Igniting the Fire: Virulence Factors in the Pathogenesis of Sepsis

1. LowyFD (1998) Staphylococcus aureus infections. N Engl J Med 339: 520–532.

2. AngusDC, Linde-ZwirbleWT, LidickerJ, ClermontG, CarcilloJ, et al. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29: 1303–1310.

3. RussellJA (2006) Management of sepsis. N Engl J Med 355: 1699–1713.

4. CannonCM, HolthausCV, ZubrowMT, PosaP, GunagaS, et al. (2012) The GENESIS Project (GENeralized Early Sepsis Intervention Strategies): A Multicenter Quality Improvement Collaborative. J Intensive Care Med 28: 355–368.

5. SalomaoR, BrunialtiMK, RapozoMM, Baggio-ZappiaGL, GalanosC, et al. (2012) Bacterial sensing, cell signaling, and modulation of the immune response during sepsis. Shock 38: 227–242.

6. HashimotoM, TawaratsumidaK, KariyaH, KiyoharaA, SudaY, et al. (2006) Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus. J Immunol 177: 3162–3169.

7. Bubeck WardenburgJ, WilliamsWA, MissiakasD (2006) Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc Natl Acad Sci U S A 103: 13831–13836.

8. De KimpeSJ, KengatharanM, ThiemermannC, VaneJR (1995) The cell wall components peptidoglycan and lipoteichoic acid from Staphylococcus aureus act in synergy to cause shock and multiple organ failure. Proc Natl Acad Sci U S A 92: 10359–10363.

9. Salgado-PabonW, BreshearsL, SpauldingAR, MerrimanJA, StachCS, et al. (2013) Superantigens are critical for Staphylococcus aureus Infective endocarditis, sepsis, and acute kidney injury. MBio 4: e00494–13.

10. YoongP, TorresVJ (2013) The effects of Staphylococcus aureus leukotoxins on the host: cell lysis and beyond. Curr Opin Microbiol 16: 63–69.

11. WangR, BraughtonKR, KretschmerD, BachT-HL, QueckSY, et al. (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nature Medicine 13: 1510–1514.

12. BerubeBJ, Bubeck WardenburgJ (2013) Staphylococcus aureus alpha-Toxin: Nearly a Century of Intrigue. Toxins (Basel) 5: 1140–1166.

13. LiM, DiepBA, VillaruzAE, BraughtonKR, JiangX, et al. (2009) Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 106: 5883–5888.

14. ChuaKY, SeemannT, HarrisonPF, MonagleS, KormanTM, et al. (2011) The dominant Australian community-acquired methicillin-resistant Staphylococcus aureus clone ST93-IV [2B] is highly virulent and genetically distinct. PLoS One 6: e25887 doi:10.1371/journal.pone.0025887

15. DeLeoFR, KennedyAD, ChenL, Bubeck WardenburgJ, KobayashiSD, et al. (2011) Molecular differentiation of historic phage-type 80/81 and contemporary epidemic Staphylococcus aureus. Proc Natl Acad Sci U S A 108: 18091–18096.

16. MalachowaN, KobayashiSD, BraughtonKR, WhitneyAR, ParnellMJ, et al. (2012) Staphylococcus aureus leukotoxin GH promotes inflammation. J Infect Dis 206: 1185–1193.

17. PowersME, KimHK, WangY, Bubeck WardenburgJ (2012) ADAM10 mediates vascular injury induced by Staphylococcus aureus alpha-hemolysin. J Infect Dis 206: 352–356.

18. AlonzoF3rd, BensonMA, ChenJ, NovickRP, ShopsinB, et al. (2012) Staphylococcus aureus leucocidin ED contributes to systemic infection by targeting neutrophils and promoting bacterial growth in vivo. Mol Microbiol 83: 423–435.

19. DumontAL, NygaardTK, WatkinsRL, SmithA, KozhayaL, et al. (2011) Characterization of a new cytotoxin that contributes to Staphylococcus aureus pathogenesis. Mol Microbiol 79: 814–825.

20. NizetV (2007) Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J Allergy Clin Immunol 120: 13–22.

21. de HaasCJ, VeldkampKE, PeschelA, WeerkampF, Van WamelWJ, et al. (2004) Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J Exp Med 199: 687–695.

