Streptococcus suis DNase SsnA contributes to degradation of neutrophil extracellular traps (NETs) and evasion of NET-mediated antimicrobial activity

Microbiology (United Kingdom)

Volumn 160, Issue PART 2, 2014, Pages 385-395

  de Buhr, Nicole ^a   Neumann, Ariane ^a   Jerjomiceva, Natalja ^a   von Köckritz Blickwede, Maren ^a   Baums, Christoph G ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN SSNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL GROWTH; CONTROLLED STUDY; DEGRADATION; HOST RESISTANCE; HUMAN; HUMAN CELL; IN VITRO STUDY; MUTANT; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL EXTRACELLULAR TRAP; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; SSNA GENE; STREPTOCOCCUS SUIS; SUPERNATANT; SURVIVAL; SWINE;

ANIMALS; BACTERIAL PROTEINS; BIOPOLYMERS; CELLS, CULTURED; DEOXYRIBONUCLEASES; GENE KNOCKOUT TECHNIQUES; HOST-PATHOGEN INTERACTIONS; HUMANS; HYDROLYSIS; NEUTROPHILS; STREPTOCOCCUS SUIS; SWINE;

EID: 84893447723     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.072199-0     Document Type: Article

References (44)

1. Arends, J. P. & Zanen, H. C. (1988). Meningitis caused by Streptococcus suis in humans. Rev Infect Dis 10, 131-137.
2. Baums, C. G. & Valentin-Weigand, P. (2009). Surface-associated and secreted factors of Streptococcus suis in epidemiology, pathogenesis and vaccine development. Anim Health Res Rev 10, 65-83.
3. Baums, C. G., Kaim, U., Fulde, M., Ramachandran, G., Goethe, R. & Valentin-Weigand, P. (2006). Identification of a novel virulence determinant with serum opacification activity in Streptococcus suis. Infect Immun 74, 6154-6162.
4. Baums, C. G., Kock, C., Beineke, A., Bennecke, K., Goethe, R., Schröder, C., Waldmann, K. H. & Valentin-Weigand, P. (2009). Streptococcus suis bacterin and subunit vaccine immunogenicities and protective efficacies against serotypes 2 and 9. Clin Vaccine Immunol 16, 200-208.
5. Beineke, A., Bennecke, K., Neis, C., Schröder, C., Waldmann, K. H., Baumgärtner, W., Valentin-Weigand, P. & Baums, C. G. (2008). Comparative evaluation of virulence and pathology of Streptococcus suis serotypes 2 and 9 in experimentally infected growers. Vet Microbiol 128, 423-430.
6. Beiter, K., Wartha, F., Albiger, B., Normark, S., Zychlinsky, A. & Henriques-Normark, B. (2006). An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 16, 401-407.
7. Benga, L., Fulde, M., Neis, C., Goethe, R. & Valentin-Weigand, P. (2008). Polysaccharide capsule and suilysin contribute to extracellular survival of Streptococcus suis co-cultivated with primary porcine phagocytes. Vet Microbiol 132, 211-219.
8. Berends, E. T., Horswill, A. R., Haste, N. M., Monestier, M., Nizet, V. & von Köckritz-Blickwede, M. (2010). Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J Innate Immun 2, 576-586.
9. Bréa, D., Meurens, F., Dubois, A. V., Gaillard, J., Chevaleyre, C., Jourdan, M.-L., Winter, N., Arbeille, B., Si-Tahar, M. & other authors (2012). The pig as a model for investigating the role of neutrophil serine proteases in human inflammatory lung diseases. Biochem J 447, 363-370.
10. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y. & Zychlinsky, A. (2004). Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535.
11. Buchanan, J. T., Simpson, A. J., Aziz, R. K., Liu, G. Y., Kristian, S. A., Kotb, M., Feramisco, J. & Nizet, V. (2006). DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol 16, 396-400.
