Major pathogenicity factors of Streptococcus pyogenes

Cover Page


Cite item

Full Text

Abstract

Streptococcal diseases and their complications are among the global problems of international health. S. pyogenes (group A streptococci — GAS) is a pathogen that causes significant morbidity in different countries and different age groups of the population, occurring both sporadically and epidemically. Due to ineffective antibacterial therapy or its absence, 3–5% of people who have had streptococcal infection may develop complications such as acute rheumatic fever, rheumatic heart disease, acute post-streptococcal glomerulonephritis and invasive complications: necrotizing fasciitis and myositis, septicemia and toxic shock syndrome, highly lethal due to the rapid development of the process and systemic organ damage. According to recent estimates, at least 517 000 deaths occur annually in the world due to diseases caused by GAS. The diverse arsenal of pathogenic factors of this pathogen is manifested in a combination of joint or sequential reactions in the process of microbial colonization of tissue, formation of the focus of infection and overcoming the host's defense mechanisms. It is an important point in the process of studying the pathogenesis of diseases caused by these microbes. The pathogenic factors of GAS can be divided into extracellular and associated with the microbial cell, predominantly with its cell wall. The spectrum activity of pathogenicity factors can be quite wide (M proteins, pyrogenic exotoxins, superantigens) or limited (serine and cysteine proteinases, streptokinase). Information about the specificity of pathogenicity factors, their properties, relationships, regulation and specific function in pathology is the task of scientific, as well as complex researches, leading to understanding the pathogen-host interaction. An integrated approach to the investigation of GAS pathogenicity factors is needed to study the pathogenicity of streptococci, since pathogenicity factors do not manifest themselves in isolation and are not always independently regulated. In many cases, regulators control the expression of more than one of them. S. pyogenes has been studied for about 150 years, but a number of issues related to their pathogenicity remain unknown to this day. Some factors need more in-depth study: for example, endo-β-N-acetylglucosaminidase, arginine deiminase. Immunoglobulin-degrading enzymes require special attention due to their possible participation in the genesis of immunopathological processes of streptococcal etiology. This review summarizes the literature data about most of the pathogenicity factors of S. pyogenes and their role in the infectious process.

About the authors

L. A. Burova

Institute of Experimental Medicine

Author for correspondence.
Email: lburova@yandex.ru

Larisa A. Burova - PhD, MD (Medicine), Leading Researcher, Department of Molecular Microbiology, Institute of Experimental Medicine.

197376, St. Petersburg, Academic Pavlov str., 12.

Phone: +7 (812) 234-05-42.

Россия

A. A. Totolian

Institute of Experimental Medicine

Email: totolyan@hotmail.com

Artem A. Totolian - RAS Full Member, PhD, MD (Medicine), Head Researcher, Department of Molecular Microbiology, Institute of Experimental Medicine.

197376, St. Petersburg, Academic Pavlov str., 12.

