Immunization with Staphylococcus aureus iron regulated surface determinant B (IsdB) confers protection via Th17/IL17 pathway in a murine sepsis model

Human Vaccines and Immunotherapeutics

Volumn 8, Issue 3, 2012, Pages 326-336

  Joshi, Amita ^a   Pancari, Greg ^a   Cope, Leslie ^a   Bowman, Edward P ^b   Cua, Daniel ^b   Proctor, Richard A ^c   McNeely, Tessie ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

^b MRL Palo Alto   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Antibodies; Immune response; Staphylococcus; T cells; Th17; Vaccine

Indexed keywords

BOVINE SERUM ALBUMIN; CD19 ANTIGEN; CD45 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 4; STAPHYLOCOCCUS AUREUS IRON REGULATED SURFACE DETERMINANT B VACCINE; STAPHYLOCOCCUS VACCINE; SYNDECAN 1; UNCLASSIFIED DRUG;

ACTIVE IMMUNIZATION; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CAUSE OF DEATH; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG EFFICACY; DRUG SCREENING; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; INTRACELLULAR SIGNALING; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PLASMA CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROVOCATION TEST; SPLEEN CELL; STAPHYLOCOCCAL BACTEREMIA; SURVIVAL RATE; TH17 CELL;

EID: 84859093780     PISSN: None     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.8.3.18946     Document Type: Article

References (71)

