Mechanisms of NDV-3 vaccine efficacy in MRSA skin versus invasive infection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 51, 2014, Pages E5555-E5563

  Yeaman, Michael R ^a,b,c   Filler, Scott G ^a,b,c   Chaili, Siyang ^b,c   Barr, Kevin ^c   Wang, Huiyuan ^b,c   Kupferwasser, Deborah ^b,c   Hennessey, John P ^d   Fu, Yue ^a,b,c   Schmidt, Clint S ^d   Edwards, John E ^a,b,c   Xiong, Yan Q ^a,b,c   Ibrahim, Ashraf S ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARBOR UCLA MEDICAL CENTER   (United States)

^c St John's Cardiovascular Research Center   (United States)

^d NovaDigm Therapeutics Inc   (United States)

Author keywords

Skin; Staphylococcus aureus; Th17; Th22; Vaccine

Indexed keywords

BACTERIAL VACCINE; INTERLEUKIN 17; INTERLEUKIN 22; NDV 3 VACCINE; UNCLASSIFIED DRUG; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; CD3+ T LYMPHOCYTE; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; INNATE IMMUNITY; LOW DRUG DOSE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN ABSCESS; STAPHYLOCOCCAL SKIN INFECTION; ANIMAL; DISEASE MODEL; IMMUNOLOGY; METABOLISM; SKIN DISEASES, BACTERIAL; STAPHYLOCOCCAL INFECTIONS; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANIMALS; BACTERIAL VACCINES; DISEASE MODELS, ANIMAL; INTERLEUKIN-17; INTERLEUKINS; MICE; SKIN DISEASES, BACTERIAL; STAPHYLOCOCCAL INFECTIONS; T-LYMPHOCYTES;

EID: 84929499068     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1415610111     Document Type: Article

References (87)

