Development of a Human Vaccine

David R. Tribble; Shahida Baqar; Stuart A. Thompson

doi:10.1128/9781555815554.ch24

Chapter 24 : Development of a Human Vaccine

Authors: David R. Tribble¹, Shahida Baqar², Stuart A. Thompson³

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Preventive Medicine & Biometrics Department, Uniformed Services University of the Health Sciences, 4301 Jones Bridge Rd., Bethesda, MD 20814-5119; 2: Enteric Diseases Program, Naval Medical Research Center, 503 Robert Grant Ave., Silver Spring, MD 20910-7500; 3: Department of Biochemistry and Molecular Biology, Medical College of Georgia 1120 15th St., Augusta, GA 30912-2100

Content Type: Monograph

Publication Year: 2008

Category: Bacterial Pathogenesis

Book DOI: 10.1128/9781555815554

Chapter DOI: 10.1128/9781555815554.ch24

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Development of a Human Vaccine, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555815554/9781555814373_Chap24-1.gif /docserver/preview/fulltext/10.1128/9781555815554/9781555814373_Chap24-2.gif

Abstract:

Observational and experimental studies provide evidence of acquired immunity developing in humans exposed to Campylobacter jejuni, lending support for vaccine development. Campylobacter vaccine development strategy must integrate basic science knowledge of pathogenesis and immunity, as well as an appreciation of the antigens and host responses associated with the development of protective immunity. More practical concerns include the need to optimize vaccine production methodology, delivery methods, and regimen selection followed by an assessment of vaccine safety, immunogenicity, and efficacy in target populations. The major impact of diarrheal disease in industrialized countries such as the United States relates to short-term morbidity and economic burden. Surveys among travel medicine practitioners in the United States and the United Kingdom have provided estimates on the level of support and potential application for vaccines to prevent traveler’s diarrhea (TD), and specifically, Campylobacter-only vaccines. The survey was limited by low response rate but was able to assess providers providing care in high-volume practices. A major consideration in the development of any vaccine is safety. For Campylobacter, this includes symptoms that may be caused by a vaccine in the first 24 to 72 h, as well as the potential for postvaccination sequelae a few weeks after immunization. Campylobacter vaccine development at the U.S. Naval Medical Research Center recently completed clinical studies of subunit Campylobacter vaccine based on the flagellin protein. Increased understanding of the burden of campylobacteriosis combined with evidence of acquired immunity provides the need and rationale for disease prevention strategies that include vaccine approaches.

Citation: Tribble D, Baqar S, Thompson S. 2008. Development of a Human Vaccine, p 329-444. In Nachamkin I, Szymanski C, Blaser M (ed), Campylobacter, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch24

Highlighted Text: Show | Hide

Full text loading...

References

/content/book/10.1128/9781555815554.ch24

1. Abimiku, A. G., and, J. M. Dolby. 1988. Cross-protection of infant mice against intestinal colonisation by Campylobacter jejuni: importance of heat-labile serotyping (Lior) antigens. J. Med. Microbiol. 26: 265– 268.

2. Alm, R. A.,, P. Guerry,, M. E. Power,, H. Lior, and, T. J. Trust. 1991. Analysis of the role of flagella in the heat-labile Lior serotyping scheme of thermophilic campylobacters by mutant allele exchange. J. Clin. Microbiol. 29: 2438– 2445.

3. Ang, C. W.,, B. C. Jacobs, and, J. D. Laman. 2004. The GuillainBarré syndrome: a true case of molecular mimicry. Trends Immunol. 25: 61– 66.

4. Babakhani, F. K.,, G. A. Bradley, and, L. A. Joens. 1993. Newborn piglet model for campylobacteriosis. Infect. Immun. 61: 3466– 3475.

5. Bacon, D. J.,, R. A. Alm,, D. H. Burr,, L. Hu,, D. J. Kopecko,, C. P. Ewing,, T. J. Trust, and, P. Guerry. 2000. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect. Immun. 68: 4384– 4390.

6. Bacon, D. J.,, R. A. Alm,, L. Hu,, T. E. Hickey,, C. P. Ewing,, R. A. Batchelor,, T. J. Trust, and, P. Guerry. 2002. DNA sequence and mutational analyses of the pVir plasmid of Campylobacter jejuni 81-176. Infect. Immun. 70: 6242– 6250.

7. Bacon, D. J.,, C. M. Szymanski,, D. H. Burr,, R. P. Silver,, R. A. Alm, and, P. Guerry. 2001. A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol. Microbiol. 40: 769– 777.

8. Bagos, P. G.,, T. D. Liakopoulos,, I. C. Spyropoulos, and, S. J. Hamodrakas. 2004. PRED-TMBB: a web server for predicting the topology of beta-barrel outer membrane proteins. Nucleic Acids Res. 32: W400– W404.

9. Baqar, S.,, L. A. Applebee, and, A. L. Bourgeois. 1995a. Immunogenicity and protective efficacy of a prototype Campylobacter killed whole-cell vaccine in mice. Infect. Immun. 63: 3731– 3735.

10. Baqar, S.,, L. Applebee,, T. Gilliland,, P. Guerry, and, M. A. Monteiro. 2007a. Immunogenicity of a Campylobacter jejuni capsular polysaccharide conjugate vaccine in mice. Abstract. 107th Am. Soc. Microbiol.