1. Lee JC. The prospects for developing a vaccine against Staphylococcus aureus. Trends Microbiol 1996; 4:162-6; PMID:8728611; http://dx.doi.org/10.1016/ 0966-842X(96)10021-4
2. Middleton JR. Staphylococcus aureus antigens and challenges in vaccine development. Expert Rev Vaccines 2008; 7:805-15; PMID:18665778; http://dx.doi.org/10.1586/14760584.7.6.805
3. Otto M. Targeted immunotherapy for staphylococcal infections : focus on anti-MSCRAMM antibodies. BioDrugs 2008; 22:27-36; PMID:18215088; http://dx.doi.org/10.2165/00063030-200822010-00003
4. Schaffer AC, Lee JC. Vaccination and passive immunisation against Staphylococcus aureus. Int J Antimicrob Agents 2008; 32(Suppl 1):S71-8; PMID:18757184; http://dx.doi.org/10.1016/j.ijantimicag.2008.06.009
5. Cunnion KM, Benjamin DK, Jr., Hester CG, Frank MM. Role of complement receptors 1 and 2 (CD35 and CD21), C3, C4, and C5 in survival by mice of Staphylococcus aureus bacteremia. J Lab Clin Med 2004; 143:358-65; PMID:15192652; http://dx.doi.org/10.1016/j.lab.2004.03.005
6. Gregory SH, Sagnimeni AJ, Wing EJ. Bacteria in the bloodstream are trapped in the liver and killed by immigrating neutrophils. J Immunol 1996; 157:2514-20; PMID:8805652
7. Verdrengh M, Tarkowski A. Role of neutrophils in experimental septicemia and septic arthritis induced by Staphylococcus aureus. Infect Immun 1997; 65:2517-21; PMID:9199413
8. Peterson PK, Wilkinson BJ, Kim Y, Schmeling D, Douglas SD, Quie PG, et al. The key role of peptidoglycan in the opsonization of Staphylococcus aureus. J Clin Invest 1978; 61:597-609; PMID:641141; http://dx.doi.org/10.1172/JCI108971
9. Verbrugh HA, Peterson PK, Nguyen BYT, Sisson SP, Kim Y. Opsonization of encapsulated Staphylococcus aureus: the role of specific antibody and complement. J Immunol 1982; 129:1681-7; PMID:7108223
10. Leijh PCJ, van den Barselaar MT, Daha MR, van Furth R. Participation of immunoglobulins and complement components in the intracellular killing of Staphylococcus aureus and Escherichia coli by human granulocytes. Infect Immun 1981; 33:714-24; PMID:7026443
11. Anwar S, Prince LR, Foster SJ, Whyte MKB, Sabroe I. The rise and rise of Staphylococcus aureus: laughing in the face of granulocytes. Clin Exp Immunol 2009; 157:216-24; PMID:19604261; http://dx.doi.org/10.1111/j.1365-2249.2009. 03950.x
12. Robertson CM, Perrone EE, McConnell KW, Dunne WM, Boody B, Brahmbhatt T, et al. Neutrophil depletion causes a fatal defect in murine pulmonary Staphylococcus aureus clearance. J Surg Res 2008; 150:278-85; PMID:18621398; http://dx.doi.org/10.1016/j.jss.2008.02.009
13. Voyich JM, Braughton KR, Sturdevant DE, Whitney AR, Saïd-Salim B, Porcella SF, et al. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 2005; 175:3907-19; PMID:16148137
14. Spellberg B, Ibrahim AS, Yeaman MR, Lin L, Fu Y, Avanesian V, et al. The antifungal vaccine derived from the recombinant N terminus of Als3p protects mice against the bacterium Staphylococcus aureus. Infect Immun 2008; 76:4574-80; PMID:18644876; http://dx.doi.org/10.1128/IAI.00700-08
15. Gjertsson I, Hultgren OH, Stenson M, Holmdahl R, Tarkowski A. Are B lymphocytes of importance in severe Staphylococcus aureus infections? Infect Immun 2000; 68:2431-4; PMID:10768927; http://dx.doi.org/10.1128/IAI.68.5.2431- 2434.2000
16. Gjertsson I, Nitschke L, Tarkowski A. The role of B cell CD22 expression in Staphylococcus aureus arthritis and sepsis. Microbes Infect 2004; 6:377-82; PMID:15050965; http://dx.doi.org/10.1016/j.micinf.2003.12.013
17. Zhao Y, Abdelnour A, Holmdahl R, Tarkowski A & Th International Congress of Immunology. The XID defect provides protection against Staphylococcus aureus-induced arthritis. J Immunol 1995; 155:2067-76; PMID:7636257
18. Sasaki S, Nishikawa S, Miura T, Mizuki M, Yamada K, Madarame H, et al. Interleukin-4 and interleukin-10 are involved in host resistance to Staphylococcus aureus infection through regulation of gamma interferon. Infect Immun 2000; 68:2424-30; PMID:10768926; http://dx.doi.org/10.1128/IAI.68.5.2424- 2430.2000
19. Lin L, Ibrahim AS, Xu X, Farber JM, Avanesian V, Baquir B, et al. Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLoS Pathog 2009; 5:e1000703; PMID:20041174; http://dx.doi.org/10.1371/journal.ppat.1000703
