The genotoxin colibactin is a determinant of virulence in Escherichia coli K1 experimental neonatal systemic infection

Infection and Immunity

Volumn 83, Issue 9, 2015, Pages 3704-3711

  McCarthy, Alex J ^a   Martin, Patricia ^b,c,d,e   Cloup, Emilie ^b,c,d,e   Stabler, Richard A ^f   Oswald, Eric ^b,c,d,e,g   Taylor, Peter W ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b INSERM   (France)

^c CEMAGREF   (France)

^d France   (France)

^e UNIVERSITÉ PAUL SABATIER   (France)

^f LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^g CHU PURPAN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; COLIBACTIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; PEPTIDE; POLYKETIDE;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; ENZYME SPECIFICITY; ESCHERICHIA COLI; GASTROINTESTINAL TRACT; GENE FUNCTION; GENE SEQUENCE; GENOMIC INSTABILITY; GENOTOXICITY; GENOTOXICITY ASSAY; IMMUNOHISTOCHEMISTRY; NEWBORN INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY ISLAND; PHENOTYPE; PLASMID; PRIORITY JOURNAL; SEPTICEMIA; SINGLE NUCLEOTIDE POLYMORPHISM; VIRULENCE; ANIMAL; DISEASE MODEL; ESCHERICHIA COLI INFECTION; GENETICS; GENOMIC ISLAND; METABOLISM; MOLECULAR GENETICS; NEWBORN; PATHOGENICITY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RAT; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BASE SEQUENCE; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GENOMIC ISLANDS; IMMUNOHISTOCHEMISTRY; MOLECULAR SEQUENCE DATA; PEPTIDES; POLYKETIDES; POLYMERASE CHAIN REACTION; RATS; RATS, WISTAR; VIRULENCE;

EID: 84939505955     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00716-15     Document Type: Article

References (35)

