1,562
Views
0
CrossRef citations to date
0
Altmetric
Review

Contribution of cryptic epitopes in designing a group A streptococcal vaccine

, &
Pages 2034-2052 | Received 21 Sep 2017, Accepted 03 Apr 2018, Published online: 14 Jun 2018

References

  • The Australian immunisation handbook. Canberra: Australian Department of Health; 2015 update.
  • Landry S, Heilman C. Future directions in vaccines: The payoffs of basic research. Health Aff (Millwood). 2005;24:758–69. doi:10.1377/hlthaff.24.3.758. PMID:15886171.
  • Good MF, Yanow SK. Cryptic epitope for antibodies should not be forgotten in vaccine design. Expert Rev Vaccines. 2016;15:675–6. doi:10.1586/14760584.2016.1154791. PMID:26881480.
  • Pandey M, Ozberk V, Calcutt A, Langshaw E, Powell J, Rivera-Hernandez T, Ho MF, Philips Z, Batzloff MR, Good MF. Streptococcal immunity is constrained by lack of immunological memory following a single episode of pyoderma. PLoS Pathog. 2016;12:e1006122. doi:10.1371/journal.ppat.1006122. PMID:28027314.
  • Carapetis JR, Steer AC, Mulholland EK, Weber M. The global burden of group A streptococcal diseases. Lancet Infect Dis. 2005;5:685–94. doi:10.1016/S1473-3099(05)70267-X. PMID:16253886.
  • Jackson SJ, Steer AC, Campbell H. Systematic Review: Estimation of global burden of non-suppurative sequelae of upper respiratory tract infection: Rheumatic fever and post-streptococcal glomerulonephritis. Trop Med Int Health. 2011;16:2–11. doi:10.1111/j.1365-3156.2010.02670.x. PMID:21371205.
  • Watkins DA, Johnson CO, Colquhoun SM, Karthikeyan G, Beaton A, Bukhman G, Forouzanfar MH, Longenecker CT, Mayosi BM, Mensah GA, et al. Global, regional, and national burden of rheumatic heart disease, 1990–2015. N Engl J Med. 2017;377:713–22. doi:10.1056/NEJMoa1603693. PMID:28834488.
  • Sika-Paotonu D, Beaton A, Raghu A, Steer A, Carapetis J. Acute rheumatic fever and rheumatic heart disease. In: Ferretti JJ, Stevens DL, Fischetti VA, editors. Streptococcus pyogenes: Basic Biology to Clinical Manifestations. Oklahoma City (OK): University of Oklahoma Health Sciences Center (c) The University of Oklahoma Health Sciences Center; 2016.
  • Guilherme L, Kohler KF, Postol E, Kalil J. Genes, autoimmunity and pathogenesis of rheumatic heart disease. Ann Pediatr Cardiol. 2011;4:13–21. doi:10.4103/0974-2069.79617. PMID:21677799.
  • Klingenberg R. The heart in rheumatic, autoimmune and inflammatory diseases. Eur Heart J. 2017;38:2985. doi:10.1093/eurheartj/ehx556. PMID:29088444.
  • Guilherme L, Kalil J. Rheumatic fever and rheumatic heart disease: Cellular mechanisms leading autoimmune reactivity and disease. J Clin Immunol. 2010;30:17–23. doi:10.1007/s10875-009-9332-6. PMID:19802690.
  • Kaplan MH, Meyeserian M. An immunological cross-reaction between group-A streptococcal cells and human heart tissue. Lancet (London, England). 1962;1:706–10. doi:10.1016/S0140-6736(62)91653-7. PMID:14453769.
  • Zabriskie JB. Mimetic relationships between group A streptococci and mammalian tissues. Adv Immunol. 1967;7:147–88. doi:10.1016/S0065-2776(08)60128-5. PMID:4868522.
  • Massell BF, Honikman LH, Amezcua J. Rheumatic fever following streptococcal vaccination. Report of three cases. JAMA. 1969;207:1115–9. doi:10.1001/jama.1969.03150190037007. PMID:5818242.
  • D'Alessandri R, Plotkin G, Kluge RM, Wittner MK, Fox EN, Dorfman A, Waldman RH. Protective studies with group A streptococcal M protein vaccine. III. Challenge of volunteers after systemic or intranasal immunization with Type 3 or Type 12 group A Streptococcus. J Infect Dis. 1978;138:712–8. doi:10.1093/infdis/138.6.712. PMID:368261.
  • Fox EN, Waldman RH, Wittner MK, Mauceri AA, Dorfman A. Protective study with a group A streptococcal M protein vaccine. Infectivity challenge of human volunteers. J Clin Invest. 1973;52:1885–92. doi:10.1172/JCI107372. PMID:4719668.
  • Revocation of status of specific products; Group A streptococcus. Direct final rule. Fed Regist. 2005;70:72197–9. PMID:16323338.
  • Cunningham MW. Rheumatic fever, autoimmunity, and molecular mimicry: The streptococcal connection. Int Rev Immunol. 2014;33:314–29. doi:10.3109/08830185.2014.917411. PMID:24892819.
  • Cunningham MW. Post-streptococcal autoimmune sequelae: Rheumatic fever and beyond. In: Ferretti JJ, Stevens DL, Fischetti VA, editors. Streptococcus pyogenes: Basic Biology to Clinical Manifestations. Oklahoma City (OK): University of Oklahoma Health Sciences Center (c) The University of Oklahoma Health Sciences Center; 2016.
  • Cunningham MW, Antone SM, Smart M, Liu R, Kosanke S. Molecular analysis of human cardiac myosin-cross-reactive B- and T-cell epitopes of the group A streptococcal M5 protein. Infect Immun. 1997;65:3913–23. PMID:9284171.
