Characterization of two Campylobacter jejuni strains for use in volunteer experimental-infection studies

Infection and Immunity

Volumn 76, Issue 12, 2008, Pages 5655-5667

  Poly, Frédéric ^a   Read, Timothy D ^a   Chen, Yu Han ^b   Monteiro, Mario A ^b   Serichantalergs, Oralak ^c   Pootong, Piyarat ^c   Bodhidatta, Ladaporn ^c   Mason, Carl J ^c   Rockabrand, David ^a   Baqar, Shahida ^a   Porter, Chad K ^a   Tribble, David ^d   Darsley, Michael ^e   Guerry, Patricia ^a  

^a NAVAL MEDICAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF GUELPH   (Canada)

^c ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

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

^e ACE BioSciences AS   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC; BACTERIAL POLYSACCHARIDE; FLAGELLIN; GALACTOSE; GANGLIOSIDE; LIPOOLIGOSACCHARIDE; N ACETYLGLUCOSAMINE; OLIGOSACCHARIDE; SODIUM PHOSPHATE COTRANSPORTER; TETRACYCLINE;

ADULT; ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; CAMPYLOBACTER JEJUNI; CARBOHYDRATE ANALYSIS; CASE REPORT; CONTROLLED STUDY; DIARRHEA; DNA PROBE; GENE LOCUS; GLYCOSYLATION; GRAM NEGATIVE INFECTION; GUILLAIN BARRE SYNDROME; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; SOUTHEAST ASIA;

BASE SEQUENCE; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; GANGLIOSIDES; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HUMAN EXPERIMENTATION; HUMANS; LIPOPOLYSACCHARIDES; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES, BACTERIAL;

EID: 57349137205     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00780-08     Document Type: Article

References (64)