12. Chabot-Roy, G., Willson, P., Segura, M., Lacouture, S. & Gottschalk, M. (2006). Phagocytosis and killing of Streptococcus suis by porcine neutrophils. Microb Pathog 41, 21-32.
13. Chang, A., Khemlani, A., Kang, H. & Proft, T. (2011). Functional analysis of Streptococcus pyogenes nuclease A (SpnA), a novel group A streptococcal virulence factor. Mol Microbiol 79, 1629-1642.
14. Charland, N., Harel, J., Kobisch, M., Lacasse, S. & Gottschalk, M. (1998). Streptococcus suis serotype 2 mutants deficient in capsular expression. Microbiology 144, 325-332.
15. Chow, O. A., von Köckritz-Blickwede, M., Bright, A. T., Hensler, M. E., Zinkernagel, A. S., Cogen, A. L., Gallo, R. L., Monestier, M., Wang, Y. & other authors (2010). Statins enhance formation of phagocyte extracellular traps. Cell Host Microbe 8, 445-454.
16. Derré-Bobillot, A., Cortes-Perez, N. G., Yamamoto, Y., Kharrat, P., Couvé, E., Da Cunha, V., Decker, P., Boissier, M.-C., Escartin, F. & other authors (2013). Nuclease A (Gbs0661), an extracellular nuclease of Streptococcus agalactiae, attacks the neutrophil extracellular traps and is needed for full virulence. Mol Microbiol 89, 518-531.
17. Fittipaldi, N., Sekizaki, T., Takamatsu, D., Harel, J., Domínguez-Punaro, M. L., Von Aulock, S., Draing, C., Marois, C., Kobisch, M. & Gottschalk, M. (2008). D-alanylation of lipoteichoic acid contributes to the virulence of Streptococcus suis. Infect Immun 76, 3587-3594.
18. Fontaine, M. C., Perez-Casal, J. & Willson, P. J. (2004). Investigation of a novel DNase of Streptococcus suis serotype 2. Infect Immun 72, 774-781.
19. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V. & Zychlinsky, A. (2007). Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176, 231-241.
20. Gómez-Gascón, L., Luque, I., Olaya-Abril, A., Jiménez-Munguía, I., Orbegozo-Medina, R. A., Peralbo, E., Tarradas, C. & Rodríguez-Ortega, M. J. (2012). Exploring the pan-surfome of Streptococcus suis: looking for common protein antigens. J Proteomics 75, 5654-5666.
21. Gottschalk, M. (2011). Streptococcosis. In Diseases of Swine, pp. 841-855. Edited by J. J. Zimmerman, L. A. Kariker, A. Ramirez, K. J. Schwartz & G. W. Stevenson. Oxford, UK: Wiley-Blackwell.
22. Gottschalk, M., Xu, J., Calzas, C. & Segura, M. (2010). Streptococcus suis: a new emerging or an old neglected zoonotic pathogen? Future Microbiol 5, 371-391.
23. Lappann, M., Danhof, S., Guenther, F., Olivares-Florez, S., Mordhorst, I. L. & Vogel, U. (2013). In vitro resistance mechanisms of Neisseria meningitidis against neutrophil extracellular traps. Mol Microbiol 89, 433-449.
24. Lauth, X., von Köckritz-Blickwede, M., McNamara, C. W., Myskowski, S., Zinkernagel, A. S., Beall, B., Ghosh, P., Gallo, R. L. & Nizet, V. (2009). M1 protein allows Group A streptococcal survival in phagocyte extracellular traps through cathelicidin inhibition. J Innate Immun 1, 202-214.
25. Losman, M. J., Fasy, T. M., Novick, K. E. & Monestier, M. (1992). Monoclonal autoantibodies to subnucleosomes from a MRL/Mp(-)+/ +mouse. Oligoclonality of the antibody response and recognition of a determinant composed of histones H2A, H2B, and DNA. J Immunol 148, 1561-1569.
26. Lun, Z. R., Wang, Q. P., Chen, X. G., Li, A. X. & Zhu, X. Q. (2007). Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect Dis 7, 201-209.
27. Mai, N. T., Hoa, N. T., Nga, T. V., Linh, D., Chau, T. T., Sinh, D. X., Phu, N. H., Chuong, L. V., Diep, T. S. & other authors (2008). Streptococcus suis meningitis in adults in Vietnam. Clin Infect Dis 46, 659-667.
