Characterization of a virulence-associated and cell-wall-located DNase of Streptococcus pyogenes

Microbiology

Volumn 156, Issue 1, 2010, Pages 184-190

  Hasegawa, Tadao ^a   Minami, Masaaki ^a   Okamoto, Akira ^b   Tatsuno, Ichiro ^a   Isaka, Masanori ^a   Ohta, Michio ^b  

^a NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; DEOXYRIBONUCLEASE; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; MAGNESIUM ION; MEMBRANE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CELL WALL; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIUM CULTURE; CELL LYSATE; CONTROLLED STUDY; DISEASE MODEL; ENZYME ACTIVITY; ESCHERICHIA COLI; MOUSE; NONHUMAN; PEPTIDE MAPPING; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; SEQUENCE HOMOLOGY; SEROTYPE; STRAIN DIFFERENCE; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SUIS; SUPERNATANT; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; BACTERIAL PROTEINS; CELL WALL; DEOXYRIBONUCLEASES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GENE KNOCKOUT TECHNIQUES; MICE; MICE, INBRED ICR; PEPTIDE MAPPING; PROTEOMICS; RECOMBINANT PROTEINS; STREPTOCOCCUS PYOGENES; VIRULENCE;

ESCHERICHIA COLI; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SUIS;

EID: 76849115257     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.031955-0     Document Type: Article

References (45)

