The Role of Host and Microbial Factors in the Pathogenesis of Pneumococcal Bacteraemia Arising from a Single Bacterial Cell Bottleneck

English version České info

Decades of research on bacterial sepsis have been devoted to analysing the steps that lead from a local event, either carriage or a localised infection, to systemic disease. Our work analyses in depth the events determining systemic infection by one of the main human pathogens, Streptococcus pneumoniae. Consistent with similar findings on the pathogenesis of bacteraemia due to other commensal pathogens, our results show that after an intravenous inoculum of a million pneumococci, the resulting septicaemia is often founded by a single bacterial cell. Investigation into the nature of this monoclonal infection identified strong within-host selective pressure for metabolic fitness during outgrowth of the bacterial population.

Vyšlo v časopise: The Role of Host and Microbial Factors in the Pathogenesis of Pneumococcal Bacteraemia Arising from a Single Bacterial Cell Bottleneck. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1004026
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004026

Souhrn

Zdroje

1. GrayBM, ConverseGM, DillonHCJ (1980) Epidemiologic studies of Streptococcus pneumoniae in infants: acquisition, carriage, and infection during the first 24 months of life. J Infect Dis 142: 923–933.

2. HogbergL, GeliP, RingbergH, MelanderE, LipsitchM, et al. (2007) Age- and serogroup-related differences in observed durations of nasopharyngeal carriage of penicillin-resistant pneumococci. J Clin Microbiol 45: 948–952.

3. MelegaroA, EdmundsWJ, PebodyR, MillerE, GeorgeR (2006) The current burden of pneumococcal disease in England and Wales. Journal of Infection 52: 37–48.

4. IspahaniP, SlackRCB, DonaldFE, WestonWC, RutterN (2004) Twenty year surveillance of invasive pneumococcal disease in Nottingham: serogroups responsible and implications for immunisation. Arch Dis Child 89: 757–762.

5. RudanI, Boschi-PintoC, MulhollandK, CampbellH (2008) Epidemiology and ethiology of childhood pneumoniae. Bull World Health Organ 86: 408–416.

6. KadiogluA, WeiserJN, PatonJC, AndrewPW (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6: 288–301.

7. ChiavoliniD, PozziG, RicciS (2008) Animal models of Streptococcus pneumoniae disease. Clin Microbiol Rev 21: 666–685.

8. WrightDH (1927) Experimental pneumococcal septicaemia and anti-pneumococcal immunity. The Journal of Pathology and Bacteriology 30: 185–252.

9. RogersDE, MellyMA (1957) Studies on bacteriemia II. Further observations on the granulocytopenia induced by the intravenous injection of staphylococci. J Exp Med 105: 99–112.

10. RogersDE (1960) Host mechanisms which act to remove bacteria from the blood stream. Bacteriol Rev 24: 50–66.

11. HoseaSW, BrownEJ, FrankMM (1980) The critical role of complement in experimental pneumococcal sepsis. J Infect Dis 142: 903–909.

12. HoseaSW, BrownEJ, HammerCH, FrankMM (1980) Role of complement activation in a model of adult respiratory distress syndrome. J Clin Invest 66: 375–382.

13. Van WyckDB, WitteMH, WitteCL (1982) Synergism between the spleen and serum complement in experimental pneumococcemia. J Infect Dis 145: 514–519.

14. BrownEJ, HoseaSW, FrankMM (1983) The role of antibody and complement in the reticuloendothelial clearance of pneumococci from the bloodstream. Rev Infect Dis 5: 797–805.

15. LevinBR, AntiaR (2001) Why we don't get sick: the within-host population dynamics of bacterial infections. Science 292: 1112–1115.

16. GrantJA, RestifO, McKinleyJT, SheppardM, MaskellDJ, et al. (2008) Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLOS Biology 6: 757–770.

17. MeynellGG, MawJ (1968) Evidence for a two-stage model of microbial infection. J Hyg (London) 66: 273–280.

18. SheppardM, WebbC, HeathF, MallowsV, EmilianusR, et al. (2003) Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol 5: 593–600 296 [pii].

19. SacristanS, MalpicaJM, FraileA, Garcia-ArenalF (2003) Estimation of population bottlenecks during systemic movement of tobacco mosaic virus in tobacco plants. J Virol 77: 9906–9911.

20. BarnesPD, BergmanMA, MecsasJ, IsbergRR (2006) Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. J Exp Med 203: 1591–1601.