20. McLoughlin RM, Solinga RM, Rich J, Zaleski KJ, Cocchiaro JL, Risley A, et al. CD4+ T cells and CXC chemokines modulate the pathogenesis of Staphylococcus aureus wound infections. Proc Natl Acad Sci U S A 2006; 103:10408-13; PMID:16801559; http://dx.doi.org/10.1073/pnas.0508961103
21. Iwakura Y, Nakae S, Saijo S, Ishigame H. The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol Rev 2008; 226: 57-79; PMID:19161416; http://dx.doi.org/10.1111/j.1600-065X.2008. 00699.x
22. Minegishi Y, Saito M, Nagasawa M, Takada H, Hara T, Tsuchiya S, et al. Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J Exp Med 2009; 206:1291-301; PMID:19487419; http://dx.doi.org/10.1084/jem.20082767
23. Tuchscherr L, Medina E, Hussain M, Völker W, Heitmann V, Niemann S, et al. Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol Med 2011; 3:129-41; PMID:21268281; http://dx.doi.org/10.1002/emmm.201000115
24. Lin Y, Ritchea S, Logar A, Slight S, Messmer M, Rangel-Moreno J, et al. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 2009; 31:799-810; PMID:19853481; http://dx.doi.org/10.1016/j.immuni.2009.08.025
25. Roche FM, Massey R, Peacock SJ, Day NPJ, Visai L, Speziale P, et al. Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology 2003; 149:643-54; PMID:12634333; http://dx.doi.org/10.1099/mic.0.25996-0
26. Morrissey JA, Cockayne A, Hammacott J, Bishop K, Denman-Johnson A, Hill PJ, et al. Conservation, surface exposure, and in vivo expression of the Frp family of iron-regulated cell wall proteins in Staphylococcus aureus. Infect Immun 2002; 70:2399-407; PMID:11953376; http://dx.doi.org/10.1128/IAI.70.5.2399- 2407.2002
27. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, et al. Passage of heme-iron across the envelope of Staphylococcus aureus. Science 2003; 299:906-9; PMID:12574635; http://dx.doi.org/10.1126/science.1081147
28. Brown M, Kowalski R, Zorman J, Wang XM, Towne V, Zhao QJ, et al. Selection and characterization of murine monoclonal antibodies to Staphylococcus aureus iron-regulated surface determinant B with functional activity in vitro and in vivo. Clin Vaccine Immunol 2009; 16:1095-104; PMID:19553551; http://dx.doi.org/10.1128/CVI.00085-09
29. Lowy FD. Staphylococcus aureus infections. N Engl J Med 1998; 339:520-32; PMID:9709046; http://dx.doi.org/10.1056/NEJM199808203390806
30. Kuklin NA, Clark DJ, Secore S, Cook J, Cope LD, McNeely T, et al. A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model. Infect Immun 2006; 74:2215-23; PMID:16552052; http://dx.doi.org/10.1128/IAI.74.4.2215-2223.2006
31. Ebert T, Smith S, Pancari G, Clark D, Hampton R, Secore S, et al. A fully human monoclonal antibody to Staphylococcus aureus iron regulated surface determinant B (IsdB) with functional activity in vitro and in vivo. Hum Antibodies 2010; 19:113-28; PMID:21178283
32. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD, et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 2007; 8:950-7; PMID:17676044; http://dx.doi.org/10.1038/ni1497
33. Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 2007; 25:821-52;PMID:17201677; http://dx.doi.org/10.1146/annurev.immunol.25.022106. 141557
34. Crome SQ, Wang AY, Levings MK. Translational minireview series on Th17 cells: function and regulation of human T helper 17 cells in health and disease. Clin Exp Immunol 2010; 159:109-19; PMID:19912252; http://dx.doi.org/10.1111/j. 1365-2249.2009.04037.x
35. Dryla A, Prustomersky S, Gelbmann D, Hanner M, Bettinger E, Kocsis B, et al. Comparison of antibody repertoires against Staphylococcus aureus in healthy individuals and in acutely infected patients. Clin Diagn Lab Immunol 2005; 12:387-98; PMID:15753252
36. Verkaik NJ, Lebon A, de Vogel CP, Hooijkaas H, Verbrugh HA, Jaddoe VWV, et al. Induction of antibodies by Staphylococcus aureus nasal colonization in young children. Clin Microbiol Infect 2010; 16:1312-7; PMID:19832714; http://dx.doi.org/10.1111/j.1469-0691.2009.03073.x
