Structurally Designed Attenuated Subunit Vaccines for S. aureus LukS-PV and LukF-PV Confer Protection in a Mouse Bacteremia Model

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Karauzum, Hatice ^a   Adhikari, Rajan P ^a   Sarwar, Jawad ^a   Devi, V Sathya ^a   Abaandou, Laura ^a   Haudenschild, Christian ^a   Mahmoudieh, Mahta ^a   Boroun, Atefeh R ^a   Vu, Hong ^a   Nguyen, Tam ^a   Warfield, Kelly L ^a   Shulenin, Sergey ^a   Aman, M Javad ^a  

^a Integrated BioTherapeutics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LUKF PV VACCINE; LUKS PV VACCINE; PANTON VALENTINE LEUKOCIDIN; STAPHYLOCOCCUS VACCINE; SUBUNIT VACCINE; UNCLASSIFIED DRUG;

ACTIVE IMMUNIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; CROSS REACTION; FEMALE; IMMUNOGENICITY; INFECTION PREVENTION; INFECTION RESISTANCE; MOUSE; NONHUMAN; OLIGOMERIZATION; PASSIVE IMMUNIZATION; STAPHYLOCOCCAL BACTEREMIA; THERMOSTABILITY;

ADJUVANTS, IMMUNOLOGIC; AMINO ACIDS; ANIMALS; ANTIBODIES, NEUTRALIZING; BACTEREMIA; BACTERIAL LOAD; BACTERIAL PROTEINS; BACTERIAL TOXINS; CROSS REACTIONS; DISEASE MODELS, ANIMAL; DRUG DESIGN; EXOTOXINS; IMMUNIZATION; LEUKOCIDINS; MICE; MICE, INBRED BALB C; MUTANT PROTEINS; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN UNFOLDING; SEQUENCE HOMOLOGY, AMINO ACID; STAPHYLOCOCCUS AUREUS; TEMPERATURE; VACCINES, ATTENUATED; VACCINES, SUBUNIT;

MUS; ORYCTOLAGUS CUNICULUS; POSIBACTERIA; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE;

EID: 84878764873     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065384     Document Type: Article

References (43)

