1887

Abstract

is an emerging pathogen transmitted by a zoonotic pathway to humans. Despite rising numbers of infections and potentially fatal outcomes, data on the colonization of the human host are lacking up to now. In this study, adhesion of two isolates to human epithelial cells, invasion of host cells and the function of two putative virulence factors with respect to these processes were investigated. strains BR-AD22 and 809 were able to adhere to Detroit562 and HeLa cells, and invade these epithelial cell lines with a rate comparable to other pathogens as shown by scanning electron microscopy, fluorescence microscopy and replication assays. Infection led to detrimental effects on the cells as deduced from measurements of transepithelial resistance. Mutant strains of putative virulence factors phospholipase D and DIP0733 homologue CULC22_00609 generated in this study showed no influence on colonization under the experimental conditions tested. The data presented here indicate a high infectious potential of this emerging pathogen.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000121
2015-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/8/1582.html?itemId=/content/journal/micro/10.1099/mic.0.000121&mimeType=html&fmt=ahah

References

  1. Antunes C.A., Sanches dos Santos L., Hacker E., Köhler S., Bösl K., Ott L., de Luna M., Hirata R. Jr, Azevedo V.A., other authors. 2015; Characterization of DIP0733, a multi-functional virulence factor of Corynebacterium diphtheriae . Microbiology 161:639–647 [View Article][PubMed]
    [Google Scholar]
  2. Axelrod S., Oschkinat H., Enders J., Schlegel B., Brinkmann V., Kaufmann S.H., Haas A., Schaible U.E. 2008; Delay of phagosome maturation by a mycobacterial lipid is reversed by nitric oxide. Cell Microbiol 10:1530–1545 [View Article][PubMed]
    [Google Scholar]
  3. Bergin I.L., Chien C.C., Marini R.P., Fox J.G. 2000; Isolation and characterization of Corynebacterium ulcerans from cephalic implants in macaques. Comp Med 50:530–535[PubMed]
    [Google Scholar]
  4. Bonmarin I., Guiso N., Le Flèche-Matéos A., Patey O., Grimont Patrick A.D., Levy-Bruhl D. 2009; Diphtheria: a zoonotic disease in France?. Vaccine 27:4196–4200 [View Article][PubMed]
    [Google Scholar]
  5. Bostock A.D., Gilbert F.R., Lewis D., Smith D.C. 1984; Corynebacterium ulcerans infection associated with untreated milk. J Infect 9:286–288 [View Article][PubMed]
    [Google Scholar]
  6. Both L., Collins S., de Zoysa A., White J., Mandal S., Efstratiou A. 2015; Molecular and epidemiological review of toxigenic diphtheria infections in England between 2007 and 2013. J Clin Microbiol 53:567–572 [View Article][PubMed]
    [Google Scholar]
  7. Burkovski A. 2013; Cell envelope of corynebacteria: structure and influence on pathogenicity. ISRN Microbiol 2013:935736 [View Article][PubMed]
    [Google Scholar]
  8. Contzen M., Sting R., Blazey B., Rau J. 2011; Corynebacterium ulcerans from diseased wild boars. Zoonoses Public Health 58:479–488 [View Article][PubMed]
    [Google Scholar]
  9. Dias A.A., Silva F.C. Jr, Pereira G.A., Souza M.C., Camello T.C., Damasceno J.A., Pacheco L.G., Miyoshi A., Azevedo V.A., other authors. 2010; Corynebacterium ulcerans isolated from an asymptomatic dog kept in an animal shelter in the metropolitan area of Rio de Janeiro, Brazil. Vector Borne Zoonotic Dis 10:743–748 [View Article][PubMed]
    [Google Scholar]