1. Singer AJ, Talan DA (2014) Management of skin abscesses in the era of methicillinresistant Staphylococcus aureus. N Engl J Med 370(11):1039-1047.
2. Miller LS, Cho JS (2011) Immunity against Staphylococcus aureus cutaneous infections. Nat Rev Immunol 11(8):505-518.
3. Cheng AG, DeDent AC, Schneewind O, Missiakas D (2011) A play in four acts: Staphylococcus aureus abscess formation. Trends Microbiol 19(5):225-232.
4. David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: Epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23(3):616-687.
5. Geria AN, Schwartz RA (2010) Impetigo update: New challenges in the era of methicillin resistance. Cutis 85(2):65-70.
6. Gunderson CG, Martinello RA (2012) A systematic review of bacteremias in cellulitis and erysipelas. J Infect 64(2):148-155.
7. Sabin BR, Peters N, Peters AT (2012) Chapter 20: Atopic dermatitis. Allergy Asthma Proc 33(Suppl 1):S67-S69.
8. Karamatsu ML, Thorp AW, Brown L (2012) Changes in community-associated methicillin-resistant Staphylococcus aureus skin and soft tissue infections presenting to the pediatric emergency department: Comparing 2003 to 2008. Pediatr Emerg Care 28(2): 131-135.
9. Klevens RM, et al.; Active Bacterial Core Surveillance (ABCs) MRSA Investigators (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298(15):1763-1771.
10. Armstrong DG (2011) An overview of foot infections in diabetes. Diabetes Technol Ther 13(9):951-957.
11. Wisplinghoff H, et al. (2004) Nosocomial bloodstream infections in US hospitals: Analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39(3):309-317.
12. Tattevin P, et al. (2012) Concurrent epidemics of skin and soft tissue infection and bloodstream infection due to community-associated methicillin-resistant Staphylococcus aureus. Clin Infect Dis 55(6):781-788.
13. Landrum ML, et al. (2012) Epidemiology of Staphylococcus aureus blood and skin and soft tissue infections in the US military health system, 2005-2010. JAMA 308(1):50-59.
14. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF (2010) Community-associated meticillinresistant Staphylococcus aureus. Lancet 375(9725):1557-1568.
15. Chambers HF, Deleo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7(9):629-641.
16. van Hal SJ, et al. (2012) Predictors of mortality in Staphylococcus aureus bacteremia. Clin Microbiol Rev 25(2):362-386.
17. Rivera AM, Boucher HW (2011) Current concepts in antimicrobial therapy against select gram-positive organisms: Methicillin-resistant Staphylococcus aureus, penicillinresistant pneumococci, and vancomycin-resistant enterococci. Mayo Clin Proc 86(12): 1230-1243.
18. Boucher H, Miller LG, Razonable RR (2010) Serious infections caused by methicillinresistant Staphylococcus aureus. Clin Infect Dis 51(Suppl 2):S183-S197.
19. Selton-Suty C, et al.; AEPEI Study Group (2012) Preeminence of Staphylococcus aureus in infective endocarditis: A 1-year population-based survey. Clin Infect Dis 54(9):1230-1239.
20. Bae IG, et al.; International Collaboration on Endocarditis-Microbiology Investigator (2009) Heterogeneous vancomycin-intermediate susceptibility phenotype in bloodstream methicillin-resistant Staphylococcus aureus isolates from an international cohort of patients with infective endocarditis: Prevalence, genotype, and clinical significance. J Infect Dis 200(9):1355-1366.
21. Sreeramoju P, et al. (2011) Recurrent skin and soft tissue infections due to methicillinresistant Staphylococcus aureus requiring operative debridement. Am J Surg 201(2): 216-220.
22. Kang YC, Tai WC, Yu CC, Kang JH, Huang YC (2012) Methicillin-resistant Staphylococcus aureus nasal carriage among patients receiving hemodialysis in Taiwan: Prevalence rate, molecular characterization and de-colonization. BMC Infect Dis 12(1):284.
23. Lanoix JP, et al. (2011) Bacterial infection profiles in lung cancer patients with febrile neutropenia. BMC Infect Dis 11:183.
24. Chen CY, et al. (2010) Epidemiology of bloodstream infections in patients with haematological malignancies with and without neutropenia. Epidemiol Infect 138(7): 1044-1051.
25. Fishman JA (2011) Infections in immunocompromised hosts and organ transplant recipients: Essentials. Liver Transpl 17(Suppl 3):S34-S37.
26. Farr AM, Aden B, Weiss D, Nash D, Marx MA (2012) Trends in hospitalization for community-associated methicillin-resistant Staphylococcus aureus in New York City, 1997-2006: Data from New York State's Statewide Planning and Research Cooperative System. Infect Control Hosp Epidemiol 33(7):725-731.
27. Shadyab AH, Crum-Cianflone NF (2012) Methicillin-resistant Staphylococcus aureus (MRSA) infections among HIV-infected persons in the era of highly active antiretroviral therapy: A review of the literature. HIV Med 13(6):319-332.