1. Altekruse, S. F., N. J. Stern, P. I. Fields, and D. L. Swerdlow. 1999. Campylobacter jejuni - an emerging foodborne pathogen. Emerg. Infect. Dis. 5:28-35.
2. Ang, C. W., M. A. de Klerk, H. P. Endtz, B. C. Jacobs, J. D. Laman, F. G. van der Meche, and P. A. van Doorn. 2001. Guillain-Barre syndrome- and Miller Fisher syndrome-associated Campylobacter jejuni lipopolysaccharides induce anti-GM1 and anti-GQ1b antibodies in rabbits. Infect. Immun. 69:2462-2469.
3. Ang, C. W., B. C. Jacobs, and J. D. Laman. 2004. The Guillain-Barre syndrome: a true case of molecular mimicry. Trends Immunol. 25:61-66.
4. Ang, C. W., J. D. Laman, H. J. Willison, E. R. Wagner, H. P. Endtz, M. A. de Klerk, A. P. Tio-Gillen, N. Van den Braak, B. C. Jacobs, and P. A. van Doorn. 2002. Structure of Campylobacter jejuni lipopolysaccharides determines antiganglioside specificity and clinical features of Guillain-Barré and Miller Fisher patients. Infect. Immun. 70:1202-1208.
5. Aspinall, G. O., C. M. Lynch, H. Pang, R. T. Shaver, and A. P. Moran. 1995. Chemical structures of the core region of Campylobacter jejuni O:3 lipopolysaccharide and an associated polysaccharide. Eur. J. Biochem. 231:570-578.
6. 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.
7. Batchelor, R. A., B. M. Pearson, L. M. Friis, P. Guerry, and J. M. Wells. 2004. Nucleotide sequences and comparison of two large conjugative plasmids from different Campylobacter species. Microbiology 150:3507- 3517.
8. 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.
9. Chiba, A., S. Kusunoki, H. Obata, R. Machinami, and I. Kanazawa. 1993. Serum anti-GQ1b IgG antibody is associated with ophthalmoplegia in Miller Fisher syndrome and Guillain-Barre syndrome: clinical and immunohistochemical studies. Neurology 43:1911-1917.
10. Ciucanu, I., and F. Kerek. 1984. A simple and rapid method for the permethylation of carbohydrates. Carbohydr. Res. 131:209-217.
11. Cover, T. L., and S. R. Blanke. 2005. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat. Rev. Microbiol. 3:320-332.
12. Dubois, M. K., J. Giles, J. Hamilton, P. Rebers, and F. Smith. 1956. Colormetric method for the determination of sugars and related substances. Anal. Chem. 28:350-356.
13. 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.
14. Gibreel, A., D. M. Tracz, L. Nonaka, T. M. Ngo, S. R. Connell, and D. E. Taylor. 2004. Incidence of antibiotic resistance in Campylobacter jejuni isolated in Alberta, Canada, from 1999 to 2002, with special reference to tet(O)-mediated tetracycline resistance. Antimicrob. Agents Chemother. 48: 3442-3450.
15. 13C NMR analysis. J. Biol. Chem. 275:3896-3906.
16. Gilbert, M., C. T. Parker, and A. P. Moran. 2008. Campylobacter jejuni lipooligosaccharides: structures and biosynthesis, p. 483-504. In I. Nachamkin, C. M. Szymanski, and M. Blaser (ed.), Campylobacter, 3rd ed. ASM Press, Washington, DC.
17. Guerry, P. 2007. Campylobacter flagella: not just for motility. Trends Microbiol. 15:456-461.
18. Guerry, P., R. A. Alm, M. E. Power, S. M. Logan, and T. J. Trust. 1991. Role of two flagellin genes in Campylobacter motility. J. Bacteriol. 173:4757-4764.
19. Guerry, P., C. P. Ewing, T. E. Hickey, M. M. Prendergast, and A. P. Moran. 2000. Sialylation of lipooligosaccharide cores affects immunogenicity and serum resistance of Campylobacter jejuni. Infect. Immun. 68:6656-6662.
20. Guerry, P., C. P. Ewing, M. Schirm, M. Lorenzo, J. Kelly, D. Pattarini, G. Majam, P. Thibault, and S. Logan. 2006. Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol. Microbiol. 60:299-311.
21. Guerry, P., C. M. Szymanski, M. M. Prendergast, T. E. Hickey, C. P. Ewing, D. L. Pattarini, and A. P. Moran. 2002. Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect. Immun. 70:787-793.
22. 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.
23. Hofreuter, D., J. Tsai, R. O. Watson, V. Novik, B. Altman, M. Benitez, C. Clark, C. Perbost, T. Jarvie, L. Du, and J. E. Galan. 2006. Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 74:4694-4707.
24. Kanipes, M. I., L. C. Holder, A. T. Corcoran, A. P. Moran, and P. Guerry. 2004. A deep-rough mutant of Campylobacter jejuni 81-176 is noninvasive for intestinal epithelial cells. Infect. Immun. 72:2452-2455.