28. Midon, M., Schäfer, P., Pingoud, A., Ghosh, M., Moon, A. F., Cuneo, M. J., London, R. E. & Meiss, G. (2011). Mutational and biochemical analysis of the DNA-entry nuclease EndA from Streptococcus pneumoniae. Nucleic Acids Res 39, 623-634.
29. Pilsczek, F. H., Salina, D., Poon, K. K., Fahey, C., Yipp, B. G., Sibley, C. D., Robbins, S. M., Green, F. H., Surette, M. G. & other authors (2010). A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 185, 7413-7425.
30. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
31. Scapinello, S., Brooks, A. S., MacInnes, J. I., Hammermueller, J., Clark, M. E. & Caswell, J. L. (2011). Bactericidal activity of porcine neutrophil secretions. Vet Immunol Immunopathol 139, 113-118.
32. Seele, J., Singpiel, A., Spoerry, C., von Pawel-Rammingen, U., Valentin-Weigand, P. & Baums, C. G. (2013). Identification of a novel host-specific IgM protease in Streptococcus suis. J Bacteriol 195, 930-940.
33. Smith, H. E., Damman, M., van der Velde, J., Wagenaar, F., Wisselink, H. J., Stockhofe-Zurwieden, N. & Smits, M. A. (1999). Identification and characterization of the cps locus of Streptococcus suis serotype 2: the capsule protects against phagocytosis and is an important virulence factor. Infect Immun 67, 1750-1756.
34. Takamatsu, D., Osaki, M. & Sekizaki, T. (2001). Thermosensitive suicide vectors for gene replacement in Streptococcus suis. Plasmid 46, 140-148.
35. Tang, J., Wang, C., Feng, Y., Yang, W., Song, H., Chen, Z., Yu, H., Pan, X., Zhou, X. & other authors (2006). Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med 3, e151.
36. Vasconcelos, D., Middleton, D. M. & Chirino-Trejo, J. M. (1994). Lesions caused by natural infection with Streptococcus suis type 9 in weaned pigs. J Vet Diagn Invest 6, 335-341.
37. von Köckritz-Blickwede, M. & Nizet, V. (2009). Innate immunity turned inside-out: antimicrobial defense by phagocyte extracellular traps. J Mol Med (Berl) 87, 775-783.
38. von Köckritz-Blickwede, M., Chow, O., Ghochani, M. & Nizet, V. (2010). Visualization and functional evaluation of phagocyte extracellular traps. In Methods in Microbiology, pp. 138-160. Edited by S. H. Kaufmann & D. Kabelitz. London, UK: Academic Press.
39. Wangkaew, S., Chaiwarith, R., Tharavichitkul, P. & Supparatpinyo, K. (2006). Streptococcus suis infection: a series of 41 cases from Chiang Mai University Hospital. J Infect 52, 455-460.
40. Wartha, F., Beiter, K., Albiger, B., Fernebro, J., Zychlinsky, A., Normark, S. & Henriques-Normark, B. (2007). Capsule and Dalanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell Microbiol 9, 1162-1171.
41. Wei, Z., Li, R., Zhang, A., He, H., Hua, Y., Xia, J., Cai, X., Chen, H. & Jin, M. (2009). Characterization of Streptococcus suis isolates from the diseased pigs in China between 2003 and 2007. Vet Microbiol 137, 196-201.
42. Willenborg, J., Fulde, M., de Greeff, A., Rohde, M., Smith, H. E., Valentin-Weigand, P. & Goethe, R. (2011). Role of glucose and CcpA in capsule expression and virulence of Streptococcus suis. Microbiology 157, 572-582.
43. Williams, A. E. & Blakemore, W. F. (1990). Pathogenesis of meningitis caused by Streptococcus suis type 2. J Infect Dis 162, 474-481.
44. Wisselink, H. J., Smith, H. E., Stockhofe-Zurwieden, N., Peperkamp, K. & Vecht, U. (2000). Distribution of capsular types and production of muramidase-released protein (MRP) and extracellular factor (EF) of Streptococcus suis strains isolated from diseased pigs in seven European countries. Vet Microbiol 74, 237-248.