11. Baqar, S.,, L. Applebee,, T. Gilliland,, C. Lin,, P. Guerry, and, M. A. Monteiro. 2007b. The synthesis and efficacy in mice of a Campylobacter jejuni capsular polysaccharide. Abstract. 4th Int. Conf. Vaccines Enteric Dis.

12. Baqar, S.,, A. L. Bourgeois,, L. A. Applebee,, A. S. Mourad,, M. T. Kleinosky,, Z. Mohran, and, J. R. Murphy. 1996. Murine intra-nasal challenge model for the study of Campylobacter pathogenesis and immunity. Infect. Immun. 64: 4933– 4939.

13. Baqar, S.,, A. L. Bourgeois,, P. J. Schultheiss,, R. I. Walker,, D. M. Rollins,, R. L. Haberberger, and, O. R. Pavlovskis. 1995b. Safety and immunogenicity of a prototype oral whole-cell killed Campylobacter vaccine administered with a mucosal adjuvant in non-human primates. Vaccine 13: 22– 28.

14. Baqar, S.,, J. Lapa,, M. Nelson,, C. Lin,, C. Porter,, C. Williams,, T. Gilliland,, R. Arora,, J. Saunders,, P. Guerry,, J. Sanders, and, D. Tribble. 2007c. Safety and immunogenicity of a recombinant Campylobacter flagellin vaccine in adult volunteers. In Vaccine for Enteric Diseases. Lisbon Portugal.

15. Baqar, S.,, B. Rice,, L. Lee,, A. L. Bourgeois,, A. N. El Din,, D. R. Tribble,, G. P. Heresi,, A. S. Mourad, and, J. R. Murphy. 2001. Campylobacter jejuni enteritis. Clin. Infect. Dis. 33: 901– 905.

16. Bell, J. A., and, D. D. Manning. 1990. A domestic ferret model of immunity to Campylobacter jejuni–induced enteric disease. Infect. Immun. 58: 1848– 1852.

17. Berven, F. S.,, K. Flikka,, H. B. Jensen, and, I. Eidhammer. 2004. BOMP: a program to predict integral beta-barrel outer membrane proteins encoded within genomes of gram-negative bacteria. Nucleic Acids Res. 32: W394– W399.

18. Bigelow, H. R.,, D. S. Petrey,, J. Liu,, D. Przybylski, and, B. Rost. 2004. Predicting transmembrane beta-barrels in proteomes. Nucleic Acids Res. 32: 2566– 2577.

19. Black, R.,, D. Perlman,, M. Clements,, M. Levine, and, M. Blaser. 1992. Human volunteer studies with Campylobacter jejuni, p. 207– 215. In I. Nachamkin,, M. Blaser, and, L. Tompkins (ed.), Campylobacter jejuni: Current Status and Future Trends. American Society for Microbiology, Washington, DC.

20. Black, R. E. 1990. Epidemiology of travelers’ diarrhea and relative importance of various pathogens. Rev. Infect. Dis. 12 (Suppl. 1): S73– S79.

21. Black, R. E.,, M. M. Levine,, M. L. Clements,, T. P. Hughes, and, M. J. Blaser. 1988. Experimental Campylobacter jejuni infection in humans. J. Infect. Dis. 157: 472– 479.

22. Black, R. E.,, M. M. Levine,, C. Ferreccio,, M. L. Clements,, C. Lanata,, J. Rooney, and, R. Germanier. 1990. Efficacy of one or two doses of Ty21a Salmonella typhi vaccine in enteric-coated capsules in a controlled field trial. Chilean Typhoid Committee. Vaccine 8: 81– 84.

23. Blaser, M. J. 1997. Epidemiologic and clinical features of Campylobacter jejuni infections. J. Infect. Dis. 176 (Suppl. 2): S103– S105.

24. Blaser, M. J., and, D. J. Duncan. 1984. Human serum antibody response to Campylobacter jejuni infection as measured in an enzyme-linked immunosorbent assay. Infect. Immun. 44: 292– 298.

25. Blaser, M. J.,, D. J. Duncan,, M. T. Osterholm,, G. R. Istre, and, W. L. Wang. 1983. Serologic study of two clusters of infection due to Campylobacter jejuni. J. Infect. Dis. 147: 820– 823.

26. Blaser, M. J.,, E. Sazie, and, L. P. Williams, Jr. 1987. The influence of immunity on raw milk—associated Campylobacter infection. JAMA 257: 43– 46.

27. Boel, G.,, H. Jin, and, V. Pancholi. 2005. Inhibition of cell surface export of group A streptococcal anchorless surface dehydrogenase affects bacterial adherence and antiphagocytic properties. Infect. Immun. 73: 6237– 6248.

28. Bolla, J. M.,, E. De,, A. Dorez, and, J. M. Pages. 2000. Purification, characterization and sequence analysis of Omp50, a new porin isolated from Campylobacter jejuni. Biochem. J. 352: 637– 643.

29. Brandtzaeg, P. 2007. Induction of secretory immunity and memory at mucosal surfaces. Vaccine 25: 5467– 5484.

30. Bremell, T.,, A. Bjelle, and, A. Svedhem. 1991. Rheumatic symptoms following an outbreak of Campylobacter enteritis: a five year follow up. Ann. Rheum. Dis. 50: 934– 938.

31. Burr, D. H.,, D. Rollins,, L. H. Lee,, D. L. Pattarini,, S. S. Walz,, J. H. Tian,, J. Pace,, A. L. Bourgeois, and, R. I. Walker. 2005. Prevention of disease in ferrets fed an inactivated whole cell Campylobacter jejuni vaccine. Vaccine 23: 4315– 4321.