  • Bessen D, Jones KF, Fischetti VA. Evidence for two distinct classes of streptococcal M protein and their relationship to rheumatic fever. J Exp Med. 1989;169:269–83. doi:10.1084/jem.169.1.269. PMID:2642529.
  • Pruksakorn S, Currie B, Brandt E, Phornphutkul C, Hunsakunachai S, Manmontri A, Robinson JH, Kehoe MA, Galbraith A, Good MF. Identification of T cell autoepitopes that cross-react with the C-terminal segment of the M protein of group A streptococci. Int Immunol. 1994;6:1235–44. doi:10.1093/intimm/6.8.1235. PMID:7981150.
  • Quinn A, Kosanke S, Fischetti VA, Factor SM, Cunningham MW. Induction of autoimmune valvular heart disease by recombinant streptococcal m protein. Infect Immun. 2001;69:4072–8. doi:10.1128/IAI.69.6.4072-4078.2001. PMID:11349078.
  • Galvin JE, Hemric ME, Kosanke SD, Factor SM, Quinn A, Cunningham MW. Induction of myocarditis and valvulitis in lewis rats by different epitopes of cardiac myosin and its implications in rheumatic carditis. Am J Pathol. 2002;160:297–306. doi:10.1016/S0002-9440(10)64373-8. PMID:11786423.
  • Kirvan CA, Galvin JE, Hilt S, Kosanke S, Cunningham MW. Identification of streptococcal m-protein cardiopathogenic epitopes in experimental autoimmune valvulitis. J Cardiovasc Transl Res. 2014;7:172–81. doi:10.1007/s12265-013-9526-4. PMID:24346820.
  • Bisno AL. Group A streptococcal infections and acute rheumatic fever. N Engl J Med. 1991;325:783–93. doi:10.1056/NEJM199109123251106. PMID:1870652.
  • Fischetti VA. Streptococcal M protein: Molecular design and biological behavior. Clin Microbiol Rev. 1989;2:285–314. doi:10.1128/CMR.2.3.285. PMID:2670192.
  • Johnson DR, Stevens DL, Kaplan EL. Epidemiologic analysis of group A streptococcal serotypes associated with severe systemic infections, rheumatic fever, or uncomplicated pharyngitis. J Infect Dis. 1992;166:374–82. doi:10.1093/infdis/166.2.374. PMID:1634809.
  • Lee GM, Wessels MR. Changing epidemiology of acute rheumatic fever in the United States. Clin Infect Dis. 2006;42:448–50. doi:10.1086/499817. PMID:16421786.
  • Shulman ST, Stollerman G, Beall B, Dale JB, Tanz RR. Temporal changes in streptococcal M protein types and the near-disappearance of acute rheumatic fever in the United States. Clin Infect Dis. 2006;42:441–7. doi:10.1086/499812. PMID:16421785.
  • Wolfe RR. Incidence of acute rheumatic fever: A persistent dilemma. Pediatrics. 2000;105:1375. doi:10.1542/peds.105.6.1375a. PMID:10877673.
  • Williamson DA, Smeesters PR, Steer AC, Steemson JD, Ng AC, Proft T, et al. M-protein analysis of streptococcus pyogenes isolates associated with acute rheumatic fever in New Zealand. J Clin Microbiol. 2015;53:3618–20. doi:10.1128/JCM.02129-15. PMID:26292296.
  • Beall B, Facklam R, Thompson T. Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci. J Clin Microbiol. 1996;34:953–8. PMID:8815115.
  • Smeesters PR, McMillan DJ, Sriprakash KS. The streptococcal M protein: A highly versatile molecule. Trends Microbiol. 2010;18:275–82. doi:10.1016/j.tim.2010.02.007. PMID:20347595.
  • Smeesters PR, Mardulyn P, Vergison A, Leplae R, Van Melderen L. Genetic diversity of group A streptococcus m protein: Implications for typing and vaccine development. Vaccine. 2008;26:5835–42. doi:10.1016/j.vaccine.2008.08.037. PMID:18789365.
  • Kuttner AG, Lenert TF. The occurrence of bacteriostatic properties in the blood of patients after recovery from streptococcal pharyngitis. J Clin Invest. 1944;23:151–61. doi:10.1172/JCI101478. PMID:16695089.
  • Rothbard S. Bacteriostatic effect of human sera on group a streptococci: Type-specific antibodies in sera of patients convalescing from group a streptococcal pharyngitis. J Exp Med. 1945;82:93–106. doi:10.1084/jem.82.2.93. PMID:19871491.
  • Wannamaker LW, Denny FW, Perry WD, Siegel AC, Rammelkamp CH, Jr. Studies on immunity to streptococcal infections in man. Am J Dis Child. 1953;86:347–8.
  • Lancefield RC. Persistence of type-specific antibodies in man following infection with group A streptococci. J Exp Med. 1959;110:271–92. doi:10.1084/jem.110.2.271. PMID:13673139.
  • Pandey M, Ozberk V, Langshaw EL, Calcutt A, Powell J, Batzloff RM, Rivera-Hernandez T, Good MF. Skin infection boosts memory B-cells specific for a cryptic vaccine epitope of group A streptococcus and broadens the immune response to enhance vaccine efficacy npj Vaccines. Vaccine. 2018;3.
  • Steer AC, Dale JB, Carapetis JR. Progress toward a global group a streptococcal vaccine. Pediatr Infect Dis J. 2013;32:180–2. doi:10.1097/INF.0b013e318281da11. PMID:23328823.
  • Dale JB. Multivalent group A streptococcal vaccine designed to optimize the immunogenicity of six tandem M protein fragments. Vaccine. 1999;17:193–200. doi:10.1016/S0264-410X(98)00150-9. PMID:9987154.