37. Verkaik NJ, Dauwalder O, Antri K, Boubekri I, de Vogel CP, Badiou C, et al. Immunogenicity of toxins during Staphylococcus aureus infection. Clin Infect Dis 2010; 50:61-8; PMID:19947854; http://dx.doi.org/10.1086/648673
38. Verkaik NJ, Boelens HA, de Vogel CP, Tavakol M, Bode LGM, Verbrugh HA, et al. Heterogeneity of the humoral immune response following Staphylococcus aureus bacteremia. Eur J Clin Microbiol Infect Dis 2010; 29:509-18; PMID:20186449; http://dx.doi.org/10.1007/s10096-010-0888-0
39. Colque-Navarro P, Palma M, Söderquist B, Flock JI, Möllby R. Antibody responses in patients with staphylococcal septicemia against two Staphylococcus aureus fibrinogen binding proteins: clumping factor and an extracellular fibrinogen binding protein. Clin Diagn Lab Immunol 2000; 7:14-20; PMID:10618270
40. Skurnik D, Merighi M, Grout M, Gadjeva M, Maira-Litran T, Ericsson M, et al. Animal and human antibodies to distinct Staphylococcus aureus antigens mutually neutralize opsonic killing and protection in mice. J Clin Invest 2010; 120:3220-33; PMID:20739753; http://dx.doi.org/10.1172/JCI42748
41. Malley R. Antibody and cell-mediated immunity to Streptococcus pneumoniae: implications for vaccine development. Journal of Molecular Medicine (Berlin) 2010; 88.
42. Zhang Z, Clarke TB, Weiser JN. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest 2009; 119:1899-909; PMID:19509469
43. McCool TL, Weiser JN. Limited role of antibody in clearance of Streptococcus pneumoniae in a murine model of colonization. Infect Immun 2004; 72:5807-13; PMID:15385481; http://dx.doi.org/10.1128/IAI.72.10.5807-5813.2004
44. Flach CF, Östberg AK, Nilsson AT, Malefyt RdeW, Raghavan S. Proinflammatory cytokine gene expression in the stomach correlates with vaccine-induced protection against Helicobacter pylori infection in mice: an important role for interleukin-17 during the effector phase. Infect Immun 2011; 79:879-86; PMID:21078851; http://dx.doi.org/10.1128/IAI.00756-10
45. Ermak TH, Giannasca PJ, Nichols R, Myers GA, Nedrud J, Weltzin R, et al. Immunization of mice with urease vaccine affords protection against Helicobacter pylori infection in the absence of antibodies and is mediated by MHC class II-restricted responses. J Exp Med 1998; 188:2277-88; PMID:9858514; http://dx.doi.org/10.1084/jem.188.12.2277
46. Grimbacher B, Holland SM, Gallin JI, Greenberg F, Hill SC, Malech HL, et al. Hyper-IgE syndrome with recurrent infections - an autosomal dominant multisystem disorder. N Engl J Med 1999; 340:692-702; PMID:10053178; http://dx.doi.org/10.1056/NEJM199903043400904
47. Milner JD, Brenchley JM, Laurence A, Freeman AF, Hill BJ, Elias KM, et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 2008; 452:773-6; PMID:18337720; http://dx.doi.org/10. 1038/nature06764
48. Ma CS, Chew GYJ, Simpson N, Priyadarshi A, Wong M, Grimbacher B, et al. Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J Exp Med 2008; 205:1551-7; PMID:18591410; http://dx.doi.org/10.1084/jem.20080218
49. Minegishi Y, Karasuyama H. Defects in Jak-STAT-mediated cytokine signals cause hyper-IgE syndrome: lessons from a primary immunodeficiency. Int Immunol 2009; 21:105-12; PMID:19088064; http://dx.doi.org/10.1093/intimm/dxn134
50. Fischer A. Human immunodeficiency: connecting STAT3, Th17 and human mucosal immunity. Immunol Cell Biol 2008; 86:549-51; PMID:18645579; http://dx.doi.org/10.1038/icb.2008.52
51. Peck A, Mellins ED. Precarious balance: Th17 cells in host defense. Infect Immun 2010; 78:32-8; PMID:19901061; http://dx.doi.org/10.1128/IAI.00929- 09
52. Puel A, Döffinger R, Natividad A, Chrabieh M, Barcenas-Morales G, Picard C, et al. Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J Exp Med 2010; 207:291-7; PMID:20123958; http://dx.doi.org/10.1084/jem. 20091983
53. Puel A, Cypowyj S, Bustamante J, Wright JF, Liu L, Lim HK, et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011; 332:65-8; PMID:21350122; http://dx.doi.org/10.1126/ science.1200439
54. Ishigame H, Kakuta S, Nagai T, Kadoki M, Nambu A, Komiyama Y, et al. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009; 30:108-19; PMID:19144317; http://dx.doi.org/10.1016/j.immuni.2008.11.009