32. Caldwell, M. B.,, P. Guerry,, E. C. Lee,, J. P. Burans, and, R. I. Walker. 1985. Reversible expression of flagella in Campylobacter jejuni. Infect. Immun. 50: 941– 943.

33. Cejka, J.,, D. W. Mood, and, C. S. Kim. 1974. Immunoglobulin concentrations in sera of normal children: quantitation against an international reference preparation. Clin. Chem. 20: 656– 659.

34. Chang, C., and, J. F. Miller. 2006. Campylobacter jejuni colonization of mice with limited enteric flora. Infect. Immun. 74: 5261– 5271.

35. 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,, B. F. Stanton,, B. A. Kay,, S. Walter,, R. Eeckels,, A.-M. Svenner-holm, and, J. Holmgren. 1990. Field trial of oral cholera vaccines in Bangladesh: results from three-year follow-up. Lancet 335: 270– 274.

36. Cohen, D.,, S. Ashkenazi,, M. S. Green,, M. Gdalevich,, G. Robin,, R. Slepon,, M. Yavzori,, N. Orr,, C. Block,, I. Ashkenazi,, J. Shemer,, D. N. Taylor,, T. L. Hale,, J. C. Sadoff,, D. Pavliakova,, R. Schneerson, and, J. B. Robbins. 1997. Double-blind vaccine-controlled randomised efficacy trial of an investigational Shigella sonnei conjugate vaccine in young adults. Lancet 349: 155– 159.

37. Coker, A. O.,, R. D. Isokpehi,, B. N. Thomas,, K. O. Amisu, and, C. L. Obi. 2002. Human campylobacteriosis in developing countries. Emerg. Infect. Dis. 8: 237– 244.

38. Connor, B. A. 2005. Sequelae of traveler’s diarrhea: focus on post-infectious irritable bowel syndrome. Clin. Infect. Dis. 41 (Suppl. 8): S577– S586.

39. Cooper, J. C.,, S. Hughes,, A. Ben-Smith,, C. O. Savage, and, J. B. Winer. 2002. T cell recognition of a non-protein antigen preparation of Campylobacter jejuni in patients with Guillain-Barré syndrome. J. Neurol. Neurosurg. Psychiatry 72: 413– 414.

40. Dallo, S. F.,, T. R. Kannan,, M. W. Blaylock, and, J. B. Baseman. 2002. Elongation factor Tu and E1 b subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol. Microbiol. 46: 1041– 1051.

41. Daniely, D.,, M. Portnoi,, M. Shagan,, A. Porgador,, N. Givon-Lavi,, E. Ling,, R. Dagan, and, Y. Mizrachi Nebenzahl. 2006. Pneumococcal 6-phosphogluconate-dehydrogenase, a putative adhesin, induces protective immune response in mice. Clin. Exp. Immunol. 144: 254– 263.

42. De, E.,, M. Jullien,, G. Labesse,, J. M. Pages,, G. Molle, and, J. M. Bolla. 2000. MOMP (major outer membrane protein) of Campylobacter jejuni; a versatile pore-forming protein. FEBS Lett. 469: 93– 97.

43. Dickinson, B. L., and, J. D. Clements. 1995. Dissociation of Escherichia coli heat-labile enterotoxin adjuvanticity from ADP-ribosyltransferase activity. Infect. Immun. 63: 1617– 1623.

44. Doig, P.,, N. Kinsella,, P. Guerry, and, T. J. Trust. 1996. Characterization of a post-translational modification of Campylobacter flagellin: identification of a sero-specific glycosyl moiety. Mol. Microbiol. 19: 379– 387.

45. Dunn, B. E., and, S. H. Phadnis. 1998. Structure, function and localization of Helicobacter pylori urease. Yale J. Biol. Med. 71: 63– 73.

46. Ericsson, C. D. 1998. Travelers’ diarrhea. Epidemiology, prevention, and self-treatment. Infect. Dis. Clin. North Am. 12: 285– 303.

47. Ferreccio, C.,, M. M. Levine,, H. Rodriguez, and, R. Contreras. 1989. Comparative efficacy of two, three, or four doses of TY21a live oral typhoid vaccine in enteric-coated capsules: a field trial in an endemic area. J. Infect. Dis. 159: 766– 769.

48. Fouts, D. E.,, E. F. Mongodin,, R. E. Mandrell,, W. G. Miller,, D. A. Rasko,, J. Ravel,, L. M. Brinkac,, R. T. DeBoy,, C. T. Parker,, S. C. Daugherty,, R. J. Dodson,, A. S. Durkin,, R. Madupu,, S. A. Sullivan,, J. U. Shetty,, M. A. Ayodeji,, A. Shvartsbeyn,, M. C. Schatz,, J. H. Badger,, C. M. Fraser, and, K. E. Nelson. 2005. Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol. 3: e15.

49. Garrow, A. G.,, A. Agnew, and, D. R. Westhead. 2005. TMB-Hunt: an amino acid composition based method to screen proteomes for beta-barrel transmembrane proteins. BMC Bioinformatics 6: 56.

50. Gaudio, P. A.,, P. Echeverria,, C. W. Hoge,, C. Pitarangsi, and, P. Goff. 1996. Diarrhea among expatriate residents in Thailand: correlation between reduced Campylobacter prevalence and longer duration of stay. J. Travel Med. 3: 77– 79.