1. Ashbaugh, C. D., Warren, H. B., Carey, V. J. & Wessels, M. R. (1998). Molecular analysis of the role of the group A streptococcal cysteine protease, hyaluronic acid capsule, and M protein in a murine model of human invasive soft-tissue infection. J Clin Invest 102, 550-560.
2. Aziz, R. K. & Kotb, M. (2008). Rise and persistence of global M1T1 clone of Streptococcus pyogenes. Emerg Infect Dis 14, 1511-1517.
3. Aziz, R. K., Ismail, S. A., Park, H. W. & Kotb, M. (2004). Post-proteomic identification of a novel phage-encoded streptodornase, Sda1, in invasive M1T1 Streptococcus pyogenes. Mol Microbiol 54, 184-197.
4. Banks, D. J., Porcella, S. F., Barbian, K. D., Beres, S. B., Philips, L. E., Voyich, J. M., DeLeo, F. R., Martin, J. M., Somerville, G. A. & Musser, J. M. (2004). Progress toward characterization of the group A Streptococcus metagenome: complete genome sequence of a macrolide-resistant serotype M6 strain. J Infect Dis 190, 727-738.
5. Beres, S. B., Sylva, G. L., Barbian, K. D., Lei, B., Hoff, J. S., Mammarella, N. D., Liu, M. Y., Smoot, J. C., Porcella, S. F. & other authors (2002). Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci U S A 99, 10078-10083.
6. Beres, S. B., Richter, E. W., Nagiec, M. J., Sumby, P., Porcella, S. F., DeLeo, F. R. & Musser, J. M. (2006). Molecular genetic anatomy of inter- and intraserotype variation in the human bacterial pathogen group A Streptococcus. Proc Natl Acad Sci U S A 103, 7059-7064.
7. Beres, S. B., Sesso, R., Pinto, S. W., Hoe, N. P., Porcella, S. F., Deleo, F. R. & Musser, J. M. (2008). Genome sequence of a Lancefield group C Streptococcus zooepidemicus strain causing epidemic nephritis: new information about an old disease. PLoS One 3, e3026.
8. 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.
9. 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.
10. Chen, C., Tang, J., Dong, W., Wang, C., Feng, Y., Wang, J., Zheng, F., Pan, X., Liu, D. & other authors (2007). A glimpse of streptococcal toxic shock syndrome from comparative genomics of S. suis 2 Chinese isolates. PLoS One 2, e315.
11. Cone, L. A., Woodard, D. R., Schlievert, P. M. & Tomory, G. S. (1987). Clinical and bacteriologic observations of a toxic shock-like syndrome due to Streptococcus pyogenes. N Engl J Med 317, 146-149.
12. Cunningham, M. W. (2000). Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13, 470-511.
13. + group A streptococci are phagocytized and killed in whole blood by C5a-activated polymorphonuclear leukocytes. Infect Immun 70, 350-359.
14. 2+-dependent endonucleases. Trends Biochem Sci 25, 272-273.
15. Emanuelsson, O., Brunak, S., von Heijne, G. & Nielsen, H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2, 953-971.
16. Ferreira, B. T., Benchetrit, L. C., De Castro, A. C., Batista, T. G. & Barrucand, L. (1992). Extracellular deoxyribonucleases of streptococci: a comparison of their occurrence and levels of production among beta-hemolytic strains of various serological groups. Zentralbl Bakteriol 277, 493-503.
17. Ferretti, J. J., McShan, W. M., Ajdic, D., Savic, D. J., Savic, G., Lyon, K., Primeaux, C., Sezate, S., Suvorov, A. N. & other authors (2001). Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci U S A 98, 4658-4663.
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. Green, N. M., Zhang, S., Porcella, S. F., Nagiec, M. J., Barbian, K. D., Beres, S. B., LeFebvre, R. B. & Musser, J. M. (2005). Genome sequence of a serotype M28 strain of group A streptococcus: potential new insights into puerperal sepsis and bacterial disease specificity. J Infect Dis 192, 760-770.
20. Hasegawa, T., Torii, K., Hashikawa, S., Iinuma, Y. & Ohta, M. (2002a). Cloning and characterization of two novel DNases from Streptococcus pyogenes. Arch Microbiol 177, 451-456.
21. Hasegawa, T., Torii, K., Hashikawa, S., Iinuma, Y. & Ohta, M. (2002b). Cloning and characterization of the deoxyribonuclease sda gene from Streptococcus pyogenes. Curr Microbiol 45, 13-17.
22. Hauser, A. R., Stevens, D. L., Kaplan, E. L. & Schlievert, P. M. (1991). Molecular analysis of pyrogenic exotoxins from Streptococcus pyogenes isolates associated with toxic shock-like syndrome. J Clin Microbiol 29, 1562-1567.
23. Herwald, H., Cramer, H., Morgelin, M., Russell, W., Sollenberg, U., Norrby-Teglund, A., Flodgaard, H., Lindbom, L. & Bjorck, L. (2004). M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 116, 367-379.
24. Holden, M. T., Scott, A., Cherevach, I., Chillingworth, T., Churcher, C., Cronin, A., Dowd, L., Feltwell, T., Hamlin, N. & other authors (2007). Complete genome of acute rheumatic fever-associated serotype M5 Streptococcus pyogenes strain Manfredo. J Bacteriol 189, 1473-1477.
25. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M. & other authors (1996). Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3, 109-136.
26. Lancefield, R. C. (1957). Differentiation of group A streptococci with a common R antigen into three serological types, with special reference to the bactericidal test. J Exp Med 106, 525-544.
27. Lukomski, S., Hoe, N. P., Abdi, I., Rurangirwa, J., Kordari, P., Liu, M., Dou, S. J., Adams, G. G. & Musser, J. M. (2000). Nonpolar inactivation of the hypervariable streptococcal inhibitor of complement gene (sic) in serotype M1 Streptococcus pyogenes significantly decreases mouse mucosal colonization. Infect Immun 68, 535-542.
28. McCarty, M. (1949). The inhibition of streptococcal desoxyribonuclease by rabbit and human antisera. J Exp Med 90, 543-553.
29. McShan, W. M., Ferretti, J. J., Karasawa, T., Suvorov, A. N., Lin, S., Qin, B., Jia, H., Kenton, S., Najar, F. & other authors (2008). Genome sequence of a nephritogenic and highly transformable M49 strain of Streptococcus pyogenes. J Bacteriol 190, 7773-7785.
30. Mitaku, S., Hirokawa, T. & Tsuji, T. (2002). Amphiphilicity index of polar amino acids as an aid in the characterization of amino acid preference at membrane-water interfaces. Bioinformatics 18, 608-616.
31. Miyakawa, Y., Yamada, T., Shitara, M. & Fukazawa, Y. (1985). Electrophoretic patterns of extracellular deoxyribonuclease (DNase) and their correlation with T-type in group A streptococci. Microbiol Immunol 29, 195-204.
32. Nakagawa, I., Kurokawa, K., Yamashita, A., Nakata, M., Tomiyasu, Y., Okahashi, N., Kawabata, S., Yamazaki, K., Shiba, T. & other authors (2003). Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution. Genome Res 13, 1042-1055.
33. Nakamura, T., Hasegawa, T., Torii, K., Hasegawa, Y., Shimokata, K. & Ohta, M. (2004). Two-dimensional gel electrophoresis analysis of the abundance of virulent exoproteins of group A streptococcus caused by environmental changes. Arch Microbiol 181, 74-81.
34. Okada, N., Tatsuno, I., Hanski, E., Caparon, M. & Sasakawa, C. (1998). Streptococcus pyogenes protein F promotes invasion of HeLa cells. Microbiology 144, 3079-3086.
35. Reichardt, W., Muller-Alouf, H., Alouf, J. E. & Kohler, W. (1992). Erythrogenic toxins A, B and C: occurrence of the genes and exotoxin formation from clinical Streptococcus pyogenes strains associated with streptococcal toxic shock-like syndrome. FEMS Microbiol Lett 79, 313-322.
36. Sawai, J., Hasegawa, T., Kamimura, T., Okamoto, A., Ohmori, D., Nosaka, N., Yamada, K., Torii, K. & Ohta, M. (2007). Growth phase-dependent effect of clindamycin on production of exoproteins by Streptococcus pyogenes. Antimicrob Agents Chemother 51, 461-467.
37. Severin, A., Nickbarg, E., Wooters, J., Quazi, S. A., Matsuka, Y. V., Murphy, E., Moutsatsos, I. K., Zagursky, R. J. & Olmsted, S. B. (2007). Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. J Bacteriol 189, 1514-1522.
38. Smoot, J. C., Barbian, K. D., Van Gompel, J. J., Smoot, L. M., Chaussee, M. S., Sylva, G. L., Sturdevant, D. E., Ricklefs, S. M., Porcella, S. F. & other authors (2002). Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc Natl Acad Sci U S A 99, 4668-4673.
39. Sumby, P., Barbian, K. D., Gardner, D. J., Whitney, A. R., Welty, D. M., Long, R. D., Bailey, J. R., Parnell, M. J., Hoe, N. P. & other authors (2005a). Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci U S A 102, 1679-1684.
40. Sumby, P., Porcella, S. F., Madrigal, A. G., Barbian, K. D., Virtaneva, K., Ricklefs, S. M., Sturdevant, D. E., Graham, M. R., Vuopio-Varkila, J. & other authors (2005b). Evolutionary origin and emergence of a highly successful clone of serotype M1 group A Streptococcus involved multiple horizontal gene transfer events. J Infect Dis 192, 771-782.
41. Tanaka, M., Hasegawa, T., Okamoto, A., Torii, K. & Ohta, M. (2005). Effect of antibiotics on group A Streptococcus exoprotein production analyzed by two-dimensional gel electrophoresis. Antimicrob Agents Chemother 49, 88-96.
42. Walker, M. J., Hollands, A., Sanderson-Smith, M. L., Cole, J. N., Kirk, J. K., Henningham, A., McArthur, J. D., Dinkla, K., Aziz, R. K. & other authors (2007). DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med 13, 981-985.
43. Wannamaker, L. W. (1958). The differentiation of three distinct desoxyribonucleases of group A streptococci. J Exp Med 107, 797-812.
44. Wannamaker, L. W. & Yasmineh, W. (1967). Streptococcal nucleases. I. Further studies on the A, B, and C enzymes. J Exp Med 126, 475-496.
45. Wannamaker, L. W., Hayes, B. & Yasmineh, W. (1967). Streptococcal nucleases. II. Characterization of DNAse D. J Exp Med 126, 497-508.