1. Escobar-Páramo P, Grenet K, Le Menac'h A, Rode L, Salgado E, Amorin C, Gouriou S, Picard B, Rahimy MC, Andremont A, Denamur E, Ruimy R. 2004. Large-scale population structure of human commensal Escherichia coli isolates. Appl Environ Microbiol 70:5698-5700. http://dx.doi.org/10.1128/AEM.70.9.5698-5700.2004.
2. Russo TA, Johnson JR. 2003. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 5:449-456. http://dx.doi.org/10.1016/S1286-4579(03)00049-2.
3. Tenaillon O, Skurnik D, Picard B, Denamur E. 2010. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8:207-217. http://dx.doi.org/10.1038/nrmicro2298.
4. Schmidt H, Hensel M. 2004. Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17:14-56. http://dx.doi.org/10.1128/CMR.17.1.14-56.2004.
5. Nougayrède JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E. 2006. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313:848-851. http://dx.doi.org/10.1126/science.1127059.
6. Johnson JR, Johnston B, Kuskowski MA, Nougayrede JP, Oswald E. 2008. Molecular epidemiology and phylogenetic distribution of the Escherichia coli pks genomic island. J Clin Microbiol 46:3906-3911. http://dx.doi.org/10.1128/JCM.00949-08.
7. Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrède JP. 2010. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci U S A 107:11537-11542. http://dx.doi.org/10.1073/pnas.1001261107.
8. Marcq I, Martin P, Payros D, Cuevas-Ramos G, Boury M, Watrin C, Nougayrède JP, Olier M, Oswald E. 2014. The genotoxin colibactin exacerbates lymphopenia and decreases survival rate in mice infected with septicemic Escherichia coli. J Infect Dis 210:285-294. http://dx.doi.org/10.1093/infdis/jiu071.
9. Nowrouzian FL, Oswald E. 2012. Escherichia coli strains with the capacity for long-term persistence in the bowel microbiota carry the potentially genotoxic pks island. Microb Pathog 53:180-182. http://dx.doi.org/10.1016/j.micpath.2012.05.011.
10. Dubois D, Baron O, Cougnoux A, Delmas J, Pradel N, Boury M, Bouchon B, Bringer MA, Nougayrède JP, Oswald E, Bonnet R. 2011. ClbP is a prototype of a peptidase subgroup involved in biosynthesis of nonribosomal peptides. J Biol Chem 286:35562-35570. http://dx.doi.org/10.1074/jbc.M111.221960.
11. Brotherton CA, Balskus EP. 2013. A prodrug resistance mechanism is involved in colibactin biosynthesis and cytotoxicity. J Am Chem Soc 135:3359-3362. http://dx.doi.org/10.1021/ja312154m.
12. Martin P, Marcq I, Magistro G, Penary M, Garcie C, Payros D, Boury M, Olier M, Nougayrède JP, Audebert M, Chalut C, Schubert S, Oswald E. 2013. Interplay between siderophores and colibactin genotoxin biosynthetic pathways in Escherichia coli. PLoS Pathog 9:e1003437. http://dx.doi.org/10.1371/journal.ppat.1003437.
13. Johnson JR, Oswald E, O'Bryan TT, Kuskowski MA, Spanjaard L. 2002. Phylogenetic distribution of virulence-associated genes among Escherichia coli isolates associated with neonatal bacterial meningitis in the Netherlands. J Infect Dis 185:774-784. http://dx.doi.org/10.1086/339343.
14. Polin RA, Harris MC. 2001. Neonatal bacterial meningitis. Semin Neonatol 6:157-172. http://dx.doi.org/10.1053/siny.2001.0045.
15. Simonsen KA, Anderson-Berry AL, Delair SF, Davies HD. 2014. Earlyonset neonatal sepsis. Clin Microbiol Rev 27:21-47. http://dx.doi.org/10.1128/CMR.00031-13.
16. Sarff LD, McCracken GH, Schiffer MS, Glode MP, Robbins JB, Ørskov I, Ørskov F. 1975. Epidemiology of Escherichia coli K1 in healthy and diseased newborns. Lancet i:1099-1104.
17. Glode MP, Sutton A, Moxon ER, Robbins JB. 1977. Pathogenesis of neonatal Escherichia coli meningitis: induction of bacteremia and meningitis in infant rats fed E. coli K1. Infect Immun 16:75-80.
18. Pluschke G, Mercer A, Kusećek B, Pohl A, Achtman M. 1983. Induction of bacteremia in newborn rats by Escherichia coli K1 is correlated with only certain O (lipopolysaccharide) antigen types. Infect Immun 39:599-608.
19. Zelmer A, Bowen M, Jokilammi A, Finne J, Luzio JP, Taylor PW. 2008. Differential expression of the polysialyl capsule during blood-to-brain transit of neuropathogenic Escherichia coli K1. Microbiology 154:2522-2532. http://dx.doi.org/10.1099/mic.0.2008/017988-0.
20. Zelmer A, Martin M, Gundogdu O, Birchenough G, Lever R, Wren BW, Luzio JP, Taylor PW. 2010. Administration of capsule-selective endosialidase E minimizes changes in organ gene expression induced by experimental systemic infection with Escherichia coli K1. Microbiology 156:2205-2215. http://dx.doi.org/10.1099/mic.0.036145-0.
21. Birchenough GMH, Johannson MEV, Stabler RA, Dalgakiran F, Hansson GC, Wren BW, Luzio JP, Taylor PW. 2013. Altered innate defenses in the neonatal gastrointestinal tract in response to colonization by neuropathogenic Escherichia coli. Infect Immun 81:3264-3275. http://dx.doi.org/10.1128/IAI.00268-13.
22. Achtman M, Mercer A, Kusećek B, Pohl A, Heuzenroeder M, Aaronson W, Sutton A, Silver RP. 1983. Six widespread bacterial clones among Escherichia coli K1 isolates. Infect Immun 39:315-335.
23. Mushtaq N, Redpath MB, Luzio JP, Taylor PW. 2004. Prevention and cure of systemic Escherichia coli K1 infection by modification of the bacterial phenotype. Antimicrob Agents Chemother 48:1503-1508. http://dx.doi.org/10.1128/AAC.48.5.1503-1508.2004.
24. Gross RJ, Cheasty T, Rowe B. 1977. Isolation of bacteriophages specific for the K1 polysaccharide antigen of Escherichia coli. J Clin Microbiol 6:548-550.
25. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
26. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120. http://dx.doi.org/10.1093/bioinformatics/btu170.
27. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the Artemis Comparison Tool. Bioinformatics 21:3422-3423. http://dx.doi.org/10.1093/bioinformatics/bti553.
28. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. http://dx.doi.org/10.1093/bioinformatics/btp324.
29. Olier M, Marcq I, Salvador-Cartier C, Secher T, Dobrindt U, Boury M, Bacquié V, Pénary M, Gaultier E, Nougayrède JP, Fioramonti J, Oswald E. 2012. Genotoxicity of Escherichia coli Nissle 1917 strain cannot be dissociated from its probiotic activity. Gut Microbes 3:501-509. http://dx.doi.org/10.4161/gmic.21737.
30. Dalgakiran F, Witcomb L, McCarthy A, Birchenough GMH, Taylor PW. 2014. Non-invasive model of neuropathogenic Escherichia coli infection in the neonatal rat. J Vis Exp 92:e52018.
31. Mushtaq N, Redpath MB, Luzio JP, Taylor PW. 2005. Treatment of experimental Escherichia coli infection with recombinant bacteriophage-derived capsule depolymerase. J Antimicrob Chemother 56:160-165. http://dx.doi.org/10.1093/jac/dki177.
32. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858-5868. http://dx.doi.org/10.1074/jbc.273.10.5858.
33. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. 2008. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 105:15064-15069. http://dx.doi.org/10.1073/pnas.0803124105.
34. Secher T, Samba-Louaka A, Oswald E, Nougayrède JP. 2013. Escherichia coli producing colibactin triggers premature and transmissible senescence in mammalian cells. PLoS One 8:e77157. http://dx.doi.org/10.1371/journal.pone.0077157.
35. Secher T, Payros D, Brehin C, Boury M, Watrin C, Gillet M, Bernard-Cadenat I, Menard S, Theodorou V, Saoudi A, Olier M, Oswald E. 2015. Oral tolerance failure upon neonatal gut colonization with Escherichia coli producing the genotoxin colibactin. Infect Immun 83:2420-2429. http://dx.doi.org/10.1128/IAI.00064-15.