  10. Dias A.A., Silva F.C. Jr, Santos L.S., Ribeiro-Carvalho M.M., Sabbadini P.S., Santos C.S., Filardy A.A., Myioshi A., Azevedo V.A., other authors. 2011; Strain-dependent arthritogenic potential of the zoonotic pathogen Corynebacterium ulcerans . Vet Microbiol 153:323–331 [View Article][PubMed]
    [Google Scholar]
  11. Eisenberg T., Mauder N., Contzen M., Rau J., Ewers C., Schlez K., Althoff G., Schauerte N., Geiger C., other authors. 2015; Outbreak with clonally related isolates of Corynebacterium ulcerans in a group of water rats. BMC Microbiol 15:42 [View Article][PubMed]
    [Google Scholar]
  12. Foster G., Patterson T., Howie F., Simpson V., Davison N., Efstratiou A., Lai S. 2002; Corynebacterium ulcerans in free-ranging otters. Vet Rec 150:524[PubMed]
    [Google Scholar]
  13. Gerlach R.G., Cláudio N., Rohde M., Jäckel D., Wagner C., Hensel M. 2008; Cooperation of Salmonella pathogenicity islands 1 and 4 is required to breach epithelial barriers. Cell Microbiol 10:2364–2376 [View Article][PubMed]
    [Google Scholar]
  14. Gey G.O., Coffman W.D., Kubicek M.T. 1952; Tissue culture studies of the proliferative capacity of cervical carcinoma and normal epithelium. Cancer Res 12:264–265
    [Google Scholar]
  15. Gilbert R., Stewart F.C. 1927; Corynebacterium ulcerans; a pathogenic microorganism resembling Corynebacterium diphtheriae . J Lab Clin Med 12:756–761
    [Google Scholar]
  16. Grant S.G., Jessee J., Bloom F.R., Hanahan D. 1990; Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A 87:4645–4649 [View Article][PubMed]
    [Google Scholar]
  17. Hart R.J. 1984; Corynebacterium ulcerans in humans and cattle in North Devon. J Hyg (Lond) 92:161–164 [View Article][PubMed]
    [Google Scholar]
  18. Hirai-Yuki A., Komiya T., Suzaki Y., Ami Y., Katsukawa C., Takahashi M., Yamamoto A., Yamada Y.K. 2013; Isolation and characterization of toxigenic Corynebacterium ulcerans from 2 closed colonies of cynomolgus macaques (Macaca fascicularis) in Japan. Comp Med 63:272–278[PubMed]
    [Google Scholar]
  19. Hirata R. Jr, Souza S.M., Rocha-de-Souza C.M., Andrade A.F., Monteiro-Leal L.H., Formiga L.C., Mattos-Guaraldi A.L. 2004; Patterns of adherence to HEp-2 cells and actin polymerisation by toxigenic Corynebacterium diphtheriae strains. Microb Pathog 36:125–130 [View Article][PubMed]
    [Google Scholar]
  20. Hogg R.A., Wessels J., Hart J., Efstratiou A., De Zoysa A., Mann G., Allen T., Pritchard G.C. 2009; Possible zoonotic transmission of toxigenic Corynebacterium ulcerans from companion animals in a human case of fatal diphtheria. Vet Rec 165:691–692[PubMed]
    [Google Scholar]
  21. Hommez J., Devriese L.A., Vaneechoutte M., Riegel P., Butaye P., Haesebrouck F. 1999; Identification of nonlipophilic corynebacteria isolated from dairy cows with mastitis. J Clin Microbiol 37:954–957[PubMed]
    [Google Scholar]
  22. Indrigo J., Hunter R.L. Jr, Actor J.K. 2003; Cord factor trehalose 6,6′-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages. Microbiology 149:2049–2059 [View Article][PubMed]
    [Google Scholar]
  23. Jakoby M., Ngouoto-Nkili C.-E., Burkovski A. 1999; Construction and application of new Corynebacterium glutamicum vectors. Biotechnol Tech 13:437–441 [View Article]
    [Google Scholar]
  24. Knoppová M., Phensaijai M., Veselý M., Zemanová M., Nesvera J., Pátek M. 2007; Plasmid vectors for testing in vivo promoter activities in Corynebacterium glutamicum Rhodococcus erythropolis . Curr Microbiol 55:234–239 [View Article][PubMed]
    [Google Scholar]