51. Georges-Courbot, M. C.,, A. M. Beraud-Cassel,, I. Gouandjika, and, A. J. Georges. 1987. Prospective study of enteric Campylobacter infections in children from birth to 6 months in the Central African Republic. J. Clin. Microbiol. 25: 836– 839.

52. Godschalk, P. C.,, M. L. Kuijf,, J. Li,, F. St Michael,, C. W. Ang,, B. C. Jacobs,, M. F. Karwaski,, D. Brochu,, A. Moterassed,, H. P. Endtz,, A. van Belkum, and, M. Gilbert. 2007. Structural characterization of Campylobacter jejuni lipooligosaccharide outer cores associated with Guillain-Barré and Miller Fisher syndromes. Infect. Immun. 75: 1245– 1254.

53. Guerry, P.,, P. Doig,, R. A. Alm,, D. H. Burr,, N. Kinsella, and, T. J. Trust. 1996. Identification and characterization of genes required for post-translational modification of Campylobacter coli VC167 flagellin. Mol. Microbiol. 19: 369– 378.

54. Guerry, P.,, P. M. Pope,, D. H. Burr,, J. Leifer,, S. W. Joseph, and, A. L. Bourgeois. 1994. Development and characterization of recA mutants of Campylobacter jejuni for inclusion in attenuated vaccines. Infect. Immun. 62: 426– 432.

55. Gundogdu, O.,, S. D. Bentley,, M. T. Holden,, J. Parkhill,, N. Dorrell, and, B. W. Wren. 2007. Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 8: 162.

56. Hannu, T.,, M. Kauppi,, M. Tuomala,, I. Laaksonen,, P. Klemets, and, M. Kuusi. 2004. Reactive arthritis following an outbreak of Campylobacter jejuni infection. J. Rheumatol. 31: 528– 530.

57. Hannu, T.,, L. Mattila,, H. Rautelin,, P. Pelkonen,, P. Lahdenne,, A. Siitonen, and, M. Leirisalo-Repo. 2002. Campylobacter-triggered reactive arthritis: a population-based study. Rheumatology (Oxford) 41: 312– 318.

58. Harris, L. A.,, S. M. Logan,, P. Guerry, and, T. J. Trust. 1987. Antigenic variation of Campylobacter flagella. J. Bacteriol. 169: 5066– 5071.

59. Hickey, T. E.,, A. L. McVeigh,, D. A. Scott,, R. E. Michielutti,, A. Bixby,, S. Carroll,, A. L. Bourgeois, and, P. Guerry. 2000. Campylobacter jejuni cytolethal distending toxin mediates release of interleukin-8 from intestinal epithelial cells. Infect. Immun. 68: 6535– 6541.

60. Hofreuter, D.,, J. Tsai,, R. O. Watson,, V. Novik,, B. Altman,, M. Benitez,, C. Clark,, C. Perbost,, T. Jarvie,, L. Du, and, J. E. Galán. 2006. Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 74: 4694– 4707.

61. Holmgren, J., and, C. Czerkinsky. 2005. Mucosal immunity and vaccines. Nat. Med. 11: S45– S53.

62. Holmgren, J.,, C. Czerkinsky,, N. Lycke, and, A. M. Svennerholm. 1992. Mucosal immunity: implications for vaccine development. Immunobiology 184: 157– 179.

63. Hughes, R. A.,, R. D. Hadden,, N. A. Gregson, and, K. J. Smith. 1999. Pathogenesis of Guillain-Barré syndrome. J. Neuroimmunol. 100: 74– 97.

64. Islam, D.,, M. D. Lewis,, A. Srijan,, L. Bodhidatta,, A. Aksomboon,, M. Gettayacamin,, S. Baqar,, D. Scott, and, C. J. Mason. 2006. Establishment of a non-human primate Campylobacter disease model for the pre-clinical evaluation of Campylobacter vaccine formulations. Vaccine 24: 3762– 3771.

65. Jin, H.,, Y. P. Song,, G. Boel,, J. Kochar, and, V. Pancholi. 2005. Group A streptococcal surface GAPDH, SDH, recognizes uPAR/CD87 as its receptor on the human pharyngeal cell and mediates bacterial adherence to host cells. J. Mol. Biol. 350: 27– 41.

66. Jones, F. R.,, S. Baqar,, A. Gozalo,, G. Nunez,, N. Espinoza,, S. M. Reyes,, M. Salazar,, R. Meza,, C. K. Porter, and, S. E. Walz. 2006. New World monkey Aotus nancymae as a model for Campylobacter jejuni infection and immunity. Infect. Immun. 74: 790– 793.

67. Jones, T. F.,, E. Scallan, and, F. J. Angulo. 2007. FoodNet: overview of a decade of achievement. Foodborne Pathog. Dis. 4: 60– 66.

68. Josic, D., and, J. G. Clifton. 2007. Use of monolithic supports in proteomics technology. J. Chromatogr. A 1144: 2– 13.

69. Kantele, A. 1991. Immune response to prolonged intestinal exposure to antigen. Scand. J. Immunol. 33: 225– 229.

70. Kaper, J. B.,, H. Lockman,, M. M. Baldini, and, M. M. Levine. 1984. Recombinant nontoxinogenic Vibrio cholerae strains as attenuated cholera vaccine candidates. Nature 308: 655– 658.

