1887

Abstract

Increasing numbers of have been isolated from humans and animals with gastroenteritis, although the virulence mechanism of this species remains largely unknown. Here, we show that isolated from a patient with diarrhoea in Thailand produced a novel variant of cytolethal distending toxin (CDT). Sequencing of a 13 965 bp genomic region of carrying the genes coding for Ch-CDT revealed three ORFs of 798, 804 and 537 bp, which code for the Ch-CdtA, Ch-CdtB and Ch-CdtC subunits, respectively. The deduced amino acid sequence of Ch-CdtA showed ∼38.9 % homology with the CdtA of , but sequences of Ch-CdtB and Ch-CdtC were homologous to CdtB (65.7 %) and CdtC (33.1 %) of , respectively. Filter-sterilized sonic lysate of demonstrated distension and death of HeLa cells by arresting the cell cycle at the G/M phase and phosphorylation of host histone H2AX, a sensitive marker of DNA double-strand breaks. Rabbit antiserum raised against recombinant Ch-CdtB was not reactive against the recombinant CdtB protein of . A reconstituted Ch-CDT holotoxin prepared using each of the recombinant subunit proteins demonstrated distension and death of HeLa cells, suggesting that the isolate indeed produced functionally active Ch-CDT. Furthermore, the immunological distinctiveness of the Ch-CDT produced by and the increasing prevalence of the species in patients and animals with gastroenteritis suggest that this species may be an important emerging zoonotic pathogen.

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2015-10-01
2019-10-20
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References

  1. Asakura M. , Samosornsuk W. , Taguchi M. , Kobayashi K. , Misawa N. , Kusumoto M. , Nishimura K. , Matsuhisa A. , Yamasaki S. . ( 2007;). Comparative analysis of cytolethal distending toxin (cdt) genes among Campylobacter jejuni, C. coli and C. fetus strains. Microb Pathog 42: 174–183 [CrossRef] [PubMed].
    [Google Scholar]
  2. Asakura M. , Samosornsuk W. , Hinenoya A. , Misawa N. , Nishimura K. , Matsuhisa A. , Yamasaki S. . ( 2008;). Development of a cytolethal distending toxin (cdt) gene-based species-specific multiplex PCR assay for the detection and identification of Campylobacter jejuni, Campylobacter coli and Campylobacter fetus . FEMS Immunol Med Microbiol 52: 260–266 [CrossRef] [PubMed].
    [Google Scholar]
  3. Bullman S. , O'Leary J. , Corcoran D. , Sleator R. D. , Lucey B. . ( 2012;). Molecular-based detection of non-culturable and emerging campylobacteria in patients presenting with gastroenteritis. Epidemiol Infect 140: 684–688 [CrossRef] [PubMed].
    [Google Scholar]
  4. Chaban B. , Ngeleka M. , Hill J. E. . ( 2010;). Detection and quantification of 14 Campylobacter species in pet dogs reveals an increase in species richness in feces of diarrheic animals. BMC Microbiol 10: 73 [CrossRef] [PubMed].
    [Google Scholar]
  5. Dasti J. I. , Tareen A. M. , Lugert R. , Zautner A. E. , Gross U. . ( 2010;). Campylobacter jejuni: a brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int J Med Microbiol 300: 205–211 [CrossRef] [PubMed].
    [Google Scholar]
  6. Edmonds P. , Patton C. M. , Griffin P. M. , Barrett T. J. , Schmid G. P. , Baker C. N. , Lambert M. A. , Brenner D. J. . ( 1987;). Campylobacter hyointestinalis associated with human gastrointestinal disease in the United States. J Clin Microbiol 25: 685–691 [PubMed].
    [Google Scholar]
  7. Fennell C. L. , Rompalo A. M. , Totten P. A. , Bruch K. L. , Flores B. M. , Stamm W. E. . ( 1986;). Isolation of “Campylobacter hyointestinalis” from a human. J Clin Microbiol 24: 146–148 [PubMed].