  • Dale JB, Penfound TA, Chiang EY, Walton WJ. New 30-valent M protein-based vaccine evokes cross-opsonic antibodies against non-vaccine serotypes of group A streptococci. Vaccine. 2011;29:8175–8. doi:10.1016/j.vaccine.2011.09.005. PMID:21920403.
  • Kotloff KL, Corretti M, Palmer K, Campbell JD, Reddish MA, Hu MC, et al. Safety and immunogenicity of a recombinant multivalent group a streptococcal vaccine in healthy adults: Phase 1 trial. JAMA. 2004;292:709–15. doi:10.1001/jama.292.6.709. PMID:15304468.
  • McNeil SA, Halperin SA, Langley JM, Smith B, Warren A, Sharratt GP, Baxendale DM, Reddish MA, Hu MC, Stroop SD, et al. Safety and immunogenicity of 26-valent group a streptococcus vaccine in healthy adult volunteers. Clin Infect Dis. 2005;41:1114–22. doi:10.1086/444458. PMID:16163629.
  • Guilherme L, Fae KC, Higa F, Chaves L, Oshiro SE, Freschi de Barros S, Puschel C, Juliano MA, Tanaka AC, Spina G, et al. Towards a vaccine against rheumatic fever. Clin Dev Immunol. 2006;13:125–32. doi:10.1080/17402520600877026. PMID:17162355.
  • McMillan DJ, Dreze PA, Vu T, Bessen DE, Guglielmini J, Steer AC, Carapetis JR, Van Melderen L, Sriprakash KS, Smeesters PR. Updated model of group A Streptococcus M proteins based on a comprehensive worldwide study. Clin Microbiol Infect. 2013;19:E222–9. doi:10.1111/1469-0691.12134. PMID:23464795.
  • Batzloff MR, Hayman WA, Davies MR, Zeng M, Pruksakorn S, Brandt ER, et al. Protection against group A streptococcus by immunization with J8-diphtheria toxoid: Contribution of J8- and diphtheria toxoid-specific antibodies to protection. J Infect Dis. 2003;187:1598–608. doi:10.1086/374800. PMID:12721940.
  • Turner CE, Kurupati P, Wiles S, Edwards RJ, Sriskandan S. Impact of immunization against SpyCEP during invasive disease with two streptococcal species: Streptococcus pyogenes and streptococcus equi. Vaccine. 2009;27:4923–9. doi:10.1016/j.vaccine.2009.06.042. PMID:19563892.
  • Cleary PP, Matsuka YV, Huynh T, Lam H, Olmsted SB. Immunization with C5a peptidase from either group A or B streptococci enhances clearance of group A streptococci from intranasally infected mice. Vaccine. 2004;22:4332–41. doi:10.1016/j.vaccine.2004.04.030. PMID:15474726.
  • Sabharwal H, Michon F, Nelson D, Dong W, Fuchs K, Manjarrez RC, Sarkar A, Uitz C, Viteri-Jackson A, Suarez RS, et al. Group A streptococcus (GAS) carbohydrate as an immunogen for protection against GAS infection. J Infect Dis. 2006;193:129–35. doi:10.1086/498618. PMID:16323141.
  • Salvadori LG, Blake MS, McCarty M, Tai JY, Zabriskie JB. Group A streptococcus-liposome ELISA antibody titers to group A polysaccharide and opsonophagocytic capabilities of the antibodies. J Infect Dis. 1995;171:593–600. doi:10.1093/infdis/171.3.593. PMID:7876606.
  • Hu MC, Walls MA, Stroop SD, Reddish MA, Beall B, Dale JB. Immunogenicity of a 26-valent group A streptococcal vaccine. Infect Immun. 2002;70:2171–7. doi:10.1128/IAI.70.4.2171-2177.2002. PMID:11895984.
  • Steer AC, Law I, Matatolu L, Beall BW, Carapetis JR. Global emm type distribution of group A streptococci: Systematic review and implications for vaccine development. Lancet Infect Dis. 2009;9:611–6. doi:10.1016/S1473-3099(09)70178-1. PMID:19778763.
  • McNeil SA HS, Langley JM, Smith B, Warren A, Baxendale DM, Sharratt GP, et al. A double-blind, randomized phase II trial of the safety and immunogenicity of 26-valent group A streptococcus vaccine in healthy adults. Int Cong Ser. 2006;1289:303–6. doi:10.1016/j.ics.2005.12.002.
  • Dale JB, Batzloff MR, Cleary PP, Courtney HS, Good MF, Grandi G, Halperin S, Margarit IY, McNeil S, Pandey M et al. Current approaches to group A streptococcal vaccine development. In: Ferretti JJ, Stevens DL, Fischetti VA, editors. Streptococcus pyogenes: Basic Biology to Clinical Manifestations. Oklahoma City (OK): University of Oklahoma Health Sciences Center (c) The University of Oklahoma Health Sciences Center; 2016.
  • Dale JB, Penfound TA, Tamboura B, Sow SO, Nataro JP, Tapia M, Kotloff KL. Potential coverage of a multivalent M protein-based group A streptococcal vaccine. Vaccine. 2013;31:1576–81. doi:10.1016/j.vaccine.2013.01.019. PMID:23375817.
  • Dale JB, Smeesters PR, Courtney HS, Penfound TA, Hohn CM, Smith JC, Baudry JY. Structure-based design of broadly protective group a streptococcal M protein-based vaccines. Vaccine. 2017;35:19–26. doi:10.1016/j.vaccine.2016.11.065. PMID:27890396.