71. Kapperud, G.,, J. Lassen,, S. M. Ostroff, and, S. Aasen. 1992. Clinical features of sporadic Campylobacter infections in Norway. Scand. J. Infect. Dis. 24: 741– 749.

72. Karlyshev, A. V.,, J. M. Ketley, and, B. W. Wren. 2005. The Campylobacter jejuni glycome. FEMS Microbiol. Rev. 29: 377– 390.

73. Karlyshev, A. V.,, D. Linton,, N. A. Gregson,, A. J. Lastovica, and, B. W. Wren. 2000. Genetic and biochemical evidence of a Campylobacter jejuni capsular polysaccharide that accounts for Penner serotype specificity. Mol. Microbiol. 35: 529– 541.

74. Knaust, A.,, M. V. Weber,, S. Hammerschmidt,, S. Bergmann,, M. Frosch, and, O. Kurzai. 2007. Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitidis. J. Bacteriol. 189: 3246– 3255.

75. Koga, M.,, M. Gilbert,, M. Takahashi,, J. Li,, S. Koike,, K. Hirata, and, N. Yuki. 2006. Comprehensive analysis of bacterial risk factors for the development of Guillain-Barré syndrome after Campylobacter jejuni enteritis. J. Infect. Dis. 193: 547– 555.

76. Koga, M.,, M. Takahashi,, M. Masuda,, K. Hirata, and, N. Yuki. 2005. Campylobacter gene polymorphism as a determinant of clinical features of Guillain-Barré syndrome. Neurology 65: 1376– 1381.

77. Konkel, M. E.,, B. J. Kim,, V. Rivera-Amill, and, S. G. Garvis. 1999. Bacterial secreted proteins are required for the internalization of Campylobacter jejuni into cultured mammalian cells. Mol. Microbiol. 32: 691– 701.

78. Konkel, M. E.,, J. D. Klena,, V. Rivera-Amill,, M. R. Monteville,, D. Biswas,, B. Raphael, and, J. Mickelson. 2004. Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional flagellar export apparatus. J. Bacteriol. 186: 3296– 3303.

79. Korlath, J. A.,, M. T. Osterholm,, L. A. Judy,, J. C. Forfang, and, R. A. Robinson. 1985. A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J. Infect. Dis. 152: 592– 596.

80. Labesse, G.,, E. Garnotel,, S. Bonnel,, C. Dumas,, J. M. Pages, and, J. M. Bolla. 2001. MOMP, a divergent porin from Campylobacter: cloning and primary structural characterization. Biochim. Biophys. Res. Commun. 280: 380– 387.

81. Lara-Tejero, M., and, J. E. Galán. 2000. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 290: 354– 357.

82. Lara-Tejero, M., and, J. E. Galán. 2001. CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect. Immun. 69: 4358– 4365.

83. Lee, L. H.,, E. Burg III,, S. Baqar,, A. L. Bourgeois,, D. H. Burr,, C. P. Ewing,, T. J. Trust, and, P. Guerry. 1999. Evaluation of a truncated recombinant flagellin subunit vaccine against Campylobacter jejuni. Infect. Immun. 67: 5799– 5805.

84. Lindsay, J. A. 1997. Chronic sequelae of foodborne disease. Emerg. Infect. Dis. 3: 443– 452.

85. Linton, D.,, E. Allan,, A. V. Karlyshev,, A. D. Cronshaw, and, B. W. Wren. 2002. Identification of N-acetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni. Mol. Microbiol. 43: 497– 508.

86. Lior, H.,, D. L. Woodward,, J. A. Edgar,, L. J. Laroche, and, P. Gill. 1982. Serotyping of Campylobacter jejuni by slide agglutination based on heat-labile antigenic factors. J. Clin. Microbiol. 15: 761– 768.

87. Logan, S. M.,, P. Guerry,, D. M. Rollins,, D. H. Burr, and, T. J. Trust. 1989. In vivo antigenic variation of Campylobacter flagellin. Infect. Immun. 57: 2583– 2585.

88. Lüneberg, E.,, E. Glenn-Calvo,, M. Hartmann,, W. Bär, and, M. Frosch. 1998. The central, surface-exposed region of the flagellar hook protein FlgE of Campylobacter jejuni shows hypervariability among strains. J. Bacteriol. 180: 3711– 3714.

89. Mallett, C. P.,, L. VanDeVerg,, H. H. Collins, and, T. L. Hale. 1993. Evaluation of Shigella vaccine safety and efficacy in an intra-nasally challenged mouse model. Vaccine 11: 190– 196.

90. Mansfield, L. S.,, J. A. Bell,, D. L. Wilson,, A. J. Murphy,, H. M. Elsheikha,, V. A. Rathinam,, B. R. Fierro,, J. E. Linz, and, V. B. Young. 2007. C57BL/6 and congenic interleukin-10-deficient mice can serve as models of Campylobacter jejuni colonization and enteritis. Infect. Immun. 75: 1099– 1115.

91. Marcus, E. A., and, D. R. Scott. 2001. Cell lysis is responsible for the appearance of extracellular urease in Helicobacter pylori. Helicobacter 6: 93– 99.

92. Martin, P. M.,, J. Mathiot,, J. Ipero,, M. Kirimat,, A. J. Georges, and, M. C. Georges-Courbot. 1989. Immune response to Campylobacter jejuni and Campylobacter coli in a cohort of children from birth to 2 years of age. Infect. Immun. 57: 2542– 2546.

93. Mattila, L. 1994. Clinical features and duration of traveler’s diarrhea in relation to its etiology. Clin. Infect. Dis. 19: 728– 734.

