Peptidoglycan Branched Stem Peptides Contribute to Streptococcus pneumoniae Virulence by Inhibiting Pneumolysin Release

PLoS Pathogens

Volumn 11, Issue 6, 2015, Pages

  Greene, Neil G ^a   Narciso, Ana R ^b   Filipe, Sergio R ^b   Camilli, Andrew ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GALACTOSIDASE; CHOLINE; PEPTIDOGLYCAN; PNEUMOLYSIN; PLY PROTEIN, STREPTOCOCCUS PNEUMONIAE; STREPTOLYSIN; VIRULENCE FACTOR;

ALLELE; ANALYTIC METHOD; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BINDING ASSAY; CORRELATION COEFFICIENT; ENZYME ACTIVITY; ESCHERICHIA COLI; HEMOLYSIS; LUNG INFECTION; MILLER ASSAY; MOUSE; MURINAE; NONHUMAN; PNEUMONIA; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; RNA EXTRACTION; STREPTOCOCCUS PNEUMONIAE; STRUCTURE ANALYSIS; WESTERN BLOTTING; ANIMAL; CELL WALL; CHEMISTRY; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PENICILLIN RESISTANCE; PHYSIOLOGY; PNEUMOCOCCAL INFECTION; VIRULENCE;

BACTERIA (MICROORGANISMS); MURINAE; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; BACTERIAL PROTEINS; CELL WALL; MICE; PENICILLIN RESISTANCE; PEPTIDOGLYCAN; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS; VIRULENCE; VIRULENCE FACTORS;

EID: 84936760752     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004996     Document Type: Article

References (63)