25. Kanipes, M. I., E. Papp-Szabo, P. Guerry, and M. A. Monteiro. 2006. Mutation of waaC, encoding heptosyltransferase I in Campylobacter jejuni 81-176, affects the structure of both lipooligosaccharide and capsular carbohydrate. J. Bacteriol. 188:3273-3279.
26. Kanipes, M. I., X. Tan, A. Akelaitis, J. Li, D. Rockabrand, P. Guerry, and M. A. Monteiro. 2008. Genetic analysis of lipooligosaccharide core biosynthesis in Campylobacter jejuni 81-176. J. Bacteriol. 190:1568-1574.
27. Karlyshev, A. V., O. L. Champion, C. Churcher, J. R. Brisson, H. C. Jarrell, M. Gilbert, D. Brochu, M. F. St. Michael, J. Li, W. W. Wakarchuk, I. Goodhead, M. Sanders, K. Stevens, B. White, J. Parkhill, B. W. Wren, and C. M. Szymanski. 2005. Analysis of Campylobacter jejuni capsular loci reveals multiple mechanisms for the generation of structural diversity and the ability to form complex heptoses. Mol. Microbiol. 55:90-103.
28. 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.
29. Kopecko, D. J., L. Hu, and K. J. Zaal. 2001. Campylobacter jejuni -microtubule-dependent invasion. Trends Microbiol. 9:389-396.
30. Logan, S. M., I. C. Schoenhofen, and P. Guerry. 2008. O-linked flagellar glycosylation in Campylobacter, p. 471-481. In I. Nachamkin, C. M. Szymanski, and M. Blaser (ed.), Campylobacter, 3rd ed. ASM Press, Washington, DC.
31. Logan, S. M., J. F. Kelly, P. Thibault, C. P. Ewing, and P. Guerry. 2002. Structural heterogeneity of carbohydrate modifications affects serospecificity of Campylobacter flagellins. Mol. Microbiol. 46:587-597.
32. Mandrell, R. E., C. T. Parker, A. H. Bates, E. Vinogradov, J. Li, F. St. Michael, and M. Gilbert. 2007. Campylobacter jejuni strain RM1221 lipooligosaccharide mimics globo- and lactoneo-series P blood group antigens, abstr. D-027. Abstr. 107th Gen. Meet. Am. Soc. Microbiol.
33. Mardis, E. R. 2008. The impact of next-generation sequencing technology on genetics. Trends Genet. 24:133-141.
34. Margulies, M., M. Egholm, W. E. Altman, S. Attiya, J. S. Bader, L. A. Bemben, J. Berka, M. S. Braverman, Y. J. Chen, Z. Chen, S. B. Dewell, L. Du, J. M. Fierro, X. V. Gomes, B. C. Godwin, W. He, S. Helgesen, C. H. Ho, G. P. Irzyk, S. C. Jando, M. L. Alenquer, T. P. Jarvie, K. B. Jirage, J. B. Kim, J. R. Knight, J. R. Lanza, J. H. Leamon, S. M. Lefkowitz, M. Lei, J. Li, K. L. Lohman, H. Lu, V. B. Makhijani, K. E. McDade, M. P. McKenna, E. W. Myers, E. Nickerson, J. R. Nobile, R. Plant, B. P. Puc, M. T. Ronan, G. T. Roth, G. J. Sarkis, J. F. Simons, J. W. Simpson, M. Srinivasan, K. R. Tartaro, A. Tomasz, K. A. Vogt, G. A. Volkmer, S. H. Wang, Y. Wang, M. P. Weiner, P. Yu, R. F. Begley, and J. M. Rothberg. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376-380.
35. McNally, D. J., A. J. Aubry, J. P. Hui, N. H. Khieu, D. Whitfield, C. P. Ewing, P. Guerry, J. R. Brisson, S. M. Logan, and E. C. Soo. 2007. Targeted metabolomics analysis of Campylobacter coli VC167 reveals legionaminic acid derivatives as novel flagellar glycans. J. Biol. Chem. 282:14463-14475.
36. McNally, D. J., J. P. Hui, A. J. Aubry, K. K. Mui, P. Guerry, J. R. Brisson, S. M. Logan, and E. C. Soo. 2006. Functional characterization of the flagellar glycosylation locus in Campylobacter jejuni 81-176 using a focused metabolomics approach. J. Biol. Chem. 281:18489-18498.
37. McNally, D. J., M. P. Lamoureux, A. V. Karlyshev, L. M. Fiori, J. Li, G. Thacker, R. A. Coleman, N. H. Khieu, B. W. Wren, J. R. Brisson, H. C. Jarrell, and C. M. Szymanski. 2007. Commonality and biosynthesis of the O-methyl phosphoramidate capsule modification in Campylobacter jejuni. J. Biol. Chem. 282:28566-28576.
38. Moran, A. P. 1997. Structure and conserved characteristics of Campylobacter jejuni lipopolysaccharides. J. Infect. Dis. 176(Suppl. 2):S115-S121.
39. 1a-like epitope. Infect. Immun. 70:5299-5303.
40. Nirdnoy, W., C. J. Mason, and P. Guerry. 2005. Mosaic structure of a multiple-drug-resistant, conjugative plasmid from Campylobacter jejuni. Antimicrob. Agents Chemother. 49:2454-2459.
41. Oberhelman, R. A., and D. N. Taylor. 2000. Campylobacter infections in developing countries, p 139-154. In I. Nachamkin and M. J. Blaser (ed.), Campylobacter, 2nd ed. ASM Press, Washington, DC.
42. 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.
43. Parker, C. T., S. T. Horn, M. Gilbert, W. G. Miller, D. L. Woodward, and R. E. Mandrell. 2005. Comparison of Campylobacter jejuni lipooligosaccharide biosynthesis loci from a variety of sources. J. Clin. Microbiol. 43:2771-2781.
