. Microbial pathogenesis: lipid rafts as pathogen portals. Curr. Biol. 10:R823-R825.
77. Roy, K., G. M. Hilliard, D. J. Hamilton, J. Luo, M. M. Ostmann, and J. M. Fleckenstein. 2009. Enterotoxigenic Escherichia coli EtpA mediates adhesion between flagella and host cells. Nature 457:594-598.
78. Sánchez, J., and J. Holmgren. 2005. Virulence factors, pathogenesis and vaccine protection in cholera and ETEC diarrhea. Curr. Opin. Immunol. 17:388-398.
79. Sears, C. L., and J. B. Kaper. 1996. Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 60:167-215.
80. Selsted, M. E., and A. J. Ouellette. 2005. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6:551-557.
81. Shin, J. S., and S. N. Abraham. 2001. Caveolae as portals of entry for microbes. Microbes Infect. 3:755-761.
82. Silva, A. J., G. J. Leitch, A. Camilli, and J. A. Benitez. 2006. Contribution of hemagglutinin/protease and motility to the pathogenesis of El Tor biotype cholera. Infect. Immun. 74:2072-2079.
83. Sjoling A. Qadri F. Nicklasson M. Begum Y.A. Wiklund G. Svennerholm A.-M. In vivo expression of the heat stable (estA) and heat labile (eltB) toxin genes of enterotoxigenic Escherichia coli (ETEC) Microbes and Infection 2006 8 12 13 2797-2802 DOI 10.1016/j.micinf.2006.08.011, PII S128645790600308X 83. Sjoling, A., F. Qadri, M. Nicklasson, Y. A. Begum, G. Wiklund, and A. M. Svennerholm. 2006. In vivo expression of the heat stable (estA) and heat labile (eltB) toxin genes of enterotoxigenic Escherichia coli (ETEC). Microbes Infect. 8:2797-2802. (Pubitemid 44767738)
84. Spangler, B. D. 1992. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56:622-647.
85. Steffen, R., F. Castelli, H. Dieter Nothdurft, L. Rombo, and N. Jane Zuckerman. 2005. Vaccination against enterotoxigenic Escherichia coli, a cause of travelers' diarrhea. J. Travel Med. 12:102-107.
86. Steinsland, H., P. Valentiner-Branth, H. K. Gjessing, P. Aaby, K. Molbak, and H. Sommerfelt. 2003. Protection from natural infections with enterotoxigenic Escherichia coli: longitudinal study. Lancet 362:286-291.
87. Taïeb, N., N. Yahi, and J. Fantini. 2004. Rafts and related glycosphingolipid-enriched microdomains in the intestinal epithelium: bacterial targets linked to nutrient absorption. Adv. Drug Deliv. Rev. 56:779-794.
88. Tayot, J. L., J. Holmgren, L. Svennerholm, M. Lindblad, and M. Tardy. 1981. Receptor-specific large-scale purification of cholera toxin on silica beads derivatized with lysoGM1 ganglioside. Eur. J. Biochem. 113:249-258.
89. Thomson, A. B., C. I. Cheeseman, M. Keelan, R. Fedorak, and M. T. Clandinin. 1994. Crypt cell production rate, enterocyte turnover time and appearance of transport along the jejunal villus of the rat. Biochim. Biophys. Acta 1191:197-204.
90. Tobias, J., K. Andersson, A. Bialik, and D. Cohen. 2008. Preexisting antibodies to homologous colonization factors and heat-labile toxin in serum, and the risk to develop enterotoxigenic Escherichia coli-associated diarrhea. Diagn. Microbiol. Infect. Dis. 60:229-231.
91. Torres, A. G., X. Zhou, and J. B. Kaper. 2005. Adherence of diarrheagenic Escherichia coli strains to epithelial cells. Infect. Immun. 73:18-29.
92. Trachman, J. D., and M. Yasmin. 2004. Thermo-osmoregulation of heat-labile enterotoxin expression by Escherichia coli. Curr. Microbiol. 49:353-360.
93. Vimal, D. B., M. Khullar, S. Gupta, and N. K. Ganguly. 2000. Intestinal mucins: the binding sites for Salmonella typhimurium. Mol. Cell. Biochem. 204:107-117.
94. Wennerås, C., and V. Erling. 2004. Prevalence of enterotoxigenic Escherichia coli-associated diarrhoea and carrier state in the developing world. J. Health Popul. Nutr. 22:370-382.
95. Wolf, M. K. 2000. Bacterial infections of the small intestine and colon. Curr. Opin. Gastroenterol. 16:4-11.
96. Wooldridge, K. G., P. H. Williams, and J. M. Ketley. 1996. Host signal transduction and endocytosis of Campylobacter jejuni. Microb. Pathog. 21: 299-305.
97. Yu, J., F. Cassels, T. Scharton-Kersten, S. A. Hammond, A. Hartman, E. Angov, B. Corthesy, C. Alving, and G. Glenn. 2002. Transcutaneous immunization using colonization factor and heat labile enterotoxin induces correlates of protective immunity for enterotoxigenic Escherichia coli. Infect. Immun. 70:1056-1068.
98. Zaalouk, T. K., M. Bajaj-Elliott, J. T. George, and V. McDonald. 2004. Differential regulation of β-defensin gene expression during Cryptosporidium parvum infection. Infect. Immun. 72:2772-2779.
99. Zhang, W., E. M. Berberov, J. Freeling, D. He, R. A. Moxley, and D. H. Francis. 2006. Significance of heat-stable and heat-labile enterotoxins in porcine colibacillosis in an additive model for pathogenicity studies. Infect. Immun. 74:3107-3114.