  • Guilherme L, Postol E, Freschi de Barros S, Higa F, Alencar R, Lastre M, Zayas C, Puschel CR, Silva WR, Sa-Rocha LC, et al. A vaccine against S. pyogenes: Design and experimental immune response. Methods. 2009;49:316–21. doi:10.1016/j.ymeth.2009.03.024. PMID:19409999.
  • Guerino MT, Postol E, Demarchi LM, Martins CO, Mundel LR, Kalil J, Guilherme L. HLA class II transgenic mice develop a safe and long lasting immune response against StreptInCor, an anti-group A streptococcus vaccine candidate. Vaccine. 2011;29:8250–6. doi:10.1016/j.vaccine.2011.08.113. PMID:21907752.
  • Postol E, Alencar R, Higa FT, Freschi de Barros S, Demarchi LM, Kalil J, Guilherme L. StreptInCor: A candidate vaccine epitope against S. pyogenes infections induces protection in outbred mice. PLoS One. 2013;8:e60969. doi:10.1371/journal.pone.0060969. PMID:23593359.
  • De Amicis KM, Freschi de Barros S, Alencar RE, Postol E, Martins Cde O, Arcuri HA, Goulart C, Kalil J, Guilherme L. Analysis of the coverage capacity of the StreptInCor candidate vaccine against Streptococcus pyogenes. Vaccine. 2014;32:4104–10. doi:10.1016/j.vaccine.2013.08.043. PMID:23994376.
  • McNeilly C, Cosh S, Vu T, Nichols J, Henningham A, Hofmann A, Fane A, Smeesters PR, Rush CM, Hafner LM, et al. Predicted Coverage and Immuno-Safety of a Recombinant C-Repeat Region Based Streptococcus pyogenes Vaccine Candidate. PLoS One. 2016;11:e0156639. doi:10.1371/journal.pone.0156639. PMID:27310707.
  • Brandt ER, Sriprakash KS, Hobb RI, Hayman WA, Zeng W, Batzloff MR, Jackson DC, Good MF. New multi-determinant strategy for a group A streptococcal vaccine designed for the Australian Aboriginal population. Nat Med. 2000;6:455–9. doi:10.1038/74719. PMID:10742155.
  • Pandey M, Langshaw E, Hartas J, Lam A, Batzloff MR, Good MF. A synthetic M protein peptide synergizes with a CXC chemokine protease to induce vaccine-mediated protection against virulent streptococcal pyoderma and bacteremia. J Immunol (Baltimore, Md: 1950). 2015;194:5915–25. doi:10.4049/jimmunol.1500157.
  • Pandey M, Mortensen R, Calcutt A, Powell J, Batzloff MR, Dietrich J, Good MF. Combinatorial Synthetic Peptide Vaccine Strategy Protects against Hypervirulent CovR/S Mutant Streptococci. J Immunol (Baltimore, Md: 1950). 2016;196:3364–74. doi:10.4049/jimmunol.1501994.
  • Pandey M, Powell J, Calcutt A, Zaman M, Phillips ZN, Ho MF, Batzloff MR, Good MF. Physicochemical characterisation, immunogenicity and protective efficacy of a lead streptococcal vaccine: Progress towards Phase I trial. Sci Rep. 2017;7:13786. doi:10.1038/s41598-017-14157-7. PMID:29062085.
  • Rodriguez-Ortega MJ, Norais N, Bensi G, Liberatori S, Capo S, Mora M, Scarselli M, Doro F, Ferrari G, Garaguso I, et al. Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat Biotechnol. 2006;24:191–7. doi:10.1038/nbt1179. PMID:16415855.
  • Cheng Q, Stafslien D, Purushothaman SS, Cleary P. The group B streptococcal C5a peptidase is both a specific protease and an invasin. Infect Immun. 2002;70:2408–13. doi:10.1128/IAI.70.5.2408-2413.2002. PMID:11953377.
  • Ji Y, Carlson B, Kondagunta A, Cleary PP. Intranasal immunization with C5a peptidase prevents nasopharyngeal colonization of mice by the group A Streptococcus. Infect Immun. 1997;65:2080–7. PMID:9169735.
  • Ji Y, McLandsborough L, Kondagunta A, Cleary PP. C5a peptidase alters clearance and trafficking of group A streptococci by infected mice. Infect Immun. 1996;64:503–10. PMID:8550199.
  • Bronze MS, Beachey EH, Dale JB. Protective and heart-crossreactive epitopes located within the NH2 terminus of type 19 streptococcal M protein. J Exp Med. 1988;167:1849–59. doi:10.1084/jem.167.6.1849. PMID:2455015.
  • Guzman CA, Talay SR, Molinari G, Medina E, Chhatwal GS. Protective immune response against Streptococcus pyogenes in mice after intranasal vaccination with the fibronectin-binding protein SfbI. J Infect Dis. 1999;179:901–6. doi:10.1086/314655. PMID:10068585.
  • Roggiani M, Stoehr JA, Olmsted SB, Matsuka YV, Pillai S, Ohlendorf DH, Schlievert PM. Toxoids of streptococcal pyrogenic exotoxin A are protective in rabbit models of streptococcal toxic shock syndrome. Infect Immun. 2000;68:5011–7. doi:10.1128/IAI.68.9.5011-5017.2000. PMID:10948118.
  • Schlievert PM, Assimacopoulos AP, Cleary PP. Severe invasive group A streptococcal disease: Clinical description and mechanisms of pathogenesis. J Lab Clin Med. 1996;127:13–22. doi:10.1016/S0022-2143(96)90161-4. PMID:8592092.
  • Kuo CF, Wu JJ, Lin KY, Tsai PJ, Lee SC, Jin YT, Lei HY, Lin YS. Role of streptococcal pyrogenic exotoxin B in the mouse model of group A streptococcal infection. Infect Immun. 1998;66:3931–5. PMID:9673282.