28. Renner ED, et al. (2008) Novel signal transducer and activator of transcription 3 (STAT3) mutations, reduced T(H)17 cell numbers, and variably defective STAT3 phosphorylation in hyper-IgE syndrome. J Allergy Clin Immunol 122(1):181-187.
29. Horváth R, et al. (2011) Expansion of T helper type 17 lymphocytes in patients with chronic granulomatous disease. Clin Exp Immunol 166(1):26-33.
30. van den Berg JM, et al. (2009) Chronic granulomatous disease: The European experience. PLoS ONE 4(4):e5234.
31. Song E, et al. (2011) Chronic granulomatous disease: A review of the infectious and inflammatory complications. Clin Mol Allergy 9(1):10.
32. Chmiel JF, et al. (2014) Antibiotic management of lung infections in cystic fibrosis. I. The microbiome, methicillin-resistant Staphylococcus aureus, gram-negative bacteria, and multiple infections. Ann Am Thorac Soc 11(7):1120-1129.
33. Ma CS, et al. (2008) Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J ExpMed 205(7):1551-1557.
34. Milner JD, et al. (2008) Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 452(7188):773-776.
35. Freeman AF, Holland SM (2008) The hyper-IgE syndromes. Immunol Allergy Clin North Am 28(2):277-291, viii 10.1016/j.iac.2008.01.005.
36. Minegishi Y, et al. (2009) Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J Exp Med 206(6):1291-1301.
37. Winkelstein JA, et al. (2000) Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore) 79(3):155-169.
38. Bagnoli F, Bertholet S, Grandi G (2012) Inferring reasons for the failure of Staphylococcus aureus vaccines in clinical trials. Front Cell Infect Microbiol 2:16.
39. Weisman LE (2007) Antibody for the prevention of neonatal noscocomial staphylococcal infection: A review of the literature. Arch Pediatr 14(Supp 1):S31-S34.
40. Weems JJ, Jr, et al. (2006) Phase II, randomized, double-blind, multicenter study comparing the safety and pharmacokinetics of tefibazumab to placebo for treatment of Staphylococcus aureus bacteremia. Antimicrob Agents Chemother 50(8):2751-2755.
41. Weisman LE, et al. (2011) A randomized study of a monoclonal antibody (pagibaximab) to prevent staphylococcal sepsis. Pediatrics 128(2):271-279.
42. Proctor RA (2012) Challenges for a universal Staphylococcus aureus vaccine. Clin Infect Dis 54(8):1179-1186.
43. Sheppard DC, et al. (2004) Functional and structural diversity in the Als protein family of Candida albicans. J Biol Chem 279(29):30480-30489.
44. Yeaman MR, et al. (2014) Applying convergent immunity to innovative vaccines targeting Staphylococcus aureus. Front Immunol 5:463 10.3389/fimmu.2014.00463.
45. Spellberg BJ, et al. (2006) Efficacy of the anti-Candida rAls3p-N or rAls1p-N vaccines against disseminated and mucosal candidiasis. J Infect Dis 194(2):256-260.
46. Spellberg B, et al. (2008) The antifungal vaccine derived from the recombinant N terminus of Als3p protects mice against the bacterium Staphylococcus aureus. Infect Immun 76(10):4574-4580.
47. Lin L, et al. (2009) Immunological surrogate marker of rAls3p-N vaccine-induced protection against Staphylococcus aureus. FEMS Immunol Med Microbiol 55(3):293-295.
48. Lin L, et al. (2009) Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLoS Pathog 5(12): e1000703.
49. Schmidt CS, et al. (2012) NDV-3, a recombinant alum-adjuvanted vaccine for Candida and Staphylococcus aureus, is safe and immunogenic in healthy adults. Vaccine 30(52):7594-7600.
50. Bals R, et al. (1999) Mouse β-defensin 3 is an inducible antimicrobial peptide expressed in the epithelia of multiple organs. Infect Immun 67(7):3542-3547.
51. Montgomery CP, et al. (2014) Protective immunity against recurrent Staphylococcus aureus skin infection requires antibody and interleukin-17A. Infect Immun 82(5): 2125-2134.
52. Fowler VG, Jr, Proctor RA (2014) Where does a Staphylococcus aureus vaccine stand? Clin Microbiol Infect 20(Suppl 5):66-75.
53. Seok J, et al.; Inflammation and Host Response to Injury, Large Scale Collaborative Research Program (2013) Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA 110(9):3507-3512.
54. Takao K, Miyakawa T (2014) Genomic responses in mouse models greatly mimic human inflammatory diseases. Proc Natl Acad Sci USA, 10.1073/pnas.1401965111.
55. Salgado-Pabón W, Schlievert PM (2014) Models matter: The search for an effective Staphylococcus aureus vaccine. Nat Rev Microbiol 12(8):585-591.
56. Murugaiyan G, Mittal A, Weiner HL (2010) Identification of an IL-27/osteopontin axis in dendritic cells and its modulation by IFN-gamma limits IL-17-mediated autoimmune inflammation. Proc Natl Acad Sci USA 107(25):11495-11500.