94. Miller, N., and, I. Saunders. 2007. Current perceptions of travelers’ diarrhea treatments and vaccines: results from a postal questionnaire survey and physician interviews. J. Travel Med. 14: 158– 167.

95. Millson, M.,, M. Bokhout,, J. Carlson,, L. Spielberg,, R. Aldis,, A. Borczyk, and, H. Lior. 1991. An outbreak of Campylobacter jejuni gastroenteritis linked to meltwater contamination of a municipal well. Can. J. Public Health 82: 27– 31.

96. Mishu, B., and, M. J. Blaser. 1993. Role of infection due to Campylobacter jejuni in the initiation of Guillain-Barré syndrome. Clin. Infect. Dis. 17: 104– 108.

97. Nachamkin, I., and, A. M. Hart. 1985. Western blot analysis of the human antibody response to Campylobacter jejuni cellular antigens during gastrointestinal infection. J. Clin. Microbiol. 21: 33– 38.

98. Nesvizhskii, A. I. 2007. Protein identification by tandem mass spectrometry and sequence database searching. Methods Mol. Biol. 367: 87– 119.

99. Newburg, D. S.,, G. M. Ruiz-Palacios, and, A. L. Morrow. 2005. Human milk glycans protect infants against enteric pathogens. Annu. Rev. Nutr. 25: 37– 58.

100. Oelschlaeger, T. A.,, P. Guerry, and, D. J. Kopecko. 1993. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc. Natl. Acad. Sci. USA 90: 6884– 6888.

101. Pancholi, V., and, G. S. Chhatwal. 2003. Housekeeping enzymes as virulence factors for pathogens. Int. J. Med. Microbiol. 293: 391– 401.

102. Pancholi, V., and, V. A. Fischetti. 1998. Alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J. Biol. Chem. 273: 14503– 14515.

103. Pancholi, V., and, V. A. Fischetti. 1992. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J. Exp. Med. 176: 415– 426.

104. Park, K. J.,, M. M. Gromiha,, P. Horton, and, M. Suwa. 2005. Discrimination of outer membrane proteins using support vector machines. Bioinformatics 21: 4223– 4229.

105. Parkhill, J.,, B. W. Wren,, K. Mungall,, J. M. Ketley,, C. Churcher,, D. Basham,, T. Chillingworth,, R. M. Davies,, T. Feltwell,, S. Holroyd,, K. Jagels,, A. V. Karlyshev,, S. Moule,, M. J. Pallen,, C. W. Penn,, M. A. Quail,, M. A. Rajandream,, K. M. Rutherford,, A. H. van Vliet,, S. Whitehead, and, B. G. Barréll. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665– 668.

106. Pavlovskis, O. R.,, D. M. Rollins,, R. L. Haberberger, Jr.,, A. E. Green,, L. Habash,, S. Strocko, and, R. I. Walker. 1991. Significance of flagella in colonization resistance of rabbits immunized with Campylobacter spp. Infect. Immun. 59: 2259– 2264.

107. Pawelec, D. P.,, D. Korsak,, A. K. Wyszynska,, E. Rozynek,, J. Popowski, and, E. K. Jagusztyn-Krynicka. 2000. Genetic diversity of the Campylobacter genes coding immunodominant proteins. FEMS Microbiol. Lett. 185: 43– 49.

108. Pei, Z., and, M. J. Blaser. 1993. PEB1, the major cell-binding factor of Campylobacter jejuni, is a homolog of the binding component in gram-negative nutrient transport systems. J. Biol. Chem. 268: 18717– 18725.

109. Pei, Z.,, C. Burucoa,, B. Grignon,, S. Baqar,, X. Z. Huang,, D. J. Kopecko,, A. L. Bourgeois,, J. L. Fauchère, and, M. J. Blaser. 1998. Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect. Immun. 66: 938– 943.

110. 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.

111. Penner, J. L., and, J. N. Hennessy. 1980. Passive hemagglutination technique for serotyping Campylobacter fetus subsp. jejuni on the basis of soluble heat-stable antigens. J. Clin. Microbiol. 12: 732– 737.

112. Petruccelli, B. P.,, G. S. Murphy,, J. L. Sanchez,, S. Walz,, R. DeFraites,, J. Gelnett,, R. L. Haberberger,, P. Echeverria, and, D. N. Taylor. 1992. Treatment of traveler’s diarrhea with ciprofloxacin and loperamide. J. Infect. Dis. 165: 557– 560.

113. Poly, F.,, T. Read,, D. R. Tribble,, S. Baqar,, M. Lorenzo, and, P. Guerry. 2007. Genome sequence of a clinical isolate of Campylobacter jejuni from Thailand. Infect. Immun. 75: 3425– 3433.

114. Pope, J. E.,, A. Krizova,, A. X. Garg,, H. Thiessen-Philbrook, and, J. M. Ouimet. 2007. Campylobacter reactive arthritis: a systematic review. Semin. Arthritis Rheum. 37: 48– 55.

115. Power, M. E.,, P. Guerry,, W. D. McCubbin,, C. M. Kay, and, T. J. Trust. 1994. Structural and antigenic characteristics of Campylobacter coli FlaA flagellin. J. Bacteriol. 176: 3303– 3313.