55. Cho JS, Pietras EM, Garcia NC, Ramos RI, Farzam DM, Monroe HR, et al. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J Clin Invest 2010; 120:1762-73; PMID:20364087; http://dx.doi.org/10.1172/JCI40891
56. Kim HK, DeDent A, Cheng AG, McAdow M, Bagnoli F, Missiakas DM, et al. IsdA and IsdB antibodies protect mice against Staphylococcus aureus abscess formation and lethal challenge. Vaccine 2010; 28:6382-92; PMID:20226248; http://dx.doi.org/10.1016/j.vaccine.2010.02.097
57. Markham RB, Pier GB, Schreiber JR. The role of cytophilic IgG3 antibody in T cell-mediated resistance to infection with the extracellular bacterium, Pseudomonas aeruginosa. J Immunol 1991; 146:316-20; PMID:1898604
58. Culkin SJ, Rhinehart-Jones T, Elkins KL. A novel role for B cells in early protective immunity to an intracellular pathogen, Francisella tularensis strain LVS. J Immunol 1997; 158:3277-84; PMID:9120284
59. Lin L, Ibrahim AS, Baquir B, Avanesian V, Fu Y, Spellberg B. Immunological surrogate marker of rAls3p-N vaccine-induced protection against Staphylococcus aureus. FEMS Immunol Med Microbiol 2009; 55:293-5; PMID:19159425; http://dx.doi.org/10.1111/j.1574-695X.2008.00531.x
60. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986; 136:2348-57; PMID:2419430
61. Spellberg B, Daum R. A new view on development of a Staphylococcus aureus vaccine: insights from mice and men. Hum Vaccin 2010; 6:857-9; PMID:20930569; http://dx.doi.org/10.4161/hv.6.10.12469
62. Fattom AI, Sarwar J, Ortiz A, Naso R. A Staphylococcus aureus capsular polysaccharide (CP) vaccine and CP-specific antibodies protect mice against bacterial challenge. Infect Immun 1996; 64:1659-65; PMID:8613375
63. Fattom AI, Horwith G, Fuller S, Propst M, Naso R. Development of StaphVAX, a polysaccharide conjugate vaccine against S. aureus infection: from the lab bench to phase III clinical trials. Vaccine 2004; 22:880-7; PMID:15040941; http://dx.doi.org/10.1016/j.vaccine.2003.11.034
64. Cook J, Hepler R, Pancari G, Kuklin N, Fan HX, Wang XM, et al. Staphylococcus aureus capsule type 8 antibodies provide inconsistent efficacy in murine models of staphylococcal infection. Hum Vaccin 2009; 5:254-63; PMID:18787395; http://dx.doi.org/10.4161/hv.5.4.6765
65. Patti JM. A humanized monoclonal antibody targeting Staphylococcus aureus. Vaccine 2004; 22(Suppl 1):S39-43; PMID:15576200; http://dx.doi.org/10. 1016/j.vaccine.2004.08.015
66. Vernachio JH, Bayer AS, Ames B, Bryant D, Prater BD, Syribeys PJ, et al. Human immunoglobulin G recognizing fibrinogen-binding surface proteins is protective against both Staphylococcus aureus and Staphylococcus epidermidis infections in vivo. Antimicrob Agents Chemother 2006; 50:511-8; PMID:16436704; http://dx.doi.org/10.1128/AAC.50.2.511-518.2006
67. Burnie JP, Matthews RC, Carter T, Beaulieu E, Donohoe M, Chapman C, et al. Identification of an immunodominant ABC transporter in methicillinresistant Staphylococcus aureus infections. Infect Immun 2000; 68:3200-9; PMID:10816464; http://dx.doi.org/10.1128/IAI.68.6.3200-3209.2000
68. Rupp ME, Holley HP, Jr., Lutz J, Dicpinigaitis PV, Woods CW, Levine DP, et al. Phase II, randomized, multicenter, double-blind, placebo-controlled trial of a polyclonal anti-Staphylococcus aureus capsular polysaccharide immune globulin in treatment of Staphylococcus aureus bacteremia. Antimicrob Agents Chemother 2007; 51:4249-54; PMID:17893153; http://dx.doi.org/10.1128/AAC.00570- 07
69. DeJonge M, Burchfield D, Bloom B, Duenas M, Walker W, Polak M, et al. Clinical trial of safety and efficacy of INH-A21 for the prevention of nosocomial staphylococcal bloodstream infection in premature infants. J Pediatr 2007; 151:260-5, 265, e1; PMID:17719934; http://dx.doi.org/10.1016/j.jpeds.2007. 04.060
70. Weems JJ, Jr., Steinberg JP, Filler S, Baddley JW, Corey GR, Sampathkumar P, et al. 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 2006; 50:2751-5; PMID:16870768; http://dx.doi.org/10.1128/AAC.00096-06
71. Chao CC, Chen SJ, Adamopoulos IE, Davis N, Hong K, Vu A, et al. Anti-IL-17A therapy protects against bone erosion in experimental models of rheumatoid arthritis. Autoimmunity 2011; 44:243-52; PMID:20925596; http://dx.doi.org/10.3109/08916934.2010.517815