1. Bogaert D, de Groot R, Hermans PWM, (2004) Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis 4: 144–154. doi: 10.1016/S1473-3099(04)00938-7 14998500
2. Kadioglu A, Weiser JN, Paton JC, Andrew PW, (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6: 288–301. doi: 10.1038/nrmicro1871 18340341
3. Rubins JB, Duane PG, Charboneau D, Janoff EN, (1992) Toxicity of pneumolysin to pulmonary endothelial cells in vitro. Infect Immun 60: 1740–1746. 1563759
4. Zysk G, Schneider-Wald BK, Hwang JH, Bejo L, Kim KS, et al. (2001) Pneumolysin is the main inducer of cytotoxicity to brain microvascular endothelial cells caused by Streptococcus pneumoniae. Infect Immun 69: 845–852. doi: 10.1128/IAI.69.2.845–852.2001 11159977
5. Baba H, Kawamura I, Kohda C, Nomura T, Ito Y, et al. (2001) Essential role of domain 4 of pneumolysin from Streptococcus pneumoniae in cytolytic activity as determined by truncated proteins. Biochem Biophys Res Commun 281: 37–44. doi: 10.1006/bbrc.2001.4297 11178957
6. Paton JC, Rowan-Kelly B, Ferrante A, (1984) Activation of human complement by the pneumococcal toxin pneumolysin. Infect Immun 43: 1085–1087. 6698602
7. Ratner AJ, Hippe KR, Aguilar JL, Bender MH, Nelson AL, et al. (2006) Epithelial cells are sensitive detectors of bacterial pore-forming toxins. J Biol Chem 281: 12994–12998. doi: 10.1074/jbc.M511431200 16520379
8. Shoma S, Tsuchiya K, Kawamura I, Nomura T, Hara H, et al. (2008) Critical involvement of pneumolysin in production of interleukin-1α and caspase-1-dependent cytokines in infection with Streptococcus pneumoniae in vitro: a novel function of pneumolysin in caspase-1 activation. Infect Immun 76: 1547–1557. doi: 10.1128/IAI.01269-07 18195026
9. McNeela EA, Burke Á, Neill DR, Baxter C, Fernandes VE, et al. (2010) Pneumolysin activates the NLRP3 inflammasome and promotes proinflammatory cytokines independently of TLR4. PLoS Pathog 6: e1001191. doi: 10.1371/journal.ppat.1001191 21085613
10. Walker JA, Allen RL, Falmagne P, Johnson MK, Boulnois GJ, (1987) Molecular cloning, characterization, and complete nucleotide sequence of the gene for pneumolysin, the sulfhydryl-activated toxin of Streptococcus pneumoniae. Infect Immun 55: 1184–1189. 3552992
11. Balachandran P, Hollingshead SK, Paton JC, Briles DE, (2001) The autolytic enzyme LytA of Streptococcus pneumoniae is not responsible for releasing pneumolysin. J Bacteriol 183: 3108–3116. doi: 10.1128/JB.183.10.3108–3116.2001 11325939
12. Price KE, Camilli A, (2009) Pneumolysin localizes to the cell wall of Streptococcus pneumoniae. J Bacteriol 191: 2163–2168. doi: 10.1128/JB.01489-08 19168620
13. Price KE, Greene NG, Camilli A, (2012) Export requirements of pneumolysin in Streptococcus pneumoniae. J Bacteriol 194: 3651–3660. doi: 10.1128/JB.00114-12 22563048
14. Typas A, Banzhaf M, Gross CA, Vollmer W, (2011) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10: 123–136. doi: 10.1038/nrmicro2677 22203377
15. Schleifer KH, Kandler O, (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36: 407–477. 4568761
16. Garcia-Bustos JF, Chait BT, Tomasz A, (1987) Structure of the peptide network of pneumococcal peptidoglycan. J Biol Chem 262: 15400–15405. 2890629
17. Filipe SR, Pinho MG, Tomasz A, (2000) Characterization of the murMN operon involved in the synthesis of branched peptidoglycan peptides in Streptococcus pneumoniae. J Biol Chem 275: 27768–27774. doi: 10.1074/jbc.M004675200 10869361
18. Lloyd AJ, Gilbey AM, Blewett AM, De Pascale G, Zoeiby El A, et al. (2008) Characterization of tRNA-dependent peptide bond formation by MurM in the synthesis of Streptococcus pneumoniae peptidoglycan. J Biol Chem 283: 6402–6417. doi: 10.1074/jbc.M708105200 18077448
19. De Pascale G, Lloyd AJ, Schouten JA, Gilbey AM, Roper DI, et al. (2008) Kinetic characterization of lipid II-Ala:alanyl-tRNA ligase (MurN) from Streptococcus pneumoniae using semisynthetic aminoacyl-lipid II substrates. J Biol Chem 283: 34571–34579. doi: 10.1074/jbc.M805807200 18842590
20. Filipe SR, Tomasz A, (2000) Inhibition of the expression of penicillin resistance in Streptococcus pneumoniae by inactivation of cell wall muropeptide branching genes. Proc Natl Acad Sci USA 97: 4891–4896. doi: 10.1073/pnas.080067697 10759563