  • McCormick JK, Tripp TJ, Olmsted SB, Matsuka YV, Gahr PJ, Ohlendorf DH, Schlievert PM. Development of streptococcal pyrogenic exotoxin C vaccine toxoids that are protective in the rabbit model of toxic shock syndrome. J Immunol (Baltimore, Md: 1950). 2000;165:2306–12. doi:10.4049/jimmunol.165.4.2306.
  • Courtney HS, Hasty DL, Dale JB. Serum opacity factor (SOF) of Streptococcus pyogenes evokes antibodies that opsonize homologous and heterologous SOF-positive serotypes of group A streptococci. Infect Immun. 2003;71:5097–103. doi:10.1128/IAI.71.9.5097-5103.2003. PMID:12933852.
  • Mora M, Bensi G, Capo S, Falugi F, Zingaretti C, Manetti AG, Maggi T, Taddei AR, Grandi G, Telford JL. Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. PNAS. 2005;102:15641–6. doi:10.1073/pnas.0507808102. PMID:16223875.
  • van Sorge NM, Cole JN, Kuipers K, Henningham A, Aziz RK, Kasirer-Friede A, Lin L, Berends ETM, Davies MR, Dougan G, et al. The classical lancefield antigen of group a Streptococcus is a virulence determinant with implications for vaccine design. Cell Host Microbe. 2014;15:729–40. doi:10.1016/j.chom.2014.05.009. PMID:24922575.
  • Cunningham MW. Pathogenesis of group A streptococcal infections. Clin Microbiol Rev. 2000;13:470–511. doi:10.1128/CMR.13.3.470-511.2000. PMID:10885988.
  • Bessen D, Fischetti VA. Influence of intranasal immunization with synthetic peptides corresponding to conserved epitopes of M protein on mucosal colonization by group A streptococci. Infect Immun. 1988;56:2666–72. PMID:2458320.
  • Jones KF, Fischetti VA. The importance of the location of antibody binding on the M6 protein for opsonization and phagocytosis of group A M6 streptococci. J Exp Med. 1988;167:1114–23. doi:10.1084/jem.167.3.1114. PMID:2450950.
  • Pruksakorn S, Currie B, Brandt E, Martin D, Galbraith A, Phornphutkul C, Hunsakunachai S, Manmontri A, Good MF. Towards a vaccine for rheumatic fever: Identification of a conserved target epitope on M protein of group A streptococci. Lancet (London, England). 1994;344:639–42. doi:10.1016/S0140-6736(94)92083-4. PMID:7520963.
  • Good MF, Pandey M, Batzloff MR, Tyrrell GJ. Strategic development of the conserved region of the M protein and other candidates as vaccines to prevent infection with group A streptococci. Expert Rev Vaccines. 2015;14:1459–70. doi:10.1586/14760584.2015.1081817. PMID:26485214.
  • Brandt ER, Hayman WA, Currie B, Carapetis J, Wood Y, Jackson DC, Cooper J, Melrose WD, Saul AJ, Good MF. Opsonic human antibodies from an endemic population specific for a conserved epitope on the M protein of group A streptococci. Immunology. 1996;89:331–7. doi:10.1046/j.1365-2567.1996.d01-754.x. PMID:8958044.
  • Fae KC, da Silva DD, Oshiro SE, Tanaka AC, Pomerantzeff PM, Douay C, Charron D, Toubert A, Cunningham MW, Kalil J, et al. Mimicry in recognition of cardiac myosin peptides by heart-intralesional T cell clones from rheumatic heart disease. J Immunol (Baltimore, Md: 1950). 2006;176:5662–70. doi:10.4049/jimmunol.176.9.5662.
  • Guilherme L, Fae KC, Oshiro SE, Tanaka AC, Pomerantzeff PM, Kalil J. Rheumatic fever: How S. pyogenes-primed peripheral T cells trigger heart valve lesions. Ann N Y Acad Sci. 2005;1051:132–40. doi:10.1196/annals.1361.054. PMID:16126952.
  • Relf WA, Cooper J, Brandt ER, Hayman WA, Anders RF, Pruksakorn S, Currie B, Saul A, Good MF. Mapping a conserved conformational epitope from the M protein of group A streptococci. Pept Res. 1996;9:12–20. PMID:8727479.
  • Brandt ER, Hayman WA, Currie B, Pruksakorn S, Good MF. Human antibodies to the conserved region of the M protein: Opsonization of heterologous strains of group A streptococci. Vaccine. 1997;15:1805–12. doi:10.1016/S0264-410X(97)00178-3. PMID:9364687.
  • Hayman WA, Brandt ER, Relf WA, Cooper J, Saul A, Good MF. Mapping the minimal murine T cell and B cell epitopes within a peptide vaccine candidate from the conserved region of the M protein of group A streptococcus. Int Immunol. 1997;9:1723–33. doi:10.1093/intimm/9.11.1723. PMID:9418133.
  • Batzloff MR, Fane A, Gorton D, Pandey M, Rivera-Hernandez T, Calcutt A, Yeung G, Hartas J, Johnson L, Rush CM, et al. Preclinical immunogenicity and safety of a Group A streptococcal M protein-based vaccine candidate. Hum Vaccin Immunother. 2016;12:3089–96. doi:10.1080/21645515.2016.1222999. PMID:27541593.
  • Pandey M, Wykes MN, Hartas J, Good MF, Batzloff MR. Long-term antibody memory induced by synthetic peptide vaccination is protective against Streptococcus pyogenes infection and is independent of memory T cell help. J Immunol (Baltimore, Md: 1950). 2013;190:2692–701. doi:10.4049/jimmunol.1202333.
