A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development

Journal of Infectious Diseases

Volumn 210, Issue 8, 2014, Pages 1325-1338

  Sanderson Smith, Martina ^a   De Oliveira, David M P ^a   Guglielmini, Julien ^b,c   McMillan, David J ^d,e   Vu, Therese ^d,f   Holien, Jessica K ^g   Henningham, Anna ^h   Steer, Andrew C ^i,j,k   Bessen, Debra E ^l   Dale, James B ^m,n,o   Curtis, Nigel ^i,j,k   Beall, Bernard W ^p   Walker, Mark J ^h   Parker, Michael W ^g,q   Carapetis, Jonathan R ^r   Van Melderen, Laurence ^f   Sriprakash, Kadaba S ^d   Smeesters, Pierre R ^f,i   Batzloff, Michael ^a   Towers, Rebecca ^a   Goossens, Herman ^f   Malhotra Kumar, Surhbi ^f   Guilherme, Luiza ^s   Torres, Rosangela ^s   Low, Donald ^s   McGeer, Allison ^s   Krizova, Paula ^s   El Tayeb, Sawsan ^s   Kado, Joe ^s   Van Der Linden, Mark ^s   Erdem, Guliz ^s   Moses, Alon ^s   Nir Paz, Ran ^s   Ikebe, Tadayoshi ^s   Watanabe, Haruo ^s   Sow, Samba ^s   Tamboura, Boubou ^s   Kittang, Bard ^s   Melo Cristino, José ^s   Ramirez, Mario ^s   Straut, Monica ^s   Suvorov, Alexander ^s   Totolian, Artem ^s   Engel, Mark ^s   Mayosi, Bongani ^s   Whitelaw, Andrew ^s   Darenberg, Jessica ^s   Normark, Birgitta Henriques ^s   Ni, Chuan Chiang ^s   Wu, Jiunn Jong ^s   De Zoysa, Aruni ^s   Efstratiou, Androulla ^s   Shulman, Stanford ^l   Tanz, Robert ^l   more..

^a UNIVERSITY OF WOLLONGONG   (Australia)

^b INSTITUT PASTEUR   (France)

^c CNRS   (France)

^d QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF THE SUNSHINE COAST   (Australia)

^f UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^g ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^h UNIVERSITY OF QUEENSLAND   (Australia)

ⁱ MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^j UNIVERSITY OF MELBOURNE   (Australia)

^k ROYAL CHILDREN'S HOSPITAL   (Australia)

^l NEW YORK MEDICAL COLLEGE   (United States)

^m UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

ⁿ Department of Veterans   (United States)

^o UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^p NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^q UNIVERSITY OF MELBOURNE   (Australia)

^r UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^s NONE   (United Kingdom)

more..

Author keywords

Epidemiology; Fibrinogen; IgA; IgG; M protein; Molecular typing; Plasminogen; Streptococcus pyogenes; Vaccine

Indexed keywords

M PROTEIN; PROTEIN VARIANT; STREPTOCOCCUS ANTIGEN; STREPTOCOCCUS VACCINE; VIRULENCE FACTOR; BACTERIAL PROTEIN; FIBRINOGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; PLASMINOGEN; RECOMBINANT PROTEIN; VACCINE;

ARTICLE; BACTERIAL GENE; BACTERIAL IMMUNITY; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CLASSIFICATION; CONTROLLED STUDY; DISEASE SURVEILLANCE; EMM GENE; FEASIBILITY STUDY; FUNCTIONAL ASSESSMENT; GENE CLUSTER; MOLECULAR TYPING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; STREPTOCOCCUS PYOGENES; VACCINE PRODUCTION; AMINO ACID SEQUENCE; EPIDEMIOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY;

EPIDEMIOLOGY; FIBRINOGEN; IGA; IGG; M PROTEIN; MOLECULAR TYPING; PLASMINOGEN; STREPTOCOCCUS PYOGENES; VACCINE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; RECOMBINANT PROTEINS; STREPTOCOCCAL VACCINES; STREPTOCOCCUS PYOGENES;

EID: 84910012882     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu260     Document Type: Article

References (50)