21. BrownSP, CornellSJ, SheppardM, GrantAJ, MaskellDJ, et al. (2006) Intracellular demography and the dynamics of Salmonella enterica infections. PLoS Biol 4: e349.

22. MeynellGG, StockerBAD (1957) Some hypotheses on the aetiology of fatal infections in partially resistant hosts and their application to mice challenged with Salmonella paratyphi-B or Salmonella typhimurium by intraperitoneal injection. J Gen Microbiol 16: 58.

23. MargolisE, LevinBR (2007) Within-host evolution for the invasiveness of commensal bacteria: an experimental study of bacteremias resulting from Haemophilus influenzae nasal carriage. J Infect Dis 196: 1068–1075.

24. MeynellGG (1957) The applicability of the hypothesis of indipendent action to fatal infections in mice given Salmonella typhimurium by mouth. J Gen Microbiol 16: 396–404.

25. MoxonER, MurphyPA (1978) Haemophilus influenzae bacteremia and meningitis resulting from survival of a single organism. Proc Natl Acad Sci USA 75: 1534–1536.

26. PlunschkeG, MercerA, KusecekB, PohlA, AchtmanM (1983) Induction of bacteremia in newborn rats Escherichia coli K1 is correlated with only certain O (lipopolysaccharide) antigen type. Infect Immun 39: 599–607.

27. RubinLG (1987) Bacterial colonizzation and resulting from multiplication of a single organism. Reviews of Infectious Diseases 9: 488–493.

28. OggioniMR, MemmiG, MaggiT, ChiavoliniD, IannelliF, et al. (2003) Pneumococcal zinc metalloproteinase ZmpC cleaves human matrix metalloproteinase 9 and is a virulence factor in experimental pneumonia. Mol Microbiol 49: 795–805.

29. WeiserJN, AustrianR, SreenivasanPK, MasureHR (1994) Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infect Immun 62: 2582–2589.

30. RipollVM, KadiogluA, CoxR, HumeDA, DennyP (2010) Macrophages from BALB/c and CBA/Ca mice differ in their cellular responses to Streptococcus pneumoniae. J Leukoc Biol 87: 735–741.

31. van RooijenN, SandersA (1994) Liposome mediated depletion of macrophages:mechanism of action, preparation of liposomes and applications. J Immunol Methods 174: 83–93.

32. FlemingTJ, FlemingML, MalekTR (1993) Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family. J Immunol 151: 2399–2408.

33. DaleyJM, ThomayAA, ConnollyMD, ReichnerSJ, AlbinaJE (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. Journal of Leukocyte Biology 83: 64–70.

34. AlateryA, BastaS (2008) An efficient culture method for generating large quantities of mature mouse splenic macrophages. J Immunol Methods 338: 47–57.

35. BrownEJ, HoseaSW, FrankMM (1981) The role of complement in the localisation of pneumococci in the splenic reticuloendothelial system during experimental bacteremia. The Journal of Immunology 126: 2230–2234.

36. BrownEJ, HoseaSW, FrankMM (1981) The role of the spleen in experimental pneumococcal bacteremia. J Clin Invest 67: 975–982.

37. ShortleyG, WilkinsJR (1965) Independen-action and birth-death models in experimental microbiology. Bacteriol Rev 29: 102–141.

38. stevensKE, SebertME (2011) Frequent beneficial mutations during single-colony serial transfer of Streptococcus pneumoniae. Plos Genet 7: e1002232.

39. PericoneCD, BaeD, ShchepetovM, McCoolT, WeiserJN (2002) Short-sequence tandem and nontandem DNA repeats and endogenous hydrogen peroxide production contribute to genetic instability of Streptococcus pneumoniae. J Bacteriol 184: 4392–4399.

40. MunozR, GarciaE, de la CampaAG (1996) Quinine specifically inhibits the proteolipid subunit of the F0F1 H+ -ATPase of Streptococcus pneumoniae. J Bacteriol 178: 2455–2458.

41. PikisA, CamposJM, RodriguezWJ, KeithJM (2001) Optochin resistance in Streptococcus pneumoniae: mechanism, significance, and clinical implications. J Infect Dis 184: 582–590.

42. Martin-GalianoAJ, GorgojoB, KuninCM, de la CampaAG (2002) Mefloquine and new related compounds target the F(0) complex of the F(0)F(1) H(+)-ATPase of Streptococcus pneumoniae. Antimicrob Agents Chemother 46: 1680–1687.