  • Batzloff MR, Yan H, Davies MR, Hartas J, Lowell GH, White G, Burt DS, Leanderson T, Good MF. Toward the development of an antidisease, transmission-blocking intranasal vaccine for group a streptococcus. J Infect Dis. 2005;192:1450–5. doi:10.1086/466528. PMID:16170764.
  • Bessen D, Fischetti VA. Passive acquired mucosal immunity to group A streptococci by secretory immunoglobulin A. J Exp Med. 1988;167:1945–50. doi:10.1084/jem.167.6.1945. PMID:3290383.
  • Zaman M, Ozberk V, Langshaw EL, McPhun V, Powell JL, Phillips ZN, Ho MF, Calcutt A, Batzloff MR, Toth I, et al. Novel platform technology for modular mucosal vaccine that protects against streptococcus. Sci Rep. 2016;6:39274. doi:10.1038/srep39274. PMID:27976706.
  • Olive C, Clair T, Yarwood P, Good MF. Protection of mice from group A streptococcal infection by intranasal immunisation with a peptide vaccine that contains a conserved M protein B cell epitope and lacks a T cell autoepitope. Vaccine. 2002;20:2816–25. doi:10.1016/S0264-410X(02)00205-0. PMID:12034109.
  • Batzloff MR, Hartas J, Zeng W, Jackson DC, Good MF. Intranasal vaccination with a lipopeptide containing a conformationally constrained conserved minimal peptide, a universal T cell epitope, and a self-adjuvanting lipid protects mice from group A streptococcus challenge and reduces throat colonization. J Infect Dis. 2006;194:325–30. doi:10.1086/505146. PMID:16826480.
  • Sanderson-Smith M, De Oliveira DM, Guglielmini J, McMillan DJ, Vu T, Holien JK, Henningham A, Steer AC, Bessen DE, Dale JB, et al. A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development. J Infect Dis. 2014;210:1325–38. doi:10.1093/infdis/jiu260. PMID:24799598.
  • Turner P, Ngeth P, Turner C, Sao S, Day NP, Baker C, Steer AC, Smeesters PR. Molecular Epidemiology of Group A Streptococcus Infections in Cambodian Children, 2007–2012. Pediatr Infect Dis J. 2015;34:1414–5. doi:10.1097/INF.0000000000000878. PMID:26780027.
  • Rattanavong S, Dance DA, Davong V, Baker C, Frost H, Phetsouvanh R, Vongsouvath M, Newton PN, Steer AC, Smeesters PR. Group A streptococcal strains isolated in Lao People's Democratic Republic from 2004 to 2013. Epidemiol Infect. 2016;144:1770–3. doi:10.1017/S0950268815002927. PMID:26645633.
  • Churchward G. The two faces of Janus: Virulence gene regulation by CovR/S in group A streptococci. Mol Microbiol. 2007;64:34–41. doi:10.1111/j.1365-2958.2007.05649.x. PMID:17376070.
  • Hollands A, Pence MA, Timmer AM, Osvath SR, Turnbull L, Whitchurch CB, Walker MJ, Nizet V. Genetic switch to hypervirulence reduces colonization phenotypes of the globally disseminated group A streptococcus M1T1 clone. J Infect Dis. 2010;202:11–9. doi:10.1086/653124. PMID:20507231.
  • Turner CE, Kurupati P, Jones MD, Edwards RJ, Sriskandan S. Emerging role of the interleukin-8 cleaving enzyme SpyCEP in clinical Streptococcus pyogenes infection. J Infect Dis. 2009;200:555–63. doi:10.1086/603541. PMID:19591574.
  • Edwards RJ, Taylor GW, Ferguson M, Murray S, Rendell N, Wrigley A, Bai Z, Boyle J, Finney SJ, Jones A, et al. Specific C-terminal cleavage and inactivation of interleukin-8 by invasive disease isolates of Streptococcus pyogenes. J Infect Dis. 2005;192:783–90. doi:10.1086/432485. PMID:16088827.
  • Zinkernagel AS, Timmer AM, Pence MA, Locke JB, Buchanan JT, Turner CE, Mishalian I, Sriskandan S, Hanski E, Nizet V. The IL-8 protease SpyCEP/ScpC of group A Streptococcus promotes resistance to neutrophil killing. Cell Host & Microbe. 2008;4:170–8. doi:10.1016/j.chom.2008.07.002.
  • Sumby P, Zhang S, Whitney AR, Falugi F, Grandi G, Graviss EA, Deleo FR, Musser JM. A chemokine-degrading extracellular protease made by group A Streptococcus alters pathogenesis by enhancing evasion of the innate immune response. Infect Immun. 2008;76:978–85. doi:10.1128/IAI.01354-07. PMID:18174342.
  • Alam FM, Bateman C, Turner CE, Wiles S, Sriskandan S. Non-invasive monitoring of Streptococcus pyogenes vaccine efficacy using biophotonic imaging. PLoS One. 2013;8:e82123. doi:10.1371/journal.pone.0082123. PMID:24278474.
  • Henningham A, Gillen CM, Walker MJ. Group a streptococcal vaccine candidates: Potential for the development of a human vaccine. Curr Top Microbiol Immunol. 2013;368:207–42. PMID:23250780.
  • Perepared for WHO PD-VAC. Status of vaccine research and development of vaccines for streptococcus pyogenes.
  • Nooh MM, El-Gengehi N, Kansal R, David CS, Kotb M. HLA transgenic mice provide evidence for a direct and dominant role of HLA class II variation in modulating the severity of streptococcal sepsis. J Immunol (Baltimore, Md: 1950). 2007;178:3076–83. doi:10.4049/jimmunol.178.5.3076.