44. Parker, C. T., B. Quinones, W. G. Miller, S. T. Horn, and R. E. Mandrell. 2006. Comparative genomic analysis of Campylobacter jejuni strains reveals diversity due to genomic elements similar to those present in C. jejuni strain RM1221. J. Clin. Microbiol. 44:4125-4135.
45. 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. Barrell. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668.
46. 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.
47. Poly, F., D. Threadgill, and A. Stintzi. 2004. Identification of Campylobacter jejuni ATCC 43431-specific genes by whole microbial genome comparisons. J. Bacteriol. 186:4781-4795.
48. Pratt, A., and V. Korolik. 2005. Tetracycline resistance of Australian Campylobacter jejuni and Campylobacter coli isolates. J. Antimicrob. Chemother. 55:452-460.
49. Prendergast, M. M., D. R. Tribble, S. Baqar, D. A. Scott, J. A. Ferris, R. I. Walker, and A. P. Moran. 2004. In vivo phase variation and serologic response to lipooligosaccharide of Campylobacter jejuni in experimental human infection. Infect. Immun. 72:916-922.
50. Reina, J., N. Borrell, and A. Serra. 1992. Emergence of resistance to erythromycin and fluoroquinolones in thermotolerant Campylobacter strains isolated from feces 1987-1991. Eur. J. Clin. Microbiol. Infect. Dis. 11:1163-1166.
51. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
52. Sawardeker, J., and J. Sloneker. 1967. Quantitative determination of monosaccharides as their alditol acetates by gas liquid chromatograph. Anal. Chem. 37:1602-1604.
53. Serichantalergs, O., A. Dalsgaard, L. Bodhidatta, S. Krasaesub, C. Pitarangsi, A. Srijan, and C. J. Mason. 2007. Emerging fluoroquinolone and macrolide resistance of Campylobacter jejuni and Campylobacter coli isolates and their serotypes in Thai children from 1991 to 2000. Epidemiol. Infect. 135:1299-1306.
54. Shendure, J., R. D. Mitra, C. Varma, and G. M. Church. 2004. Advanced sequencing technologies: methods and goals. Nat. Rev. Genet. 5:335-344.
55. Stintzi, A., D. Marlow, K. Palyada, H. Naikare, R. Panciera, L. Whitworth, and C. Clarke. 2005. Use of genome-wide expression profiling and mutagenesis to study the intestinal lifestyle of Campylobacter jejuni. Infect. Immun. 73:1797-1810.
56. Suerbaum, S., C. Josenhans, T. Sterzenbach, B. Drescher, P. Brandt, M. Bell, M. Droge, B. Fartmann, H. P. Fischer, Z. Ge, A. Horster, R. Holland, K. Klein, J. Konig, L. Macko, G. L. Mendz, G. Nyakatura, D. B. Schauer, Z. Shen, J. Weber, M. Frosch, and J. G. Fox. 2003. The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc. Natl. Acad. Sci. USA 100:7901-7906.
57. Taboada, E. N., R. R. Acedillo, C. D. Carrillo, W. A. Findlay, D. T. Medeiros, O. L. Mykytczuk, M. J. Roberts, C. A. Valencia, J. M. Farber, and J. H. Nash. 2004. Large-scale comparative genomics meta-analysis of Campylobacter jejuni isolates reveals low level of genome plasticity. J. Clin. Microbiol. 42:4566-4576.
58. Thibault, P., S. M. Logan, J. F. Kelly, J. R. Brisson, C. P. Ewing, T. J. Trust, and P. Guerry. 2001. Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J. Biol. Chem. 276:34862-34870.
59. Vimr, E., and C. Lichtensteiger. 2002. To sialylate, or not to sialylate: that is the question. Trends Microbiol. 10:254-257.
60. Westphal, O. K., and K. Jann. 1965. Bacterial lipooligosaccharde. Extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5:83-91.
61. Willison, H. J., and N. Yuki. 2002. Peripheral neuropathies and anti-glycolipid antibodies. Brain 125:2591-2625.
62. Wosten, M. M., C. T. Parker, A. van Mourik, M. R. Guilhabert, L. van Dijk, and J. P. van Putten. 2006. The Campylobacter jejuni PhosS/PhosR operon represents a non-classical phosphate-sensitive two-component system. Mol. Microbiol. 62:278-291.
63. Yao, R., D. H. Burr, P. Doig, T. J. Trust, H. Niu, and P. Guerry. 1994. Isolation of motile and non-motile insertional mutants of Campylobacter jejuni: the role of motility in adherence and invasion of eukaryotic cells. Mol. Microbiol. 14:883-893.
64. Yuki, N., K. Susuki, M. Koga, Y. Nishimoto, M. Odaka, K. Hirata, K. Taguchi, T. Miyatake, K. Furukawa, T. Kobata, and M. Yamada. 2004. Carbohydrate mimicry between human ganglioside GM1 and Campylobacter jejuni lipooligosaccharide causes Guillain-Barre syndrome. Proc. Natl. Acad. Sci. USA 101:11404-11409.