116. Prokhorova, T. A.,, P. N. Nielsen,, J. Petersen,, T. Kofoed,, J. S. Crawford,, C. Morsczeck,, A. Boysen, and, P. Schrotz-King. 2006. Novel surface polypeptides of Campylobacter jejuni as traveller’s diarrhoea vaccine candidates discovered by proteomics. Vaccine 24: 6446– 6455.

117. Radcliff, F. J.,, S. L. Hazell,, T. Kolesnikow,, C. Doidge, and, A. Lee. 1997. Catalase, a novel antigen for Helicobacter pylori vaccination. Infect. Immun. 65: 4668– 4674.

118. Rangarajan, E. S.,, S. Bhatia,, D. C. Watson,, C. Munger,, M. Cygler,, A. Matte, and, N. M. Young. 2007. Structural context for protein N-glycosylation in bacteria: the structure of PEB3, an adhesin from Campylobacter jejuni. Protein Sci. 16: 990– 995.

119. Rao, M. R.,, A. B. Naficy,, S. J. Savarino,, R. Abu-Elyazeed,, T. F. Wierzba,, L. F. Peruski,, I. Abdel-Messih,, R. Frenck, and, J. D. Clemens. 2001. Pathogenicity and convalescent excretion of Campylobacter in rural Egyptian children. Am. J. Epidemiol. 154: 166– 173.

120. Riddle, M. S.,, J. W. Sanders,, S. D. Putnam, and, D. R. Tribble. 2006. Incidence, etiology, and impact of diarrhea among long-term travelers (U.S. military and similar populations): a systematic review. Am. J. Trop. Med. Hyg. 74: 891– 900.

121. Rollwagen, F. M.,, N. D. Pacheco,, J. D. Clements,, O. Pavlovskis,, D. M. Rollins, and, R. I. Walker. 1993. Killed Campylobacter elicits immune response and protection when administered with an oral adjuvant. Vaccine 11: 1316– 1320.

122. Ruiz, J.,, F. Marco,, I. Oliveira,, J. Vila, and, J. Gascon. 2007. Trends in antimicrobial resistance in Campylobacter spp. causing traveler’s diarrhea. APMIS 115: 218– 224.

123. Ruiz-Palacios, G. M.,, J. J. Calva,, L. K. Pickering,, Y. Lopez-Vidal,, P. Volkow,, H. Pezzarossi, and, M. S. West. 1990. Protection of breast-fed infants against Campylobacter diarrhea by antibodies in human milk. J. Pediatr. 116: 707– 713.

124. Russell, R. G.,, M. J. Blaser,, J. I. Sarmiento, and, J. Fox. 1989. Experimental Campylobacter jejuni infection in Macaca nemestrina. Infect. Immun. 57: 1438– 1444.

125. Russell, R. G.,, J. I. Sarmiento,, J. Fox, and, P. Panigrahi. 1990. Evidence of reinfection with multiple strains of Campylobacter jejuni and Campylobacter coli in Macaca nemestrina housed under hyperendemic conditions. Infect. Immun. 58: 2149– 2155.

126. Ryan, E. T.,, S. B. Calderwood, and, F. Qadri. 2006. Live attenuated oral cholera vaccines. Expert Rev. Vaccines 5: 483– 494.

127. Sabarth, N.,, S. Lamer,, U. Zimny-Arndt,, P. R. Jungblut,, T. F. Meyer, and, D. Bumann. 2002. Identification of surface proteins of Helicobacter pylori by selective biotinylation, affinity purification, and two-dimensional gel electrophoresis. J. Biol. Chem. 277: 27896– 27902.

128. Sabin, A. B. 1965. Oral poliovirus vaccine. History of its development and prospects for eradication of poliomyelitis. JAMA 194: 872– 876.

129. Samuel, M. C.,, D. J. Vugia,, S. Shallow,, R. Marcus,, S. Segler,, T. McGivern,, H. Kassenborg,, K. Reilly,, M. Kennedy,, F. Angulo, and, R. V. Tauxe. 2004. Epidemiology of sporadic Campylobacter infection in the United States and declining trend in incidence, FoodNet 1996–1999. Clin. Infect. Dis. 38 (Suppl. 3): S165– S174.

130. Sanchez, J. L.,, B. Vasquez,, R. E. Begue,, R. Meza,, G. Castellares,, C. Cabezas,, D. M. Watts,, A. M. Svennerholm,, J. C. Sadoff, and, D. N. Taylor. 1994. Protective efficacy of oral whole-cell/recombinant-B-subunit cholera vaccine in Peruvian military recruits. Lancet 344: 1273– 1276.

131. Schaumburg, J.,, O. Diekmann,, P. Hagendorff,, S. Bergmann,, M. Rohde,, S. Hammerschmidt,, L. Jansch,, J. Wehland, and, U. Karst. 2004. The cell wall subproteome of Listeria monocytogenes. Proteomics 4: 2991– 3006.

132. Schrotz-King, P.,, T. A. Prokhorova,, P. N. Nielsen,, J. S. Crawford, and, C. Morsczeck. 2007. Campylobacter jejuni proteomics for new travellers’ diarrhoea vaccines. Travel Med. Infect. Dis. 5: 106– 109.

133. Sizemore, D. R.,, B. Warner,, J. Lawrence,, A. Jones, and, K. P. Killeen. 2006. Live, attenuated Salmonella typhimurium vectoring Campylobacter antigens. Vaccine 24: 3793– 3803.