  25. Lucas E.A., Billington S.J., Carlson P., McGee D.J., Jost B.H. 2010; Phospholipase D promotes Arcanobacterium haemolyticum adhesion via lipid raft remodeling and host cell death following bacterial invasion. BMC Microbiol 10:270 [View Article][PubMed]
    [Google Scholar]
  26. Mattos-Guaraldi A.L., Sampaio J.L., Santos C.S., Pimenta F.P., Pereira G.A., Pacheco L.G., Miyoshi A., Azevedo V., Moreira L.O., other authors. 2008; First detection of Corynebacterium ulcerans producing a diphtheria-like toxin in a case of human with pulmonary infection in the Rio de Janeiro metropolitan area, Brazil. Mem Inst Oswaldo Cruz 103:396–400 [View Article][PubMed]
    [Google Scholar]
  27. Meinel D.M., Margos G., Konrad R., Krebs S., Blum H., Sing A. 2014; Next generation sequencing analysis of nine Corynebacterium ulcerans isolates reveals zoonotic transmission and a novel putative diphtheria toxin-encoding pathogenicity island. Genome Med 6:113 [View Article][PubMed]
    [Google Scholar]
  28. Meinel D.M., Konrad R., Berger A., König C., Schmidt-Wieland T., Hogardt M., Bischoff H., Ackermann N., Hörmansdorfer S., other authors. 2015; Zoonotic transmission of toxigenic Corynebacterium ulcerans strain, Germany, 2012. Emerg Infect Dis 21:356–358 [View Article][PubMed]
    [Google Scholar]
  29. Moreira L.O., Mattos-Guaraldi A.L., Andrade A.F. 2008; Novel lipoarabinomannan-like lipoglycan (CdiLAM) contributes to the adherence of Corynebacterium diphtheriae to epithelial cells. Arch Microbiol 190:521–530 [View Article][PubMed]
    [Google Scholar]
  30. Morris W.E., Uzal F.A., Cipolla A.L. 2005; Pyogranulomatous meningoencephalitis in a goat due to Corynebacterium ulcerans . Vet Rec 156:317–318 [View Article][PubMed]
    [Google Scholar]
  31. Olson M.E., Goemans I., Bolingbroke D., Lundberg S. 1988; Gangrenous dermatitis caused by Corynebacterium ulcerans in Richardson ground squirrels. J Am Vet Med Assoc 193:367–368[PubMed]
    [Google Scholar]
  32. Ott L., Burkovski A. 2014; Toxigenic corynebacteria: adhesion, invasion and host response. In Corynebacterium diphtheriae and Related Toxigenic Species pp. 143–170 Edited by Burkovski A. Dordrecht: Springer;
    [Google Scholar]
  33. Ott L., Höller M., Rheinlaender J., Schäffer T.E., Hensel M., Burkovski A. 2010; Strain-specific differences in pili formation and the interaction of Corynebacterium diphtheriae with host cells. BMC Microbiol 10:257 [View Article][PubMed]
    [Google Scholar]
  34. Ott L., McKenzie A., Baltazar M.T., Britting S., Bischof A., Burkovski A., Hoskisson P.A. 2012; Evaluation of invertebrate infection models for pathogenic corynebacteria. FEMS Immunol Med Microbiol 65:413–421 [View Article][PubMed]
    [Google Scholar]
  35. Ott L., Scholz B., Höller M., Hasselt K., Ensser A., Burkovski A. 2013; Induction of the NFκ-B signal transduction pathway in response to Corynebacterium diphtheriae infection. Microbiology 159:126–135 [View Article][PubMed]
    [Google Scholar]
  36. Pappenheimer A.M., Jr. 1977; Diphtheria toxin. Annu Rev Biochem 46:69–94 [View Article][PubMed]
    [Google Scholar]
  37. Peterson W.D. Jr, Stulberg C.S., Swanborg N.K., Robinson A.R. 1968; Glucose-6-phosphate dehydrogenase isoenzymes in human cell cultures determined by sucrose-agar gel and cellulose acetate zymograms. Proc Soc Exp Biol Med 128:772–776 [View Article][PubMed]
    [Google Scholar]
  38. Sambrook J., Fritsch E.F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  39. Sangal V., Hoskisson P.A. 2014; Infection of infectors. In Corynebacterium diphtheriae and Related Toxigenic Species pp. 67–81 Edited by Burkovski A. Dordrecht: Springer;