1. Carapetis JR, Steer AC, Mulholland EK, Weber M. The global burden of group A streptococcal diseases. Lancet Infect Dis 2005;5:685-94.
2. Steer AC, Lamagni T, Curtis N, Carapetis JR. Invasive group a streptococcal disease: epidemiology, pathogenesis and management. Drugs 2012;72:1213-27.
3. Dale JB, Fischetti VA, Carapetis JR, et al. Group A streptococcal vaccines: paving a path for accelerated development. Vaccine 2013;31(suppl 2):B216-22.
4. Smeesters PR, McMillan DJ, Sriprakash KS. The streptococcal M protein: a highly versatile molecule. Trends Microbiol 2010;18:275-82.
5. Fischetti VA. Streptococcal M protein: molecular design and biological behavior. Clin Microbiol Rev 1989;2:285-314.
6. Whatmore AM, Kapur V, Sullivan DJ, Musser JM, Kehoe MA. Noncongruent relationships between variation in emm gene sequences and the population genetic structure of group A streptococci. Mol Microbiol 1994;14:619-31.
7. 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.
8. Facklam RF, Martin DR, Lovgren M, et al. Extension of the Lancefield classification for group A streptococci by addition of 22 new M protein gene sequence types from clinical isolates: emm103 to emm124. Clin Infect Dis 2002;34:28-38.
9. McMillan DJ, Dreze PA, Vu T, et al. Updated model of group A Streptococcus M proteins based on a comprehensive worldwide study. Clin Microbiol Infect 2013;19:E222-9.
10. Denny FW Jr, Perry WD, Wannamaker LW. Type-specific streptococcal antibody. J Clin Invest 1957;36:1092-100.
11. Lancefield RC. Persistence of type-specific antibodies in man following infection with group A streptococci. J Exp Med 1959;110:271-92.
12. Smeesters PR, McMillan DJ, Sriprakash KS, Georgousakis MM. Differences among group A streptococcus epidemiological landscapes: consequences for M protein-based vaccines? Expert Rev Vaccines 2009;8:1705-20.
13. 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.
14. Smeesters PR, Vergison A, Campos D, De Aguiar E, Miendje Deyi VY, Van Melderen L. Differences between Belgian and Brazilian group A Streptococcus epidemiologic landscape. PLoS ONE 2006;1:e10.
15. 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.
16. Smeesters PR, Dramaix M, Van Melderen L. The emm-type diversity does not always reflect the M protein genetic diversity-is there a case for designer vaccine against GAS. Vaccine 2010;28:883-5.
17. Smeesters PR. Immunity and vaccine development against Streptococcus pyogenes: is emm-typing enough? In: Proceedings of the Belgian Royal Academies of Medicine 2014;3:89-98.
18. 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.
19. Watson RF, Rothbard S, Swift HF. Type-specific protection and immunity following intranasal inoculation of monkeys with group A hemolytic streptococci. J Exp Med 1946;84:127-42.
20. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792-7.
21. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010;27:221-4.
22. Criscuolo A, Gribaldo S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 2010;10:210.
23. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010;59:307-21.
24. Sanderson-Smith ML, Walker MJ, Ranson M. The maintenance of high affinity plasminogen binding by group A streptococcal plasminogenbinding M-like protein is mediated by arginine and histidine residues within the a1 and a2 repeat domains. J Biol Chem 2006;281:25965-71.
25. Wistedt AC, Ringdahl U, Muller-Esterl W, Sjobring U. Identification of a plasminogen-binding motif in PAM, a bacterial surface protein. Mol Microbiol 1995;18:569-78.
26. Rios-Steiner JL, Schenone M, Mochalkin I, Tulinsky A, Castellino FJ. Structure and binding determinants of the recombinant kringle-2 domain of human plasminogen to an internal peptide from a group A Streptococcal surface protein. J Mol Biol 2001;308:705-19.
27. Bessen DE. Localization of immunoglobulin A-binding sites within M or M-like proteins of group A streptococci. Infect Immun 1994;62:1968-74.