57. Lee J, et al. (2013) Interferon gamma suppresses collagen-induced arthritis by regulation of Th17 through the induction of indoleamine-2,3-doxygenase. PLoS One 8(4): 60900.
58. Doodes PD, et al. (2010) IFN-gamma regulates the requirement for IL-17 in proteoglycan-induced arthritis. J Immunol 184(3):1552-1559.
59. Conti HR, et al. (2009) Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med 206(2):299-311.
60. + T cells and CXC chemokines modulate the pathogenesis of Staphylococcus aureus wound infections. Proc Natl Acad Sci USA 103(27): 10408-10413.
61. Cho JS, et al. (2010) IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J Clin Invest 120(5):1762-1773.
62. Sanos SL, Vonarbourg C, Mortha A, Diefenbach A (2011) Control of epithelial cell function by interleukin-22-producing RORγt+ innate lymphoid cells. Immunology 132(4):453-465.
63. Mölne L, Corthay A, Holmdahl R, Tarkowski A (2003) Role of gamma/delta T cell receptor-expressing lymphocytes in cutaneous infection caused by Staphylococcus aureus. Clin Exp Immunol 132(2):209-215.
64. Puel A, et al. (2011) Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332(6025):65-68.
65. Kupper TS, Fuhlbrigge RC (2004) Immune surveillance in the skin: Mechanisms and clinical consequences. Nat Rev Immunol 4(3):211-222.
66. Basu R, et al. (2012) Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 37(6):1061-1075.
67. Ziesché E, et al. (2009) Dexamethasone suppresses interleukin-22 associated with bacterial infection in vitro and in vivo. Clin Exp Immunol 157(3):370-376.
68. Schröder JM (2010) The role of keratinocytes in defense against infection. Curr Opin Infect Dis 23(2):106-110.
69. Joshi A, et al. (2012) Immunization with Staphylococcus aureus iron regulated surface determinant B (IsdB) confers protection via Th17/IL17 pathway in a murine sepsis model. Hum Vaccin Immunother 8(3):336-346.
70. Tewary P, et al. (2013) β-defensin 2 and 3 promote the uptake of self or CpG DNA, enhance IFN-α production by human plasmacytoid dendritic cells, and promote inflammation. J Immunol 191(2):865-874.
71. Yount NY, Yeaman MR (2012) Emerging themes and therapeutic prospects for antiinfective peptides. Annu Rev Pharmacol Toxicol 52:337-360.
72. Ibrahim AS, et al. (2013) NDV-3 protects mice from vulvovaginal candidiasis through T- and B-cell immune response. Vaccine 31(47):5549-5556.
73. Minegishi Y, Karasuyama H (2009) Defects in Jak-STAT-mediated cytokine signals cause hyper-IgE syndrome: Lessons from a primary immunodeficiency. Int Immunol 21(2):105-112.
74. Yang XP, et al. (2011) Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat Immunol 12(3):247-254.
75. Miller LS, et al. (2007) Inflammasome-mediated production of IL-1beta is required for neutrophil recruitment against Staphylococcus aureus in vivo. J Immunol 179(10): 6933-6942.
76. Nestle FO, Di Meglio P, Qin JZ, Nickoloff BJ (2009) Skin immune sentinels in health and disease. Nat Rev Immunol 9(10):679-691.
77. Nabel GJ, Fauci AS (2010) Induction of unnatural immunity: Prospects for a broadly protective universal influenza vaccine. Nat Med 16(12):1389-1391.
78. Popov L, Kovalski J, Grandi G, Bagnoli F, Amieva MR (2014) Three-dimensional human skin models to understand Staphylococcus aureus skin colonization and infection. Front Immunol 5:41.
79. Brown AF, Leech JM, Rogers TR, McLoughlin RM (2014) Staphylococcus aureus colonization: Modulation of host immune response and impact on human vaccine design. Front Immunol 4:507.
80. Kadurugamuwa JL, et al. (2003) Direct continuous method for monitoring biofilm infection in a mouse model. Infect Immun 71(2):882-890.
81. Anonymous (2003) Outbreaks of community-associated methicillin-resistant Staphylococcus aureus skin infections-Los Angeles County, California, 2002-2003. MMWR Morb Mortal Wkly Rep 52(5):88.
82. Diep BA, et al. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367(9512): 731-739.
83. Baba T, et al. (2002) Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359(9320):1819-1827.
84. Voyich JM, et al. (2006) Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J Infect Dis 194(12):1761-1770.
85. Ding Y, Onodera Y, Lee JC, Hooper DC (2008) NorB, an efflux pump in Staphylococcus aureus strain MW2, contributes to bacterial fitness in abscesses. J Bacteriol 190(21): 7123-7129.
86. Ahrens K, et al. (2011) Mechanical and metabolic injury to the skin barrier leads to increased expression of murine β-defensin-1, -3, and -14. J Invest Dermatol 131(2): 443-452.
87. Robertson D, Savage K, Reis-Filho JS, Isacke CM (2008) Multiple immunofluorescence labelling of formalin-fixed paraffin-embedded (FFPE) tissue. BMC Cell Biol 9:13.