  • Rivera-Hernandez T, Pandey M, Henningham A, Cole J, Choudhury B, Cork AJ, Gillen CM, Ghaffar KA, West NP, Silvestri G, et al. Differing efficacies of lead group A streptococcal vaccine candidates and full-length M protein in cutaneous and invasive disease models. mBio. 2016;7.
  • Skinner JM, Caro-Aguilar IC, Payne AM, Indrawati L, Fontenot J, Heinrichs JH. Comparison of rhesus and cynomolgus macaques in a Streptococcus pyogenes infection model for vaccine evaluation. Microb Pathog. 2011;50:39–47. doi:10.1016/j.micpath.2010.10.004. PMID:21035535.
  • Virtaneva K, Porcella SF, Graham MR, Ireland RM, Johnson CA, Ricklefs SM, Babar I, Parkins LD, Romero RA, Corn GJ, et al. Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. PNAS. 2005;102:9014–9. doi:10.1073/pnas.0503671102. PMID:15956184.
  • Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. PNAS. 2013;110:3507–12. doi:10.1073/pnas.1222878110. PMID:23401516.
  • Takao K, Miyakawa T. Genomic responses in mouse models greatly mimic human inflammatory diseases. PNAS. 2015;112:1167–72. doi:10.1073/pnas.1401965111. PMID:25092317.
  • Justice MJ, Dhillon P. Using the mouse to model human disease: Increasing validity and reproducibility. Dis Models Mech. 2016;9:101–3. doi:10.1242/dmm.024547.
  • Osuchowski MF, Remick DG, Lederer JA, Lang CH, Aasen AO, Aibiki M, Azevedo LC, Bahrami S, Boros M, Cooney R, et al. Abandon the mouse research ship? Not just yet! Shock (Augusta, Ga). 2014;41:463–75. doi:10.1097/SHK.0000000000000153. PMID:24569509.
  • Rathore D, Sacci JB, de la Vega P, McCutchan TF. Binding and invasion of liver cells by Plasmodium falciparum sporozoites. Essential involvement of the amino terminus of circumsporozoite protein. J Biol Chem. 2002;277:7092–8. doi:10.1074/jbc.M106862200. PMID:11751898.
  • Rathore D, Nagarkatti R, Jani D, Chattopadhyay R, de la Vega P, Kumar S, McCutchan TF. An immunologically cryptic epitope of Plasmodium falciparum circumsporozoite protein facilitates liver cell recognition and induces protective antibodies that block liver cell invasion. J Biol Chem. 2005;280:20524–9. doi:10.1074/jbc.M414254200. PMID:15781464.
  • Little SF, Ivins BE, Fellows PF, Friedlander AM. Passive protection by polyclonal antibodies against Bacillus anthracis infection in guinea pigs. Infect Immun. 1997;65:5171–5. PMID:9393812.
  • Pezard C, Weber M, Sirard JC, Berche P, Mock M. Protective immunity induced by Bacillus anthracis toxin-deficient strains. Infect Immun. 1995;63:1369–72. PMID:7890396.
  • Turnbull PC, Leppla SH, Broster MG, Quinn CP, Melling J. Antibodies to anthrax toxin in humans and guinea pigs and their relevance to protective immunity. Med Microbiol Immunol (Berl). 1988;177:293–303. doi:10.1007/BF00189414.
  • Demicheli V, Rivetti D, Deeks JJ, Jefferson T, Pratt M. The effectiveness and safety of vaccines against human anthrax: A systematic review. Vaccine. 1998;16:880–4. doi:10.1016/S0264-410X(98)00023-1. PMID:9682332.
  • Institute of Medicine Committee to Assess the S. Efficacy of the Anthrax V. In: Joellenbeck LM, Zwanziger LL, Durch JS, Strom BL, editors. The Anthrax Vaccine: Is It Safe? Does It Work? Washington, (DC): National Academies Press (US) Copyright 2002 by the National Academy of Sciences. All rights reserved; 2002.
  • Pittman PR, Kim-Ahn G, Pifat DY, Coonan K, Gibbs P, Little S, Pace-Templeton JG, Myers R, Parker GW, Friedlander AM. Anthrax vaccine: Immunogenicity and safety of a dose-reduction, route-change comparison study in humans. Vaccine. 2002;20:1412–20. doi:10.1016/S0264-410X(01)00462-5. PMID:11818160.
  • Albrecht MT, Li H, Williamson ED, LeButt CS, Flick-Smith HC, Quinn CP, Westra H, Galloway D, Mateczun A, Goldman S, et al. Human monoclonal antibodies against anthrax lethal factor and protective antigen act independently to protect against Bacillus anthracis infection and enhance endogenous immunity to anthrax. Infect Immun. 2007;75:5425–33. doi:10.1128/IAI.00261-07. PMID:17646360.
  • Oscherwitz J, Yu F, Jacobs JL, Liu TH, Johnson PR, Cease KB. Synthetic peptide vaccine targeting a cryptic neutralizing epitope in domain 2 of Bacillus anthracis protective antigen. Infect Immun. 2009;77:3380–8. doi:10.1128/IAI.00358-09. PMID:19487468.
  • Guilherme L, Ferreira FM, Kohler KF, Postol E, Kalil J. A vaccine against Streptococcus pyogenes: The potential to prevent rheumatic fever and rheumatic heart disease. Am J Cardiovasc Drugs. 2013;13:1–4. doi:10.1007/s40256-013-0005-8. PMID:23355360.
  • Azmi F, Ahmad Fuaad AA, Giddam AK, Batzloff MR, Good MF, Skwarczynski M, Toth I, et al. Self-adjuvanting vaccine against group A streptococcus: Application of fibrillized peptide and immunostimulatory lipid as adjuvant. Bioorg Med Chem. 2014;22:6401–8. doi:10.1016/j.bmc.2014.09.042. PMID:25438764.
