Competence-Independent Activity of Pneumococcal Enda Mediates Degradation of Extracellular DNA and Nets and Is Important for Virulence

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Zhu, Luchang ^a   Kuang, Zhizhou ^a   Wilson, Brenda A ^b   Lau, Gee W ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ENDA PROTEIN; ENDONUCLEASE; EXTRACELLULAR DNA; NEUTROPHIL EXTRACELLULAR TRAP; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOLYSIS; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM COMPETENCE; BACTERIUM MUTANT; CONTROLLED STUDY; CYTOLYSIS; DNA DEGRADATION; GENETIC TRANSFORMATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; REGULON; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; BACTERIAL PROTEINS; DNA; ELECTROPHORESIS, AGAR GEL; ENDODEOXYRIBONUCLEASES; EXTRACELLULAR SPACE; HOST-PATHOGEN INTERACTIONS; MEMBRANE PROTEINS; MICE; MICROSCOPY, FLUORESCENCE; MUTATION; NEUTROPHIL ACTIVATION; NEUTROPHILS; PNEUMONIA, PNEUMOCOCCAL; STREPTOCOCCUS PNEUMONIAE; TRANSFORMATION, BACTERIAL; VIRULENCE;

EID: 84881171225     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070363     Document Type: Article

References (35)

1. Rosenthal AL, Lacks SA, (1980) Complex structure of the membrane nuclease of Streptococcus pneumoniae revealed by two-dimensional electrophoresis. J Mol Biol 141: 133-146.
2. Kohoutova DM, (1961) Mechanism of the transformation of the polysaccharide capsule in Pneumococcus. Nature 190: 1171-1173.
3. Lacks S, Greenberg B, (1973) Competence for deoxyribonucleic acid uptake and deoxyribonuclease action external to cells in the genetic transformation of Diplococcus pneumoniae. J Bacteriol 114: 152-163.
4. Lacks S, Greenberg B, Neuberger M, (1974) Role of a deoxyribonuclease in the genetic transformation of Diplococcus pneumoniae. Proc Natl Acad Sci U S A 71: 2305-2309.
5. Lacks S, Greenberg B, Neuberger M, (1975) Identification of a deoxyribonuclease implicated in genetic transformation of Diplococcus pneumoniae. J Bacteriol 123: 222-232.
6. Lacks S, (1962) Molecular fate of DNA in genetic transformation of Pneumococcus. J Mol Biol 5: 119-131.
7. Chen JD, Morrison DA, (1987) Modulation of competence for genetic transformation in Streptococcus pneumoniae. J Gen Microbiol 133: 1959-1967.
8. Berge M, Moscoso M, Prudhomme M, Martin B, Claverys JP, (2002) Uptake of transforming DNA in Gram-positive bacteria: a view from Streptococcus pneumoniae. Mol Microbiol 45: 411-421.
9. Hava DL, Camilli A, (2002) Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol 45: 1389-1406.
10. Beiter K, Wartha F, Albiger B, Normark S, Zychlinsky A, et al. (2006) An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 16: 401-407.
11. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
12. Avery OT, MacLeod CM, McCarty M, (1979) Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Inductions of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J Exp Med 149: 297-326.
13. Avery OT, Macleod CM, McCarty M, (1944) Studies on the Chemical Nature of the Substance Inducing Transformation of Pneumococcal Types: Induction of Transformation by a Desoxyribonucleic Acid Fraction Isolated from Pneumococcus Type Iii. J Exp Med 79: 137-158.
14. Lau GW, Haataja S, Lonetto M, Kensit SE, Marra A, et al. (2001) A functional genomic analysis of type 3 Streptococcus pneumoniae virulence. Mol Microbiol 40: 555-571.
15. Sung CK, Li H, Claverys JP, Morrison DA, (2001) An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl Environ Microbiol 67: 5190-5196.
16. Sung CK, Morrison DA, (2005) Two distinct functions of ComW in stabilization and activation of the alternative sigma factor ComX in Streptococcus pneumoniae. J Bacteriol 187: 3052-3061.