43. DiasCA, AgnesG, FrazzonAP, KrugerFD, d'AzevedoPA, et al. (2007) Diversity of mutations in the atpC gene coding for the c Subunit of F0F1 ATPase in clinical isolates of optochin-resistant Streptococcus pneumoniae from Brazil. J Clin Microbiol 45: 3065–3067.

44. NunesS, Sà-LeaoR, De LencastreH (2008) Optochin resistence among Streptococcus pneumoniae strains colonizing healthy children in Portugal. J Clin Microbiol 46: 321–324.

45. KrulwichTA, SachsG, PadanE (2011) Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol 9: 330–343 nrmicro2549 [pii];10.1038/nrmicro2549 [doi]

46. LeeEJ, PontesMH, GroismanEA (2013) A bacterial virulence protein promotes pathogenicity by inhibiting the bacterium's own F1Fo ATP synthase. Cell 154: 146–156.

47. CroucherNJ, MitchellAM, GouldKA, InverarityD, BarquistL, et al. (2013) Dominant role of nucleotide substitution in the diversification of serotype 3 pneumococci over decades and during a single infection. PLoS Genet 9: e1003868.

48. ChiavoliniD, MemmiG, MaggiT, IannelliF, PozziG, et al. (2003) The three extra-cellular zinc metalloproteinases of Streptococcus pneumoniae have a different impact on virulence in mice. BMC Microbiol 3: 14.

49. PozziG, MasalaL, IannelliF, ManganelliR, HavarsteinLS, et al. (1996) Competence for genetic transformation in encapsulated strains of Streptococcus pneumoniae: two allelic variants of the peptide pheromone. J Bacteriol 178: 6087–6090.

50. DopazoJ, MendozaA, HerreroJ, CaldaraF, HumbertY, et al. (2001) Annotated draft genomic sequence from Streptococcus pneumoniae type 19F clinical isolate. Microb Drug Resist 7: 99–125.

51. PozziG, MusmannoRA, RenzoniEA, OggioniMR, CusiMG (1988) Host-vector system for integration of recombinant DNA into chromosomes of transformable and nontransformable streptococci. J Bacteriol 170: 1969–1972.

52. IannelliF, ChiavoliniD, RicciS, OggioniMR, PozziG (2004) Pneumococcal surface protein C contributes to sepsis caused by Streptococcus pneumoniae in mice. Infect Immun 72: 3077–3080.

53. BidossiA, MulasL, DecorosiF, ColombaL, RicciS, et al. (2012) A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PLoS ONE 7: e33320.

54. TrappettiC, OgunniyiAD, OggioniMR, PatonJC (2011) Extracellular matrix fromation enhances the ability of Streptococcus pneumoniae to cause invasive disease. PLoS ONE 6: e19844.

55. Ben-HorinH, TassiniM, ViviA, NavonG, KaplanO (1995) Mechanism of action of the antineoplastic drug lonidamine: 31P and 13C nuclear magnetic resonance studies. Cancer Res 55: 2814–2821.

56. KadiogluA, CupponeAM, TrappettiC, ListT, SpreaficoA, et al. (2011) Sex-based differences in susceptibility to respiratory and systemic pneumococcal disease in mice. J Infect Dis 204: 1971–1979.

57. OggioniMR, IannelliF, RicciS, ChiavoliniD, ParigiR, et al. (2004) Antibacterial activity of a competence-stimulating peptide in experimental sepsis caused by Streptococcus pneumoniae. Antimicrob Agents Chemother 48: 4725–4732.

58. OggioniMR, TrappettiC, KadiogluA, CassoneM, IannelliF, et al. (2006) Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis. Mol Microbiol 61: 1196–1210.

59. CiabattiniA, PettiniE, AndersenP, PozziG, MedagliniD (2008) Primary activation of antigen-specific naive CD4+ and CD8+ T cells following intranasal vaccination with recombinant bacteria. Infect Immun 76: 5817–5825.

60. ZhouX, RenL, MengQ, LiY, YuY, et al. (2010) The next-generation sequencing technology and application. Protein Cell 1: 520–536.

61. KoboldtDC, ZhangQ, LarsonDE, ShenD, McLellanMD, et al. (2012) VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 22: 568–576.

62. LanieJA, NgWL, KazmierczakKM, AndrzejewskiTM, DavidsenTM, et al. (2007) Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol 189: 38–51.

63. TettelinH, NelsonKE, PaulsenIT, EisenJA, ReadTD, et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498–506.