  • Kirvan CA, Swedo SE, Heuser JS, Cunningham MW. Mimicry and autoantibody-mediated neuronal cell signaling in Sydenham chorea. Nat Med. 2003;9:914–20. doi:10.1038/nm892. PMID:12819778.
  • Shikhman AR, Cunningham MW. Immunological mimicry between N-acetyl-beta-D-glucosamine and cytokeratin peptides. Evidence for a microbially driven anti-keratin antibody response. J Immunol (Baltimore, Md: 1950). 1994;152:4375–87.
  • Shikhman AR, Greenspan NS, Cunningham MW. Cytokeratin peptide SFGSGFGGGY mimics N-acetyl-beta-D-glucosamine in reaction with antibodies and lectins, and induces in vivo anti-carbohydrate antibody response. J Immunol (Baltimore, Md: 1950). 1994;153:5593–606.
  • Simpson WJ, Musser JM, Cleary PP. Evidence consistent with horizontal transfer of the gene (emm12) encoding serotype M12 protein between group A and group G pathogenic streptococci. Infect Immun. 1992;60:1890–3. PMID:1563779.
  • Kawabata S, Kunitomo E, Terao Y, Nakagawa I, Kikuchi K, Totsuka K, Hamada, S. Systemic and mucosal immunizations with fibronectin-binding protein FBP54 induce protective immune responses against Streptococcus pyogenes challenge in mice. Infect Immun. 2001;69:924–30. doi:10.1128/IAI.69.2.924-930.2001. PMID:11159987.
  • McArthur J, Medina E, Mueller A, Chin J, Currie BJ, Sriprakash KS, Talay SR, Chhatwal GS, Walker MJ. Intranasal vaccination with streptococcal fibronectin binding protein Sfb1 fails to prevent growth and dissemination of Streptococcus pyogenes in a murine skin infection model. Infect Immun. 2004;72:7342–5. doi:10.1128/IAI.72.12.7342-7345.2004. PMID:15557665.
  • Goodfellow AM, Hibble M, Talay SR, Kreikemeyer B, Currie BJ, Sriprakash KS, Chhatwal GS. Distribution and antigenicity of fibronectin binding proteins (SfbI and SfbII) of Streptococcus pyogenes clinical isolates from the northern territory, Australia. J Clin Microbiol. 2000;38:389–92. PMID:10618121.
  • Bensi G, Mora M, Tuscano G, Biagini M, Chiarot E, Bombaci M, Capo S, Falugi F, Manetti AG, Donato P, et al. Multi high-throughput approach for highly selective identification of vaccine candidates: The Group A Streptococcus case. Mol Cell Proteomics. 2012;11:M111. 015693. doi:10.1074/mcp.M111.015693. PMID:22286755.
  • Reid SD, Green NM, Sylva GL, Voyich JM, Stenseth ET, DeLeo FR, Palzkill T, Low DE, Hill HR, Musser JM. Postgenomic analysis of four novel antigens of group a streptococcus: Growth phase-dependent gene transcription and human serologic response. J Bacteriol. 2002;184:6316–24. doi:10.1128/JB.184.22.6316-6324.2002. PMID:12399501.
  • Fritzer A, Senn BM, Minh DB, Hanner M, Gelbmann D, Noiges B, Henics T, Schulze K, Guzman CA, Goodacre J, et al. Novel conserved group A streptococcal proteins identified by the antigenome technology as vaccine candidates for a non-M protein-based vaccine. Infect Immun. 2010;78:4051–67. doi:10.1128/IAI.00295-10. PMID:20624906.
  • Reglinski M, Lynskey NN, Choi YJ, Edwards RJ, Sriskandan S. Development of a multicomponent vaccine for Streptococcus pyogenes based on the antigenic targets of IVIG. J Infect. 2016;72:450–9. doi:10.1016/j.jinf.2016.02.002. PMID:26880087.
  • Henningham A, Chiarot E, Gillen CM, Cole JN, Rohde M, Fulde M, Ramachandran V, Cork AJ, Hartas J, Magor G, et al. Conserved anchorless surface proteins as group A streptococcal vaccine candidates. J Mol Med. 2012;90:1197–207. doi:10.1007/s00109-012-0897-9. PMID:22527883.
  • Olive C, Batzloff M, Horvath A, Clair T, Yarwood P, Toth I, Good MF. Group A streptococcal vaccine delivery by immunization with a self-adjuvanting M protein-based lipid core peptide construct. Indian J Med Res. 2004;119(Suppl):88–94. PMID:15232170.
  • Olive C, Batzloff MR, Horvath A, Wong A, Clair T, Yarwood P, Toth I, Good MF. A lipid core peptide construct containing a conserved region determinant of the group A streptococcal M protein elicits heterologous opsonic antibodies. Infect Immun. 2002;70:2734–8. doi:10.1128/IAI.70.5.2734-2738.2002. PMID:11953422.
  • Olive C, Ho MF, Dyer J, Lincoln D, Barozzi N, Toth I, Good MF. Immunization with a tetraepitopic lipid core peptide vaccine construct induces broadly protective immune responses against group A streptococcus. J Infect Dis. 2006;193:1666–76. doi:10.1086/504266. PMID:16703510.
  • Olive C, Sun HK, Ho MF, Dyer J, Horvath A, Toth I, Good MF. Intranasal administration is an effective mucosal vaccine delivery route for self-adjuvanting lipid core peptides targeting the group A streptococcal M protein. J Infect Dis. 2006;194:316–24. doi:10.1086/505580. PMID:16826479.