A virulence-associated filamentous bacteriophage of Neisseria meningitidis increases host-cell colonisation

PLoS Pathogens

Volumn 13, Issue 7, 2017, Pages

  Bille, Emmanuelle ^a,b,c   Meyer, Julie ^a,b   Jamet, Anne ^a,b,c   Euphrasie, Daniel ^a,b   Barnier, Jean Philippe ^a,b,c   Brissac, Terry ^a,b,e   Larsen, Anna ^a,b   Pelissier, Philippe ^d   Nassif, Xavier ^a,b,c  

^a CNRS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d SAINT JOSEPH HOSPITAL   (France)

^e University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEFEROXAMINE; MONOCLONAL ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL SKIN DISEASE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BACTERIUM PILUS; BIOMASS; CONTROLLED STUDY; ELECTRON MICROSCOPY; EPITHELIAL CELL LINE; FEMALE; HOST CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOFLUORESCENCE TEST; IMMUNOGOLD LABELING; LUNG CANCER CELL LINE; MENINGOCOCCOSIS; MOUSE; NASOPHARYNX; NEISSERIA MENINGITIDIS; NONHUMAN; PROPHAGE; REAL TIME POLYMERASE CHAIN REACTION; SEPTICEMIA; SEVERE COMBINED IMMUNODEFICIENCY; SURVIVAL; WESTERN BLOTTING; ANIMAL; BACTERIUM ADHERENCE; EPITHELIUM CELL; FIMBRIA; GROWTH, DEVELOPMENT AND AGING; INOVIRUS; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; SCID MOUSE; VIROLOGY; VIRULENCE;

ANIMALS; BACTERIAL ADHESION; EPITHELIAL CELLS; FEMALE; FIMBRIAE, BACTERIAL; HUMANS; INOVIRUS; MENINGOCOCCAL INFECTIONS; MICE; MICE, SCID; NASOPHARYNX; NEISSERIA MENINGITIDIS; PROPHAGES; VIRULENCE;

EID: 85026871208     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006495     Document Type: Article

References (42)

1. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A. 1998;95(6):3140–5. 9501229;
2. Perkins-Balding D, Ratliff-Griffin M, Stojiljkovic I, Iron transport systems in Neisseria meningitidis. Microbiol Mol Biol Rev. 2004;68(1):154–71. doi: 10.1128/MMBR.68.1.154-171.2004 15007100;
3. Rosenstein NE, Perkins BA, Stephens DS, Popovic T, Hughes JM, Meningococcal disease. The New England journal of medicine. 2001;344(18):1378–88. doi: 10.1056/NEJM200105033441807 11333996.
4. Hill DJ, Griffiths NJ, Borodina E, Virji M, Cellular and molecular biology of Neisseria meningitidis colonization and invasive disease. Clinical science. 2010;118(9):547–64. doi: 10.1042/CS20090513 20132098;
5. Bille E, Zahar JR, Perrin A, Morelle S, Kriz P, Jolley KA, et al. A chromosomally integrated bacteriophage in invasive meningococci. J Exp Med. 2005;201(12):1905–13. doi: 10.1084/jem.20050112 15967821;
6. Bille E, Ure R, Gray SJ, Kaczmarski EB, McCarthy ND, Nassif X, et al. Association of a bacteriophage with meningococcal disease in young adults. PloS one. 2008;3(12):e3885. doi: 10.1371/journal.pone.0003885 19065260;
7. Meyer J, Brissac T, Frapy E, Omer H, Euphrasie D, Bonavita A, et al. Characterization of MDAPhi, a temperate filamentous bacteriophage of Neisseria meningitidis. Microbiology. 2015. doi: 10.1099/mic.0.000215 26602366.
8. Salmond GP, Fineran PC, A century of the phage: past, present and future. Nature reviews Microbiology. 2015;13(12):777–86. doi: 10.1038/nrmicro3564 26548913.
9. Tinsley CR, Bille E, Nassif X, Bacteriophages and pathogenicity: more than just providing a toxin?Microbes and infection / Institut Pasteur. 2006;8(5):1365–71. doi: 10.1016/j.micinf.2005.12.013 16698301.
10. Mai-Prochnow A, Hui JG, Kjelleberg S, Rakonjac J, McDougald D, Rice SA, 'Big things in small packages: the genetics of filamentous phage and effects on fitness of their host'. FEMS Microbiol Rev. 2015;39(4):465–87. doi: 10.1093/femsre/fuu007 25670735.
11. Rice SA, Tan CH, Mikkelsen PJ, Kung V, Woo J, Tay M, et al. The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. The ISME journal. 2009;3(3):271–82. doi: 10.1038/ismej.2008.109 19005496;
12. Secor PR, Sweere JM, Michaels LA, Malkovskiy AV, Lazzareschi D, Katznelson E, et al. Filamentous Bacteriophage Promote Biofilm Assembly and Function. Cell Host Microbe. 2015;18(5):549–59. doi: 10.1016/j.chom.2015.10.013 26567508;
13. Secor PR, Michaels LA, Smigiel KS, Rohani MG, Jennings LK, Hisert KB, et al. Filamentous Bacteriophage Produced by Pseudomonas aeruginosa Alters the Inflammatory Response and Promotes Noninvasive Infection In Vivo. Infect Immun. 2017;85(1). doi: 10.1128/IAI.00648-16 27795361.
14. Join-Lambert O, Lecuyer H, Miller F, Lelievre L, Jamet A, Furio L, et al. Meningococcal interaction to microvasculature triggers the tissular lesions of purpura fulminans. J Infect Dis. 2013;208(10):1590–7. doi: 10.1093/infdis/jit301 23840047.
15. Muller MG, Moe NE, Richards PQ, Moe GR, Resistance of Neisseria meningitidis to human serum depends on T and B cell stimulating protein B. Infect Immun. 2015;83(4):1257–64. doi: 10.1128/IAI.03134-14 25583528;
16. Rusznak C, Devalia JL, Lozewicz S, Davies RJ, The assessment of nasal mucociliary clearance and the effect of drugs. Respiratory medicine. 1994;88(2):89–101. 8146420.
17. Jamet A, Euphrasie D, Martin P, Nassif X, Identification of genes involved in Neisseria meningitidis colonization. Infect Immun. 2013;81(9):3375–81. doi: 10.1128/IAI.00421-13 23817612;
18. Lecuyer H, Nassif X, Coureuil M, Two strikingly different signaling pathways are induced by meningococcal type IV pili on endothelial and epithelial cells. Infect Immun. 2012;80(1):175–86. doi: 10.1128/IAI.05837-11 22064711;
19. Carrolo M, Frias MJ, Pinto FR, Melo-Cristino J, Ramirez M, Prophage spontaneous activation promotes DNA release enhancing biofilm formation in Streptococcus pneumoniae. PloS one. 2010;5(12):e15678. doi: 10.1371/journal.pone.0015678 21187931;
20. Lappann M, Claus H, van Alen T, Harmsen M, Elias J, Molin S, et al. A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. Molecular microbiology. 2010;75(6):1355–71. doi: 10.1111/j.1365-2958.2010.07054.x 20180907.
21. Nassif X, Marceau M, Pujol C, Pron B, Beretti JL, Taha MK, Type-4 pili and meningococcal adhesiveness. Gene. 1997;192(1):149–53. 9224885.
22. Wolter N, Tempia S, Cohen C, Madhi SA, Venter M, Moyes J, et al. High nasopharyngeal pneumococcal density, increased by viral coinfection, is associated with invasive pneumococcal pneumonia. J Infect Dis. 2014;210(10):1649–57. doi: 10.1093/infdis/jiu326 24907383.