    [Google Scholar]
  40. Sangal V., Nieminen L., Weinhardt B., Raeside J., Tucker N.P., Florea C.D., Pollock K.G., Hoskisson P.A. 2014; Diphtheria-like disease caused by toxigenic Corynebacterium ulcerans strain. Emerg Infect Dis 20:1257–1258 [View Article][PubMed]
    [Google Scholar]
  41. Schäfer A., Tauch A., Jäger W., Kalinowski J., Thierbach G., Pühler A. 1994; Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum . Gene 145:69–73 [View Article][PubMed]
    [Google Scholar]
  42. Scherer W.F., Syverton J.T., Gey G.O. 1953; Studies on the propagation in vitro of poliomyelitis viruses. IV. Viral multiplication in a stable strain of human malignant epithelial cells (strain HeLa) derived from an epidermoid carcinoma of the cervix. J Exp Med 97:695–710 [View Article][PubMed]
    [Google Scholar]
  43. Schuhegger R., Schoerner C., Dlugaiczyk J., Lichtenfeld I., Trouillier A., Zeller-Peronnet V., Busch U., Berger A., Kugler R., other authors. 2009; Pigs as source for toxigenic Corynebacterium ulcerans . Emerg Infect Dis 15:1314–1315 [View Article][PubMed]
    [Google Scholar]
  44. Seto Y., Komiya T., Iwaki M., Kohda T., Mukamoto M., Takahashi M., Kozaki S. 2008; Properties of corynephage attachment site and molecular epidemiology of Corynebacterium ulcerans isolated from humans and animals in Japan. Jpn J Infect Dis 61:116–122[PubMed]
    [Google Scholar]
  45. Simpson-Louredo L., Ramos J.N., Peixoto R.S., Santos L.S., Antunes C.A., Ladeira E.M., Santos C.S., Vieira V.V., Bôas M.H., other authors. 2014; Corynebacterium ulcerans isolates from humans and dogs: fibrinogen, fibronectin and collagen-binding, antimicrobial and PFGE profiles. Antonie van Leeuwenhoek 105:343–352 [View Article][PubMed]
    [Google Scholar]
  46. Sydor T., von Bargen K., Hsu F.F., Huth G., Holst O., Wohlmann J., Becken U., Dykstra T., Söhl K., other authors. 2013; Diversion of phagosome trafficking by pathogenic Rhodococcus equi depends on mycolic acid chain length. Cell Microbiol 15:458–473 [View Article][PubMed]
    [Google Scholar]
  47. Sykes J.E., Mapes S., Lindsay L.L., Samitz E., Byrne B.A. 2010; Corynebacterium ulcerans bronchopneumonia in a dog. J Vet Intern Med 24:973–976 [View Article][PubMed]
    [Google Scholar]
  48. Tauch A., Sandbote J. 2014; The family Corynebacteriaceae . In The Prokaryotes pp. 239–277 Edited by Rosenberg E., DeLong E., Lory S., Stackebrandt E., Thompson F. Berlin: Springer;
    [Google Scholar]
  49. Tejedor M.T., Martin J.L., Lupiola P., Gutierrez C. 2000; Caseous lymphadenitis caused by Corynebacterium ulcerans in the dromedary camel. Can Vet J 41:126–127[PubMed]
    [Google Scholar]
  50. Trost E., Al-Dilaimi A., Papavasiliou P., Schneider J., Viehoever P., Burkovski A., Soares S.C., Almeida S.S., Dorella F.A., other authors. 2011; Comparative analysis of two complete Corynebacterium ulcerans genomes and detection of candidate virulence factors. BMC Genomics 12:383 [View Article][PubMed]
    [Google Scholar]
  51. Wagner K.S., White J.M., Crowcroft N.S., De Martin S., Mann G., Efstratiou A. 2010; Diphtheria in the United Kingdom, 1986–2008: the increasing role of Corynebacterium ulcerans . Epidemiol Infect 138:1519–1530 [View Article][PubMed]
    [Google Scholar]
  52. Zakikhany K., Efstratiou A. 2012; Diphtheria in Europe: current problems and new challenges. Future Microbiol 7:595–607 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000121
Loading
/content/journal/micro/10.1099/mic.0.000121
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error