    [Google Scholar]
  8. Gebhart C. J. , Ward G. E. , Chang K. , Kurtz H. J. . ( 1983;). Campylobacter hyointestinalis (new species) isolated from swine with lesions of proliferative ileitis. Am J Vet Res 44: 361–367 [PubMed].
    [Google Scholar]
  9. Gebhart C. J. , Edmonds P. , Ward G. E. , Kurtz H. J. , Brenner D. J. . ( 1985;). “Campylobacter hyointestinalis” sp. nov.: a new species of Campylobacter found in the intestines of pigs and other animals. J Clin Microbiol 21: 715–720 [PubMed].
    [Google Scholar]
  10. Gebhart C. J. , Murtaugh M. P. , Lin G. F. , Ward G. E. . ( 1990;). Species-specific DNA probes for Campylobacter species isolated from pigs with proliferative enteritis. Vet Microbiol 24: 367–379 [CrossRef] [PubMed].
    [Google Scholar]
  11. Gharst G. , Oyarzabal O. A. , Hussain S. K. . ( 2013;). Review of current methodologies to isolate and identify Campylobacter spp. from foods. J Microbiol Methods 95: 84–92 [CrossRef] [PubMed].
    [Google Scholar]
  12. Gorkiewicz G. , Feierl G. , Zechner R. , Zechner E. L. . ( 2002;). Transmission of Campylobacter hyointestinalis from a pig to a human. J Clin Microbiol 40: 2601–2605 [CrossRef] [PubMed].
    [Google Scholar]
  13. Hänninen M. L. , Sarelli L. , Sukura A. , On S. L. , Harrington C. S. , Matero P. , Hirvelä-Koski V. . ( 2002;). Campylobacter hyointestinalis subsp. hyointestinalis, a common Campylobacter species in reindeer. J Appl Microbiol 92: 717–723 [CrossRef] [PubMed].
    [Google Scholar]
  14. Hickey T. E. , McVeigh A. L. , Scott D. A. , Michielutti R. E. , Bixby A. , Carroll S. A. , Bourgeois A. L. , Guerry P. . ( 2000;). Campylobacter jejuni cytolethal distending toxin mediates release of interleukin-8 from intestinal epithelial cells. Infect Immun 68: 6535–6541 [CrossRef] [PubMed].
    [Google Scholar]
  15. Hill B. D. , Thomas R. J. , Mackenzie A. R. . ( 1987;). Campylobacter hyointestinalis-associated enteritis in Moluccan rusa deer (Cervus timorensis subsp. Moluccensis). J Comp Pathol 97: 687–694 [CrossRef] [PubMed].
    [Google Scholar]
  16. Hinenoya A. , Naigita A. , Ninomiya K. , Asakura M. , Shima K. , Seto K. , Tsukamoto T. , Ramamurthy T. , Faruque S. M. , Yamasaki S. . ( 2009;). Prevalence and characteristics of cytolethal distending toxin-producing Escherichia coli from children with diarrhea in Japan. Microbiol Immunol 53: 206–215 [CrossRef] [PubMed].
    [Google Scholar]
  17. Hinenoya A. , Shima K. , Asakura M. , Nishimura K. , Tsukamoto T. , Ooka T. , Hayashi T. , Ramamurthy T. , Faruque S. M. , Yamasaki S. . ( 2014;). Molecular characterization of cytolethal distending toxin gene-positive Escherichia coli from healthy cattle and swine in Nara, Japan. BMC Microbiol 14: 97 [CrossRef] [PubMed].
    [Google Scholar]
  18. Inglis G. D. , Boras V. F. , Houde A. . ( 2011;). Enteric campylobacteria and RNA viruses associated with healthy and diarrheic humans in the Chinook health region of southwestern Alberta, Canada. J Clin Microbiol 49: 209–219 [CrossRef] [PubMed].