21. Garcia-Bustos J, Tomasz A, (1990) A biological price of antibiotic resistance: major changes in the peptidoglycan structure of penicillin-resistant pneumococci. Proc Natl Acad Sci USA 87: 5415–5419. 2371278
22. Smith AM, Klugman KP, (2001) Alterations in MurM, a cell wall muropeptide branching enzyme, increase high-level penicillin and cephalosporin resistance in Streptococcus pneumoniae. Antimicrob Agents Chemother 45: 2393–2396. doi: 10.1128/AAC.45.8.2393–2396.2001 11451707
23. Filipe SR, Severina E, Tomasz A, (2000) Distribution of the mosaic structured murM genes among natural populations of Streptococcus pneumoniae. J Bacteriol 182: 6798–6805. 11073926
24. Filipe SR, Severina E, Tomasz A, (2002) The murMN operon: a functional link between antibiotic resistance and antibiotic tolerance in Streptococcus pneumoniae. Proc Natl Acad Sci USA 99: 1550–1555. doi: 10.1073/pnas.032671699 11830670
25. Bergmann S, (2006) Versatility of pneumococcal surface proteins. Microbiology 152: 295–303. doi: 10.1099/mic.0.28610–0 16436417
26. Dijkstra AJ, Keck W, (1996) Peptidoglycan as a barrier to transenvelope transport. J Bacteriol 178: 5555–5562. 8824596
27. Gould AR, May BK, Elliott WH, (1975) Release of extracellular enzymes from Bacillus amyloliquefaciens. J Bacteriol 122: 34–40. 47325
28. Laitinen H, Tomasz A, (1990) Changes in composition of peptidoglycan during maturation of the cell wall in pneumococci. J Bacteriol 172: 5961–5967. 2120197
29. Filipe SR, Severina E, Tomasz A, (2001) Functional analysis of Streptococcus pneumoniae MurM reveals the region responsible for its specificity in the synthesis of branched cell wall peptides. J Biol Chem 276: 39618–39628. doi: 10.1074/jbc.M106425200 11522792
30. Hava DL, Hemsley CJ, Camilli A, (2003) Transcriptional regulation in the Streptococcus pneumoniae rlrA pathogenicity islet by RlrA. J Bacteriol 185: 413–421. doi: 10.1128/JB.185.2.413–421.2003 12511486
31. Vollmer W, Joris B, Charlier P, Foster S, (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32: 259–286. doi: 10.1111/j.1574-6976.2007.00099.x 18266855
32. Briles DE, King JD, Gray MA, McDaniel LS, Swiatlo E, et al. (1996) PspA, a protection-eliciting pneumococcal protein: immunogenicity of isolated native PspA in mice. Vaccine 14: 858–867. 8843627
33. Guiral S, Mitchell TJ, Martin B, Claverys J-P, (2005) Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. Proc Natl Acad Sci USA 102: 8710–8715. doi: 10.1073/pnas.0500879102 15928084
34. Demchick P, Koch AL, (1996) The permeability of the wall fabric of Escherichia coli and Bacillus subtilis. J Bacteriol 178: 768–773. 8550511
35. Koch AL, Woeste S, (1992) Elasticity of the sacculus of Escherichia coli. J Bacteriol 174: 4811–4819. 1624468
36. Merchante R, Pooley HM, Karamata D, (1995) A periplasm in Bacillus subtilis. J Bacteriol 177: 6176–6183. 7592383
37. Matias VRF, Beveridge TJ, (2005) Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol Microbiol 56: 240–251. 15773993
38. Matias VRF, Beveridge TJ, (2006) Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J Bacteriol 188: 1011–1021. doi: 10.1128/JB.188.3.1011–1021.2006 16428405
39. Matias VRF, Beveridge TJ, (2008) Lipoteichoic acid is a major component of the Bacillus subtilis periplasm. J Bacteriol 190: 7414–7418. doi: 10.1128/JB.00581-08 18790869
40. Marquis H, Hager EJ, (2000) pH-regulated activation and release of a bacteria-associated phospholipase C during intracellular infection by Listeria monocytogenes. Mol Microbiol 35: 289–298. 10652090
41. Snyder A, Marquis H, (2003) Restricted translocation across the cell wall regulates secretion of the broad-range phospholipase C of Listeria monocytogenes. J Bacteriol 185: 5953–5958. 14526005
42. Lemon JK, Weiser JN, (2015) Degradation products of the extracellular pathogen Streptococcus pneumoniae access the cytosol via its pore-forming toxin. mBio 6. doi: 10.1128/mBio.02110-14
43. Atilano ML, Pereira PM, Vaz F, Catalão MJ, Reed P, et al. (2014) Bacterial autolysins trim cell surface peptidoglycan to prevent detection by the Drosophila innate immune system. eLife 3. doi: 10.7554/eLife.02277.019