134. Sjogren, E.,, G. Ruiz-Palacios, and, B. Kaijser. 1989. Campylobacter jejuni isolations from Mexican and Swedish patients, with repeated symptomatic and/or asymptomatic diarrhoea episodes. Epidemiol. Infect. 102: 47– 57.

135. Song, Y. C.,, S. Jin,, H. Louie,, D. Ng,, R. Lau,, Y. Zhang,, R. Weerasekera,, S. Al Rashid,, L. A. Ward,, S. D. Der, and, V. L. Chan. 2004. FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion. Mol. Microbiol. 53: 541– 553.

136. Spence, J. M., and, V. L. Clark. 2000. Role of ribosomal protein L12 in gonococcal invasion of Hec1B cells. Infect. Immun. 68: 5002– 5010.

137. Steffen, R. 1986. Epidemiologic studies of travelers’ diarrhea, severe gastrointestinal infections, and cholera. Rev. Infect. Dis. 8 (Suppl. 2): S122– S130.

138. Struyvé, M.,, M. Moons, and, J. Tommassen. 1991. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J. Mol. Biol. 218: 141– 148.

139. Szymanski, C. M.,, R. Yao,, C. P. Ewing,, T. J. Trust, and, P. Guerry. 1999. Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol. 32: 1022– 1030.

140. Taylor, D. 1992. Campylobacter infections in developing countries, p. 20– 30. In I. Nachamkin,, M. Blaser, and, L. Tompkins (ed.), Campylobacter jejuni: Current Status and Future Trends. American Society for Microbiology, Washington, DC.

141. Taylor, D. N.,, D. M. Perlman,, P. D. Echeverria,, U. Lexomboon, and, M. J. Blaser. 1993. Campylobacter immunity and quantitative excretion rates in Thai children. J. Infect. Dis. 168: 754– 758.

142. Thornley, J. P.,, D. Jenkins,, K. Neal,, T. Wright,, J. Brough, and, R. C. Spiller. 2001. Relationship of Campylobacter toxigenicity in vitro to the development of postinfectious irritable bowel syndrome. J. Infect. Dis. 184: 606– 609.

143. Torres, O., and, J. R. Cruz. 1993. Protection against Campylobacter diarrhea: role of milk IgA antibodies against bacterial surface antigens. Acta Paediatr. 82: 835– 838.

144. Tribble, D. R.,, S. Baqar,, D. A. Scott,, M. L. Oplinger,, F. Trespalacios,, R. I. Walker,, J. D. Clements, and, A. L. Burgeois. 2001. Clinical development of an inactivated whole cell Campylobacter vaccine candidate. In Vaccines for Enteric Diseases, 2001, Tampere, Finland.

145. Tribble, D. R.,, J. W. Sanders,, L. W. Pang,, C. Mason,, C. Pitarangsi,, S. Baqar,, A. Armstrong,, P. Hshieh,, A. Fox,, E. A. Maley,, C. Lebron,, D. J. Faix,, J. V. Lawler,, G. Nayak,, M. Lewis,, L. Bodhidatta, and, D. A. Scott. 2007. Traveler’s diarrhea in Thailand: randomized, double-blind trial comparing single-dose and 3-day azithromycin-based regimens with a 3-day levofloxacin regimen. Clin. Infect. Dis. 44: 338– 346.

146. Vitovec, J.,, B. Koudela,, J. Sterba,, I. Tomancova,, Z. Matyas, and, P. Vladik. 1989. The gnotobiotic piglet as a model for the pathogenesis of Campylobacter jejuni infection. Zentralbl. Bakteriol. 271: 91– 103.

147. Waldispühl, J.,, B. Berger,, P. Clote, and, J. M. Steyaert. 2006. Predicting transmembrane beta-barrels and interstrand residue interactions from sequence. Proteins 65: 61– 74.

148. Walker, R. I. 2005. Considerations for development of whole cell bacterial vaccines to prevent diarrheal diseases in children in developing countries. Vaccine 23: 3369– 3385.

149. Walker, R. I.,, D. M. Rollins, and, D. H. Burr. 1992. Studies of Campylobacter infection in the adult rabbit, p. 139– 147. In I. Nachamkin,, M. Blaser, and, L. Tompkins (ed.), Campylobacter jejuni: Current Status and Future Trends. American Society for Microbiology, Washington, DC.

150. Watson, R. O.,, V. Novik,, D. Hofreuter,, M. Lara-Tejero, and, J. E. Galán. 2007. A MyD88-deficient mouse model reveals a role for Nramp1 in Campylobacter jejuni infection. Infect. Immun. 75: 1994– 2003.

151. Weynants, V. E.,, C. M. Feron,, K. K. Goraj,, M. P. Bos,, P. A. Denoel,, V. G. Verlant,, J. Tommassen,, I. R. A. Peak,, R. C. Judd,, M. P. Jennings, and, J. T. Poolman. 2007. Additive and synergistic bactericidal activity of antibodies directed against minor outer membrane proteins of Neisseria meningitidis. Infect. Immun. 75: 5432– 5442.

152. Wittmann-Liebold, B.,, H. R. Graack, and, T. Pohl. 2006. Two-dimensional gel electrophoresis as tool for proteomics studies in combination with protein identification by mass spectrometry. Proteomics 6: 4688– 4703.

153. Zhang, Q.,, J. C. Meitzler,, S. Huang, and, T. Morishita. 2000. Sequence polymorphism, predicted secondary structures, and surface-exposed conformational epitopes of Campylobacter major outer membrane protein. Infect. Immun. 68: 5679– 5689.