    [Google Scholar]
  19. Jain D. , Prasad K. N. , Sinha S. , Husain N. . ( 2008;). Differences in virulence attributes between cytolethal distending toxin positive and negative Campylobacter jejuni strains. J Med Microbiol 57: 267–272 [CrossRef] [PubMed].
    [Google Scholar]
  20. Johnson W. M. , Lior H. . ( 1987;). Response of Chinese hamster ovary cells to a cytolethal distending toxin (CDT) of Escherichia coli and possible misinterpretation as heat-labile (LT) enterotoxin. FEMS Microbiol Lett 43: 19–23 [CrossRef].
    [Google Scholar]
  21. Kabir S. M. , Kikuchi K. , Asakura M. , Shiramaru S. , Tsuruoka N. , Goto A. , Hinenoya A. , Yamasaki S. . ( 2011;). Evaluation of a cytolethal distending toxin (cdt) gene-based species-specific multiplex PCR assay for the identification of Campylobacter strains isolated from diarrheal patients in Japan. Jpn J Infect Dis 64: 19–27 [PubMed].
    [Google Scholar]
  22. Lastovica A. J. . ( 1996;). Campylobacter/Helicobacter bacteraemia in Cape Town, South Africa, 1977–1995. . In Campylobacters, Helicobacters and Related Organisms, pp. 475–479. Edited by Newell D. G. , Ketley J. M. , Feldman R. A. . New York: Plenum Press;.[CrossRef]
    [Google Scholar]
  23. Lastovica A. J. , Le Roux E. . ( 2000;). Efficient isolation of campylobacteria from stools. J Clin Microbiol 38: 2798–2799 [PubMed].
    [Google Scholar]
  24. Li L. , Sharipo A. , Chaves-Olarte E. , Masucci M. G. , Levitsky V. , Thelestam M. , Frisan T. . ( 2002;). The Haemophilus ducreyi cytolethal distending toxin activates sensors of DNA damage and repair complexes in proliferating and non-proliferating cells. Cell Microbiol 4: 87–99 [CrossRef] [PubMed].
    [Google Scholar]
  25. Man S. M. . ( 2011;). The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol Hepatol 8: 669–685 [CrossRef] [PubMed].
    [Google Scholar]
  26. Matsuda M. , Shigematsu M. , Tazumi A. , Sekizuka T. , Takamiya S. , Millar B. C. , Taneike I. , Moore J. E. . ( 2008;). Cloning and structural analysis of the full-length cytolethal distending toxin (cdt) gene operon from Campylobacter lari . Br J Biomed Sci 65: 195–199 [PubMed].
    [Google Scholar]
  27. Minet J. , Grosbois B. , Megraud F. . ( 1988;). Campylobacter hyointestinalis: an opportunistic enteropathogen?. J Clin Microbiol 26: 2659–2660 [PubMed].
    [Google Scholar]
  28. Nakajima T. , Tazumi A. , Hirayama J. , Hayashi K. , Tasaki E. , Asakura M. , Yamasaki S. , Moored J. E. , Millar B. C. , other authors . ( 2012;). Expression and analysis of a cytolethal distending toxin (cdt) gene operon in Campylobacter lari . Br J Biomed Sci 69 26–30.
    [Google Scholar]
  29. Ohya T. , Nakazawa M. . ( 1992;). Production and some properties of cytotoxins produced by Campylobacter species isolated from proliferative enteropathy in swine. J Vet Med Sci 54: 1031–1033 [CrossRef] [PubMed].
    [Google Scholar]
  30. Okuda J. , Fukumoto M. , Takeda Y. , Nishibuchi M. . ( 1997;). Examination of diarrheagenicity of cytolethal distending toxin: suckling mouse response to the products of the cdtABC genes of Shigella dysenteriae . Infect Immun 65: 428–433 [PubMed].
    [Google Scholar]
  31. Oporto B. , Hurtado A. . ( 2011;). Emerging thermotolerant Campylobacter species in healthy ruminants and swine. Foodborne Pathog Dis 8: 807–813 [CrossRef] [PubMed].