23. Deghmane AE, Giorgini D, Larribe M, Alonso JM, Taha MK, Down-regulation of pili and capsule of Neisseria meningitidis upon contact with epithelial cells is mediated by CrgA regulatory protein. Molecular microbiology. 2002;43(6):1555–64. 11952904.
24. Pujol C, Eugene E, Marceau M, Nassif X, The meningococcal PilT protein is required for induction of intimate attachment to epithelial cells following pilus-mediated adhesion. Proc Natl Acad Sci U S A. 1999;96(7):4017–22. 10097155;
25. Oldewurtel ER, Kouzel N, Dewenter L, Henseler K, Maier B, Differential interaction forces govern bacterial sorting in early biofilms. Elife. 2015;4. doi: 10.7554/eLife.10811 26402455;
26. Coureuil M, Lecuyer H, Scott MG, Boularan C, Enslen H, Soyer M, et al. Meningococcus Hijacks a beta2-adrenoceptor/beta-Arrestin pathway to cross brain microvasculature endothelium. Cell. 2010;143(7):1149–60. doi: 10.1016/j.cell.2010.11.035 21183077.
27. Mikaty G, Soyer M, Mairey E, Henry N, Dyer D, Forest KT, et al. Extracellular bacterial pathogen induces host cell surface reorganization to resist shear stress. PLoS pathogens. 2009;5(2):e1000314. doi: 10.1371/journal.ppat.1000314 19247442;
28. Sigurlasdottir S, Engman J, Eriksson OS, Saroj SD, Zguna N, Lloris-Garcera P, et al. Host cell-derived lactate functions as an effector molecule in Neisseria meningitidis microcolony dispersal. PLoS pathogens. 2017;13(4):e1006251. doi: 10.1371/journal.ppat.1006251 28384279;
29. Engman J, Negrea A, Sigurlasdottir S, Georg M, Eriksson J, Eriksson OS, et al. Neisseria meningitidis Polynucleotide Phosphorylase Affects Aggregation, Adhesion, and Virulence. Infect Immun. 2016;84(5):1501–13. doi: 10.1128/IAI.01463-15 26930706;
30. Achtman M, Neibert M, Crowe BA, Strittmatter W, Kusecek B, Weyse E, et al. Purification and characterization of eight class 5 outer membrane protein variants from a clone of Neisseria meningitidis serogroup A. J Exp Med. 1988;168(2):507–25. 2457646.
31. Omer H, Rose G, Jolley KA, Frapy E, Zahar JR, Maiden MC, et al. Genotypic and phenotypic modifications of Neisseria meningitidis after an accidental human passage. PloS one. 2011;6(2):e17145. doi: 10.1371/journal.pone.0017145 21386889;
32. Kellogg DS, Jr.Cohen IR, Norins LC, Schroeter AL, Reising G, Neisseria gonorrhoeae. II. Colonial variation and pathogenicity during 35 months in vitro. J Bacteriol. 1968;96(3):596–605. 4979098.
33. Muller MG, Ing JY, Cheng MK, Flitter BA, Moe GR, Identification of a phage-encoded Ig-binding protein from invasive Neisseria meningitidis. Journal of immunology. 2013;191(6):3287–96. doi: 10.4049/jimmunol.1301153 23926326;
34. Sanchez-Corral P, Anton LC, Alcolea JM, Marques G, Sanchez A, Vivanco F, Separation of active and inactive forms of the third component of human complement, C3, by fast protein liquid chromatography (FPLC). Journal of immunological methods. 1989;122(1):105–13. 2760472.
35. Nassif X, Lowy J, Stenberg P, O'Gaora P, Ganji A, So M, Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Molecular microbiology. 1993;8(4):719–25. 8332064.
36. Mairey E, Genovesio A, Donnadieu E, Bernard C, Jaubert F, Pinard E, et al. Cerebral microcirculation shear stress levels determine Neisseria meningitidis attachment sites along the blood-brain barrier. The Journal of experimental medicine. 2006;203(8):1939–50. doi: 10.1084/jem.20060482 16864659;
37. Geoffroy MC, Floquet S, Metais A, Nassif X, Pelicic V, Large-scale analysis of the meningococcus genome by gene disruption: resistance to complement-mediated lysis. Genome research. 2003;13(3):391–8. doi: 10.1101/gr.664303 12618369;
38. Helaine S, Carbonnelle E, Prouvensier L, Beretti JL, Nassif X, Pelicic V, PilX, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Molecular microbiology. 2005;55(1):65–77. doi: 10.1111/j.1365-2958.2004.04372.x 15612917.
39. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK, et al. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology. 2000;146 (Pt 10):2395–407. doi: 10.1099/00221287-146-10-2395 11021916.
40. Pujol C, Eugene E, de Saint Martin L, Nassif X, Interaction of Neisseria meningitidis with a polarized monolayer of epithelial cells. Infect Immun. 1997;65(11):4836–42. 9353073;
41. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW, Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Analytical biochemistry. 2000;285(2):194–204. doi: 10.1006/abio.2000.4753 11017702.
42. Sambrook J, Fritsch EF, T. M. Purification of bacteriophage lambda. Molecular Cloning A Laboratory Manual: Cold; 1989.