1. Nizet V, (2007) Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J Allergy Clin Immunol 120: 13-22.
2. Kotzin BL, Leung DY, Kappler J, Marrack P, (1993) Superantigens and their potential role in human disease. Adv Immunol 54: 99-166.
3. Meyer RD, Monday SR, Bohach GA, Schlievert SM, (2001) Prolonged course of toxic shock syndrome associated with methicillin-resistant Staphylococcus aureus enterotoxins G and I. Int J Infect Dis. 5: 163-166.
4. Schuberth HJ, Krueger C, Zerbe H, Bleckmann E, Leibold W, (2001) Characterization of leukocytotoxic and superantigen-like factors produced by Staphylococcus aureus isolates from milk of cows with mastitis. Vet Microbiol 82: 187-199.
5. Tristan A, Ferry T, Durand G, Dauwalder O, Bes M, et al. (2007) Virulence determinants in community and hospital meticillin-resistant Staphylococcus aureus. J Hosp Infect 65Suppl 2: 105-109.
6. Diep BA, Otto M, (2008) The role of virulence determinants in community-associated MRSA pathogenesis. Trends Microbiol 16: 361-369.
7. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, et al. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731-739.
8. Kaneko J, Kimura T, Narita S, Tomita T, Kamio Y, (1998) Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. Gene 215: 57-67.
9. Narita S, Kaneko J, Chiba J, Piemont Y, Jarraud S, et al. (2001) Phage conversion of Panton-Valentine leukocidin in Staphylococcus aureus: molecular analysis of a PVL-converting phage, phiSLT. Gene 268: 195-206.
10. Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, et al. (2002) Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359: 753-759.
11. Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, et al. (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29: 1128-1132.
12. Miles G, Movileanu L, Bayley H, (2002) Subunit composition of a bicomponent toxin: staphylococcal leukocidin forms an octameric transmembrane pore. Protein Sci 11: 894-902.
13. Pedelacq JD, Prevost G, Monteil H, Mourey L, Samama JP, (2000) Crystal structure of the F component of the Panton-Valentine leucocidin. Int J Med Microbiol 290: 395-401.
14. Kaneko J, Kamio Y, (2004) Bacterial two-component and hetero-heptameric pore-forming cytolytic toxins: structures, pore-forming mechanism, and organization of the genes. Biosci Biotechnol Biochem 68: 981-1003.
15. Ferreras M, Hoper F, Dalla Serra M, Colin DA, Prevost G, et al. (1998) The interaction of Staphylococcus aureus bi-component gamma-hemolysins and leucocidins with cells and lipid membranes. Biochim Biophys Acta 1414: 108-126.
16. Prevost G, Cribier B, Couppie P, Petiau P, Supersac G, et al. (1995) Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect Immun 63: 4121-4129.
17. Malachowa N, Whitney AR, Kobayashi SD, Sturdevant DE, Kennedy AD, et al. (2011) Global changes in Staphylococcus aureus gene expression in human blood. PLoS One 6: e18617.
18. Aman MJ, Karauzum H, Bowden MG, Nguyen TL, (2010) Structural model of the pre-pore ring-like structure of Panton-Valentine leukocidin: providing dimensionality to biophysical and mutational data. J Biomol Struct Dyn 28: 1-12.
19. Fattom AI, Sarwar J, Ortiz A, Naso R, (1996) A Staphylococcus aureus capsular polysaccharide (CP) vaccine and CP-specific antibodies protect mice against bacterial challenge. Infect Immun 64: 1659-1665.
20. Adhikari RP, Karauzum H, Sarwar J, Abaandou L, Mahmoudieh M, et al. (2012) Novel structurally designed vaccine for S. aureus alpha-hemolysin: protection against bacteremia and pneumonia. PLoS One 7: e38567.
21. Devi VS, Sprecher CB, Hunziker P, Mittl PR, Bosshard HR, et al. (2006) Disulfide formation and stability of a cysteine-rich repeat protein from Helicobacter pylori. Biochemistry 45: 1599-1607.
22. Yamashita K, Kawai Y, Tanaka Y, Hirano N, Kaneko J, et al. (2011) Crystal structure of the octameric pore of staphylococcal gamma-hemolysin reveals the beta-barrel pore formation mechanism by two components. Proc Natl Acad Sci U S A 108: 17314-17319.
23. Adhikari RP, Ajao AO, Aman MJ, Karauzum H, Sarwar J, et al. (2012) Lower antibody levels to Staphylococcus aureus exotoxins are associated with sepsis in hospitalized adults with invasive S. aureus infections. J Infect Dis 206: 915-923.