44. Barendt SM, Sham L-T, Winkler ME, (2011) Characterization of mutants deficient in the L,D-carboxypeptidase (DacB) and WalRK (VicRK) regulon, involved in peptidoglycan maturation of Streptococcus pneumoniae serotype 2 strain D39. J Bacteriol 193: 2290–2300. doi: 10.1128/JB.01555-10 21378199
45. 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. doi: 10.1074/jbc.M111.318584 22334685
46. Albarracín Orio AG, Piñas GE, Cortes PR, Cian MB, Echenique J, (2011) Compensatory evolution of pbp mutations restores the fitness cost imposed by β-lactam resistance in Streptococcus pneumoniae. PLoS Pathog 7: e1002000. doi: 10.1371/journal.ppat.1002000 21379570
47. Zarantonelli ML, Skoczynska A, Antignac A, Ghachi El M, Deghmane A-E, et al. (2013) Penicillin resistance compromises Nod1-dependent proinflammatory activity and virulence fitness of Neisseria meningitidis. Cell Host Microbe 13: 735–745. doi: 10.1016/j.chom.2013.04.016 23768497
48. Trzciński K, Thompson CM, Gilbey AM, Dowson CG, Lipsitch M, (2006) Incremental increase in fitness cost with increased β-lactam resistance in pneumococci evaluated by competition in an infant rat nasal colonization model. J Infect Dis 193: 1296–1303. doi: 10.1086/501367 16586368
49. Berg KH, Stamsås GA, Straume D, Håvarstein LS, (2013) Effects of low PBP2b levels on cell morphology and peptidoglycan composition in Streptococcus pneumoniae R6. J Bacteriol 195: 4342–4354. doi: 10.1128/JB.00184-13 23873916
50. Bui NK, Eberhardt A, Vollmer D, Kern T, Bougault C, et al. (2011) Isolation and analysis of cell wall components from Streptococcus pneumoniae. Anal Biochem 421: 657–666. doi: 10.1016/j.ab.2011.11.026 22192687
51. Rijneveld AW, van den Dobbelsteen GP, Florquin S, Standiford TJ, Speelman P, et al. (2002) Roles of interleukin-6 and macrophage inflammatory protein-2 in pneumolysin-induced lung inflammation in mice. J Infect Dis 185: 123–126. doi: 10.1086/338008 11756992
52. Orihuela CJ, Radin JN, Sublett JE, Gao G, Kaushal D, et al. (2004) Microarray analysis of pneumococcal gene expression during invasive disease. Infect Immun 72: 5582–5596. doi: 10.1128/IAI.72.10.5582–5596.2004 15385455
53. Berry AM, Yother J, Briles DE, Hansman D, Paton JC, (1989) Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect Immun 57: 2037–2042. 2731982
54. Berry AM, Ogunniyi AD, Miller DC, Paton JC, (1999) Comparative virulence of Streptococcus pneumoniae strains with insertion-duplication, point, and deletion mutations in the pneumolysin gene. Infect Immun 67: 981–985. 9916120
55. Orihuela CJ, Gao G, Francis KP, Yu J, Tuomanen EI, (2004) Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J Infect Dis 190: 1661–1669. 15478073
56. Benton KA, Everson MP, Briles DE, (1995) A pneumolysin-negative mutant of Streptococcus pneumoniae causes chronic bacteremia rather than acute sepsis in mice. Infect Immun 63: 448–455. 7822009
57. Bricker AL, Camilli A, (1999) Transformation of a type 4 encapsulated strain of Streptococcus pneumoniae. FEMS Microbiol Lett 172: 131–135. 10188240
58. Nickels BE, (2009) Genetic assays to define and characterize protein-protein interactions involved in gene regulation. Methods 47: 53–62. doi: 10.1016/j.ymeth.2008.10.011 18952173
59. Shainheit MG, Mule M, Camilli A, (2014) The core promoter of the capsule operon of Streptococcus pneumoniae is necessary for colonization and invasive disease. Infect Immun 82: 694–705. doi: 10.1128/IAI.01289-13 24478084
60. Karmakar M, Katsnelson M, Malak HA, Greene NG, Howell SJ, et al. (2015) Neutrophil IL-1β processing induced by pneumolysin is mediated by the NLRP3/ASC inflammasome and caspase-1 activation and is dependent on K+ efflux. J Immunol 194: 1763–1775. doi: 10.4049/jimmunol.1401624 25609842
61. Avery OT, Macleod CM, McCarty M, (1944) Studies on the chemical nature of the substance inducing transformation of pneumococcal types. J Exp Med 79: 137–158. 19871359
62. Zighelboim S, Tomasz A, (1980) Penicillin-binding proteins of multiply antibiotic-resistant South African strains of Streptococcus pneumoniae. Antimicrob Agents Chemother 17: 434–442. 6903436
63. Martin B, Prudhomme M, Alloing G, Granadel C, Claverys J-P, (2000) Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Mol Microbiol 38: 867–878. 11115120