    [Google Scholar]
  32. Pickett C. L. , Pesci E. C. , Cottle D. L. , Russell G. , Erdem A. N. , Zeytin H. . ( 1996;). Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB gene. Infect Immun 64: 2070–2078 [PubMed].
    [Google Scholar]
  33. Prouzet-Mauléon V. , Labadi L. , Bouges N. , Ménard A. , Mégraud F. . ( 2006;). Arcobacter butzleri: underestimated enteropathogen. Emerg Infect Dis 12: 307–309 [CrossRef] [PubMed].
    [Google Scholar]
  34. Purdy D. , Buswell C. M. , Hodgson A. E. , McAlpine K. , Henderson I. , Leach S. A. . ( 2000;). Characterisation of cytolethal distending toxin (CDT) mutants of Campylobacter jejuni . J Med Microbiol 49: 473–479 [PubMed].[CrossRef]
    [Google Scholar]
  35. Russell R. G. , Kiehlbauch J. A. , Gebhart C. J. , DeTolla L. J. . ( 1992;). Uncommon Campylobacter species in infant Macaca nemestrina monkeys housed in a nursery. J Clin Microbiol 30: 3024–3027.
    [Google Scholar]
  36. Samosornsuk W. , Asakura M. , Yoshida E. , Taguchi T. , Eampokalap B. , Chaicumpa W. , Yamasaki S. . ( 2015;). Isolation and characterization of Campylobacter strains from diarrheal patients in Bangkok and its suburb in Thailand. Jpn J Infect Dis 68: 209–215 [CrossRef] [PubMed].
    [Google Scholar]
  37. Shima A. , Hinenoya A. , Asakura M. , Sugimoto N. , Tsukamoto T. , Ito H. , Nagita A. , Faruque S. M. , Yamasaki S. . ( 2012;). Molecular characterizations of cytolethal distending toxin produced by Providencia alcalifaciens strains isolated from patients with diarrhea. Infect Immun 80: 1323–1332 [CrossRef] [PubMed].
    [Google Scholar]
  38. Vandenberg O. , Dediste A. , Houf K. , Ibekwem S. , Souayah H. , Cadranel S. , Douat N. , Zissis G. , Butzler J. P. , Vandamme P. . ( 2004;). Arcobacter species in humans. Emerg Infect Dis 10: 1863–1867 [CrossRef] [PubMed].
    [Google Scholar]
  39. Vandenberg O. , Houf K. , Douat N. , Vlaes L. , Retore P. , Butzler J. P. , Dediste A. . ( 2006;). Antimicrobial susceptibility of clinical isolates of non-jejuni/coli campylobacters and arcobacters from Belgium. J Antimicrob Chemother 57: 908–913 [CrossRef] [PubMed].
    [Google Scholar]
  40. Yamasaki S. , Asakura M. , Tsukamoto T. , Faruque S. M. , Deb R. , Ramamurthy T. . ( 2006;). Cytolethal distending toxin (CDT): genetic diversity, structure and role in diarrheal disease. Toxin Rev 25: 61–88 [CrossRef].
    [Google Scholar]
  41. Yokoyama K. . ( 2006;). [Occurrence of Campylobacter food poisoning]. Jpn J Food Microbiol 23: 109–113 (in Japanese).
    [Google Scholar]
  42. Young V. B. , Knox K. A. , Pratt J. S. , Cortez J. S. , Mansfield L. S. , Rogers A. B. , Fox J. G. , Schauer D. B. . ( 2004;). In vitro and in vivo characterization of Helicobacter hepaticus cytolethal distending toxin mutants. Infect Immun 72: 2521–2527 [CrossRef] [PubMed].
    [Google Scholar]
  43. Yutsudo T. , Nakabayashi N. , Hirayama T. , Takeda Y. . ( 1987;). Purification and some properties of a Vero toxin from Escherichia coli O157 : H7 that is immunologically unrelated to Shiga toxin. Microb Pathog 3: 21–30 [CrossRef] [PubMed].
    [Google Scholar]
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