22. PostmaB, PoppelierMJ, van GalenJC, ProssnitzER, van StrijpJA, et al. (2004) Chemotaxis inhibitory protein of Staphylococcus aureus binds specifically to the C5a and formylated peptide receptor. J Immunol 172: 6994–7001.

23. RooijakkersSH, RuykenM, RoosA, DahaMR, PresanisJS, et al. (2005) Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat Immunol 6: 920–927.

24. RooijakkersSH, RuykenM, van RoonJ, van KesselKP, van StrijpJA, et al. (2006) Early expression of SCIN and CHIPS drives instant immune evasion by Staphylococcus aureus. Cell Microbiol 8: 1282–1293.

25. LindmarkR, Thoren-TollingK, SjoquistJ (1983) Binding of immunoglobulins to protein A and immunoglobulin levels in mammalian sera. J Immunol Methods 62: 1–13.

26. GoodyearCS, SilvermanGJ (2004) Staphylococcal toxin induced preferential and prolonged in vivo deletion of innate-like B lymphocytes. Proc Natl Acad Sci U S A 101: 11392–11397.

27. ChengAG, KimHK, BurtsML, KrauszT, SchneewindO, et al. (2009) Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. Faseb J 23: 3393–3404.

28. KimHK, ChengAG, KimHY, MissiakasDM, SchneewindO (2010) Nontoxigenic protein A vaccine for methicillin-resistant Staphylococcus aureus infections in mice. J Exp Med 207: 1863–1870.

29. PalmqvistN, FosterT, TarkowskiA, JosefssonE (2002) Protein A is a virulence factor in Staphylococcus aureus arthritis and septic death. Microb Pathog 33: 239–249.

30. Reyes-RoblesT, AlonzoF3rd, KozhayaL, LacyDB, UnutmazD, et al. (2013) Staphylococcus aureus Leukotoxin ED Targets the Chemokine Receptors CXCR1 and CXCR2 to Kill Leukocytes and Promote Infection. Cell Host Microbe 14: 453–459.

31. PanizziP, FriedrichR, Fuentes-PriorP, RichterK, BockPE, et al. (2006) Fibrinogen substrate recognition by staphylocoagulase (pro)thrombin complexes. J Biol Chem 281: 1179–1187.

32. BjerketorpJ, JacobssonK, FrykbergL (2004) The von Willebrand factor-binding protein (vWbp) of Staphylococcus aureus is a coagulase. FEMS Microbiol Lett 234: 309–314.

33. McAdowM, KimHK, DedentAC, HendrickxAP, SchneewindO, et al. (2011) Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLoS Pathog 7: e1002307 doi:10.1371/journal.ppat.1002307

34. SchoutenM, WiersingaWJ, LeviM, van der PollT (2008) Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol 83: 536–545.

35. EngelmannB, MassbergS (2013) Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 13: 34–45.

36. WongCH, JenneCN, PetriB, ChrobokNL, KubesP (2013) Nucleation of platelets with blood-borne pathogens on Kupffer cells precedes other innate immunity and contributes to bacterial clearance. Nat Immunol 14: 785–792.

37. BhakdiS, MuhlyM, MannhardtU, HugoF, KlapettekK, et al. (1988) Staphylococcal alpha toxin promotes blood coagulation via attack on human platelets. J Exp Med 168: 527–542.

38. EdwardsAM, PottsJR, JosefssonE, MasseyRC (2010) Staphylococcus aureus host cell invasion and virulence in sepsis is facilitated by the multiple repeats within FnBPA. PLoS Pathog 6: e1000964 doi:10.1371/journal.ppat.1000964

39. CarnesEC, LopezDM, DoneganNP, CheungA, GreshamH, et al. (2010) Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nat Chem Biol 6: 41–45.

40. BagnoliF, BertholetS, GrandiG (2012) Inferring reasons for the failure of Staphylococcus aureus vaccines in clinical trials. Front Cell Infect Microbiol 2: 16.

41. LemichezE, LecuitM, NassifX, BourdoulousS (2010) Breaking the wall: targeting of the endothelium by pathogenic bacteria. Nat Rev Microbiol 8: 93–104.