24. Guillet V, Roblin P, Werner S, Coraiola M, Menestrina G, et al. (2004) Crystal structure of leucotoxin S component: new insight into the Staphylococcal beta-barrel pore-forming toxins. J Biol Chem 279: 41028-41037.
25. Romero-Steiner S, Libutti D, Pais LB, Dykes J, Anderson P, et al. (1997) Standardization of an opsonophagocytic assay for the measurement of functional antibody activity against Streptococcus pneumoniae using differentiated HL-60 cells. Clin Diagn Lab Immunol 4: 415-422.
26. Ericsson UB, Hallberg BM, Detitta GT, Dekker N, Nordlund P, (2006) Thermofluor-based high-throughput stability optimization of proteins for structural studies. Anal Biochem 357: 289-298.
27. He F, Hogan S, Latypov RF, Narhi LO, Razinkov VI, (2010) High throughput thermostability screening of monoclonal antibody formulations. J Pharm Sci 99: 1707-1720.
28. Coler RN, Baldwin SL, Shaverdian N, Bertholet S, Reed SJ, et al. (2010) A synthetic adjuvant to enhance and expand immune responses to influenza vaccines. PLoS ONE 5: e13677.
29. Coler RN, Bertholet S, Moutaftsi M, Guderian JA, Windish HP, et al. (2011) Development and characterization of synthetic glucopyranosyl lipid adjuvant system as a vaccine adjuvant. PLoS ONE 6: e16333.
30. Mullen GE, Ellis RD, Miura K, Malkin E, Nolan C, et al. (2008) Phase 1 trial of AMA1-C1/Alhydrogel plus CPG 7909: an asexual blood-stage vaccine for Plasmodium falciparum malaria. PLoS ONE 3: e2940.
31. Gravet A, Colin DA, Keller D, Girardot R, Monteil H, et al. (1998) Characterization of a novel structural member, LukE-LukD, of the bi-component staphylococcal leucotoxins family. FEBS Lett 436: 202-208.
32. Finck-Barbancon V, Duportail G, Meunier O, Colin DA, (1993) Pore formation by a two-component leukocidin from Staphylococcus aureus within the membrane of human polymorphonuclear leukocytes. Biochim Biophys Acta 1182: 275-282.
33. Holzinger D, Gieldon L, Mysore V, Nippe N, Taxman DJ, et al. (2012) Staphylococcus aureus Panton-Valentine leukocidin induces an inflammatory response in human phagocytes via the NLRP3 inflammasome. J Leukoc Biol 92: 1069-1081.
34. Perret M, Badiou C, Lina G, Burbaud S, Benito Y, et al. (2012) Cross-talk between Staphylococcus aureus leukocidins-intoxicated macrophages and lung epithelial cells triggers chemokine secretion in an inflammasome-dependent manner. Cell Microbiol 14: 1019-1036.
35. Brown EL, Dumitrescu O, Thomas D, Badiou C, Koers EM, et al. (2009) The Panton-Valentine leukocidin vaccine protects mice against lung and skin infections caused by Staphylococcus aureus USA300. Clin Microbiol Infect 15: 156-164.
36. Cremieux AC, Dumitrescu O, Lina G, Vallee C, Cote JF, et al. (2009) Panton-valentine leukocidin enhances the severity of community-associated methicillin-resistant Staphylococcus aureus rabbit osteomyelitis. PLoS One 4: e7204.
37. Diep BA, Chan L, Tattevin P, Kajikawa O, Martin TR, et al. (2010) Polymorphonuclear leukocytes mediate Staphylococcus aureus Panton-Valentine leukocidin-induced lung inflammation and injury. Proc Natl Acad Sci U S A 107: 5587-5592.
38. Varshney AK, Martinez LR, Hamilton SM, Bryant AE, Levi MH, et al. (2009) Augmented Production of Panton-Valentine Leukocidin Toxin in Methicillin-Resistant and Methicillin-Susceptible Staphylococcus aureus Is Associated with Worse Outcome in a Murine Skin Infection Model. J Infect Dis.
39. Alonzo F, 3rd, Benson MA, Chen J, Novick RP, Shopsin B, 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.
40. Malachowa N, DeLeo FR, (2011) Staphylococcus aureus survival in human blood. Virulence 2: 567-569.
41. Nilsson IM, Hartford O, Foster T, Tarkowski A, (1999) Alpha-toxin and gamma-toxin jointly promote Staphylococcus aureus virulence in murine septic arthritis. Infect Immun 67: 1045-1049.
42. Supersac G, Piemont Y, Kubina M, Prevost G, Foster TJ, (1998) Assessment of the role of gamma-toxin in experimental endophthalmitis using a hlg-deficient mutant of Staphylococcus aureus. Microb Pathog 24: 241-251.
43. Ventura CL, Malachowa N, Hammer CH, Nardone GA, Robinson MA, et al. (2010) Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. PLoS ONE 5: e11634.