17. Zhu L, Lau GW, (2011) Inhibition of competence development, horizontal gene transfer and virulence in Streptococcus pneumoniae by a modified competence stimulating peptide. PLoS Pathog 7: e1002241.
18. Morrison DA, Trombe MC, Hayden MK, Waszak GA, Chen JD, (1984) Isolation of transformation-deficient Streptococcus pneumoniae mutants defective in control of competence, using insertion-duplication mutagenesis with the erythromycin resistance determinant of pAM beta 1. J Bacteriol 159: 870-876.
19. Jeffries CD, Holtman DF, Guse DG, (1957) Rapid method for determining the activity of microorganisms on nucleic acids. J Bacteriol 73: 590-591.
20. Johnsborg O, Kristiansen PE, Blomqvist T, Havarstein LS, (2006) A hydrophobic patch in the competence-stimulating Peptide, a pneumococcal competence pheromone, is essential for specificity and biological activity. J Bacteriol 188: 1744-1749.
21. Liu CL, Tangsombatvisit S, Rosenberg JM, Mandelbaum G, Gillespie EC, et al. (2012) Specific post-translational histone modifications of neutrophil extracellular traps as immunogens and potential targets of lupus autoantibodies. Arthritis Res Ther 14: R25.
22. Hallick RB, Chelm BK, Gray PW, Orozco EM Jr, (1977) Use of aurintricarboxylic acid as an inhibitor of nucleases during nucleic acid isolation. Nucleic Acids Res 4: 3055-3064.
23. Pestova EV, Havarstein LS, Morrison DA, (1996) Regulation of competence for genetic transformation in Streptococcus pneumoniae by an auto-induced peptide pheromone and a two-component regulatory system. Mol Microbiol 21: 853-862.
24. Mellroth P, Daniels R, Eberhardt A, Ronnlund D, Blom H, et al. (2012) LytA, the major autolysin of Streptococcus pneumoniae, requires access to the nascent peptidoglycan. J Biol Chem.
25. Garcia P, Gonzalez MP, Garcia E, Lopez R, Garcia JL, (1999) LytB, a novel pneumococcal murein hydrolase essential for cell separation. Mol Microbiol 31: 1275-1281.
26. Briese T, Hakenbeck R, (1985) Interaction of the pneumococcal amidase with lipoteichoic acid and choline. Eur J Biochem 146: 417-427.
27. Mellroth P, Daniels R, Eberhardt A, Ronnlund D, Blom H, et al. (2012) LytA, major autolysin of Streptococcus pneumoniae, requires access to nascent peptidoglycan. J Biol Chem 287: 11018-11029.
28. Steinmoen H, Knutsen E, Havarstein LS, (2002) Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population. Proc Natl Acad Sci U S A 99: 7681-7686.
29. Moscoso M, Garcia E, Lopez R, (2006) Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J Bacteriol 188: 7785-7795.
30. Luo P, Li H, Morrison DA, (2003) ComX is a unique link between multiple quorum sensing outputs and competence in Streptococcus pneumoniae. Mol Microbiol 50: 623-633.
31. Lee MS, Morrison DA, (1999) Identification of a new regulator in Streptococcus pneumoniae linking quorum sensing to competence for genetic transformation. J Bacteriol 181: 5004-5016.
32. Alloing G, Martin B, Granadel C, Claverys JP, (1998) Development of competence in Streptococcus pneumonaie: pheromone autoinduction and control of quorum sensing by the oligopeptide permease. Mol Microbiol 29: 75-83.33. Chen I, Dubnau D (2004) DNA uptake during bacterial transformation. Nat Rev Microbiol 2: 241-249.
33. Tran TD, Kwon HY, Kim EH, Kim KW, Briles DE, et al. (2011) Decrease in penicillin susceptibility due to heat shock protein ClpL in Streptococcus pneumoniae. Antimicrob Agents Chemother 55: 2714-2728.
34. Moscoso M, Claverys JP, (2004) Release of DNA into the medium by competent Streptococcus pneumoniae: kinetics, mechanism and stability of the liberated DNA. Mol Microbiol 54: 783-794.
35. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498-506.