28. Johnsson E, Areschoug T, Mestecky J, Lindahl G. An IgA-binding peptide derived from a streptococcal surface protein. J Biol Chem 1999;274:14521-4.
29. Akesson P, Schmidt KH, Cooney J, Bjorck L. M1 protein and protein H: IgGFc- and albumin-binding streptococcal surface proteins encoded by adjacent genes. Biochem J 1994;300(Pt 3):877-86.
30. Pack TD, Podbielski A, Boyle MD. Identification of an amino acid signature sequence predictive of protein G-inhibitable IgG3-binding activity in group-A streptococcal IgG-binding proteins. Gene 1996;171:65-70.
31. Waldemarsson J, Stalhammar-Carlemalm M, Sandin C, Castellino FJ, Lindahl G. Functional dissection of Streptococcus pyogenes M5 protein: the hypervariable region is essential for virulence. PLoS ONE 2009;4:e7279.
32. McNamara C, Zinkernagel AS, Macheboeuf P, Cunningham MW, Nizet V, Ghosh P. Coiled-coil irregularities and instabilities in group A Streptococcus M1 are required for virulence. Science 2008;319:1405-8.
33. Ringdahl U, Sjobring U. Analysis of plasminogen-binding M proteins of Streptococcus pyogenes. Methods 2000;21:143-50.
34. Sandin C, Carlsson F, Lindahl G. Binding of human plasma proteins to Streptococcus pyogenes M protein determines the location of opsonic and non-opsonic epitopes. Mol Microbiol 2006;59:20-30.
35. Retnoningrum DS, Cleary PP. M12 protein from Streptococcus pyogenes is a receptor for immunoglobulin G3 and human albumin. Infect Immun 1994;62:2387-94.
36. Hong K. Characterization of group a streptococcal M23 protein and comparison of the M3 and M23 protein's ligand-binding domains. Curr Microbiol 2007;55:427-34.
37. Gubbe K, Misselwitz R, Welfle K, Reichardt W, Schmidt KH, Welfle H. C repeats of the streptococcal M1 protein achieve the human serum albumin binding ability by flanking regions which stabilize the coiled-coil conformation. Biochemistry 1997;36:8107-13.
38. Persson J, Beall B, Linse S, Lindahl G. Extreme sequence divergence but conserved ligand-binding specificity in Streptococcus pyogenes M protein. PLoS Pathog 2006;2:e47.
39. Dale JB, Penfound TA, Chiang EY, Walton WJ. New 30-valent M protein-based vaccine evokes cross-opsonic antibodies against nonvaccine serotypes of group A streptococci. Vaccine 2011;29:8175-8.
40. Dale JB, Penfound TA, Tamboura B, et al. Potential coverage of a multivalent M protein-based group A streptococcal vaccine. Vaccine 2013;31:1576-81.
41. 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.
42. 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 2013;190:2692-701.
43. Bauer MJ, Georgousakis MM, Vu T, et al. Evaluation of novel Streptococcus pyogenes vaccine candidates incorporating multiple conserved sequences from the C-repeat region of the M-protein. Vaccine 2012;30:2197-205.
44. Guerino MT, Postol E, Demarchi LM, et al. 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.
45. Batzloff MR, Hayman WA, Davies MR, 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.
46. Bessen DE, Lizano S. Tissue tropisms in group A streptococcal infections. Future Microbiol 2010;5:623-38.
47. McGregor KF, Spratt BG, Kalia A, et al. Multilocus sequence typing of Streptococcus pyogenes representing most known emm types and distinctions among subpopulation genetic structures. J Bacteriol 2004;186:4285-94.
48. Hausdorff WP, Van Dyke MK, Van Effelterre T. Serotype replacement after pneumococcal vaccination. Lancet 2012;379:1387-8; author reply 1388-9.
49. Sanderson-Smith ML, Dowton M, Ranson M, Walker MJ. The plasminogen-binding group A streptococcal M protein-related protein Prp binds plasminogen via arginine and histidine residues. J Bacteriol 2007;189:1435-40.
50. Sanderson-Smith ML, Dinkla K, Cole JN, et al. M protein-mediated plasminogen binding is essential for the virulence of an invasive Streptococcus pyogenes isolate. FASEB J 2008;22:2715-22.