Россия

References

  1. Бурова Л.А., Гаврилова Е.А., Пигаревский П.В., Тотолян Артем А. Роль стрептокиназы в моделировании постстрептококкового гломерулонефрита // Инфекция и иммунитет. 2021. Т. 11, № 5. С. 853–864. doi: 10.15789/2220-7619-ARO-1594
  2. Бурова Л.А., Пигаревский П.В., Снегова В.А., Дуплик Н.В., Шален К., Тотолян Артем А. Нефритогенность IgA-связывающих Streptococcus pyogenes. Моделирование IgA-гломерулонефрита // Медицинская иммунология. 2016. Т. 18, № 3. C. 221–230. doi: 10.15789/1563-0625-2016-3-221-230
  3. Старикова Э.А., Кудрявцев И.В., Бурова Л.А., Лебедева А.М., Маммедова Дж.Т., Фрейдлин И.С. Влияние стрептококковой аргининдеиминазы на формирование лейкоцитарного инфильтрата в модели воздушного кармана у мышей // Медицинская иммунология. 2020. Т. 22, № 6. С. 1121–1130. doi: 10.15789/1563-0625-IOS-2075
  4. Старикова Э.А., Соколов А.В., Бурова Л.А., Фрейдлин И.С. Иммуносупрессорные эффекты аргининдеиминазы Streptococcus pyogenes // Медицинская иммунология. 2015. Т. 17, № 4. С. 303–318. doi: 10.15789/1563-0625-2015-4-303-31
  5. Тотолян Артем А., Бурова Л.А. Fc-рецепторные белки Streptococcus pyogenes и патогенез постинфекционных осложнений (критический обзор) // Журнал микробиологии, эпидемиологии и иммунобиологии. 2014. № 3. С. 78–91.
  6. Тотолян А.А., Бурова Л.А., Пигаревский П.В. Экспериментальный постстрептококковый гломерулонефрит. СПб.: Человек, 2019. 108 с.
  7. Agniswamy J., Lei B., Musser J.M., Sun P.D. Insight of host immune evasion mediated by two variants of group A Streptococcus Mac protein. J. Biol. Chem., 2004, vol. 279, no. 50, pp. 52789–52796. doi: 10.1074/jbc.M410698200
  8. Akesson P., Moritz L., Truedsson M., Christensson B., von Pawel-Rammingenet U. IdeS, a highly specific immunoglobulin G (IgG)-cleaving enzyme from Streptococcus pyogenes, is inhibited by specific IgG antibodies generated during infection. Infect. Immun., 2006, vol. 74, no. 1, pp. 497–503. doi: 10.1128/IAI.74.1.497-503.2006
  9. Akesson P., Sjöholm A.G., Björck L. Protein SIC, a novel extracellular protein of Streptococcus pyogenes interfering with complement function. J. Biol. Chem., 1996, vol. 271, no. 2, pp. 1081–1088. doi: 10.1074/jbc.271.2.1081
  10. Ashbaugh C.D., Moser T.J., Shearer M.H., White G.L., Kennedy R.C., Wessels M.R. Bacterial determinants of persistent throat colonization and the associated immune response in primate model of human group A streptococcal pharyngeal infection. Cell Microbiol., 2000, vol. 2, no. 4, pp. 283–292. doi: 10.1046/j.1462-5822.2000.00050.x.
  11. Bastiat-Sempe B., Love J.F., Lomayesva N., Wessels M.R. Streptolysin O and NAD-glycohydrolase prevent phagolysosome acidification and promote group a streptococcus survival in macrophages. mBio, 2014, vol. 5, no. 5: e01690–e14. doi: 10.1128/mBio.01690-14.
  12. Batsford S.R., Mezzano S., Mihatsch M., Schlitz E., Rodríguez-Iturbe B. Is the nephritogenic antigen in post-streptococcal glomerulonephritis pyrogenic exotoxin B (SPE B) or GAPDH? Kidney Int., 2005, vol. 68, no. 3, pp. 1120–1129. doi: 10.1111/j.1523-1755.2005.00504.x
  13. Beckmann C., Waggoner J.D., Harris T.O., Tamura G.S., Rubens C.E. Identification of novel adgesins from group B streptococci by use of phage display revels that C5a peptidase mediates fibronectin binding. Infect. Immun., 2000, vol. 70, no. 6, pp. 2869–2876. doi: 10.1128/iai.70.6.2869-2876.2002
  14. Beres S.B., Sylva G.L., Barbian K.D., Lei B., Hoff J.S., Mammarella N.D., Liu M.Y., Smoot J.C., Porcella S.F., Parkins L.D., Campbel D.S., Smith T.M., McCormick J.K., Leung D.Y.M., Schlievert P.M., Musser J.M. Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc. Natl. Acad. Sci. USA, 2002, vol. 99, no. 15, pp. 10078–10083. doi: 10.1073/pnas.152298499
  15. Berggård K., Johnsson E., Morfeldt E., Persson J., Stålhammar-Carlemalm M., Lindahl G. Binding of human C4BP to the hypervariable region of M protein: a molecular mechanism of phagocytosis resistance in Streptococcus pyogenes. Mol. Microbiol., 2001, vol. 42, no. 2, pp. 539–551. doi: 10.1046/j.1365-2958.2001.02664.x
  16. Bisno A.L., Stevens D.L. Streptococcal infections of skin and soft tissue. N. Engl. J. Med., 1996, vol. 334, no. 4, pp. 240–245. doi: 10.1056/NEJM199601253340407
  17. Bohach G.A., Hauser A.R., Schlievert P.M. Cloning of the gene, speB, for streptococcal pyrogenic exotoxin type B in Escherichia coli. Infect. Immun., 1988, vol. 56, no. 6, pp. 1665–1667 doi: 10.1128/IAI.56.6.1665-1667.1988
  18. Boxrud P.D., Bock P.E. Coupling of conformational and proteolytic activation in the kinetic mechanism of plasminogen activation by streptokinase. J. Biol. Chem., 2004, vol. 279, no. 35, pp. 36642–36649. doi: 10.1074/jbc.M405265200
  19. Boxrud P.D., Fay W.P., Bock P.E. Streptokinase binds to human plasmin with high affinity, perturbs the plasmin active site, and induces expression of a substrate recognition exosite for plasminogen. J. Biol. Chem., 2000, vol. 275, no. 19, pp. 14579–14589. doi: 10.1074/jbc.M405265200.
  20. Bricker A.L., Cywes C., Ashbaugh C.D., Wessels M.R. NAD+-glycohydrolase acts as an intracellular toxin to enhance the extracellular survival of group A streptococci. Mol. Microbiol., 2002, vol. 44, no. 1, pp. 257–269. doi: 10.1046/j.1365-2958.2002.02876.x
  21. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., Zychlinsky A. Neutrophil extra-cellular traps kill bacteria. Science, 2004, vol. 303, no. 5663, pp. 1532–1535. doi: 10.1126/science.1092385
  22. Brosnahan A.J., Schlievert P.M. Gram-positive bacterial superantigen outside-in signaling causes toxic shock syndrome. FEBS J., 2011, vol. 278, no. 23, pp. 4649–4667. doi: 10.1111/j.1742-4658.2011.08151.x
  23. Buchanan J.T., Simpson A.J., Aziz R.K., Liu G.Y., Kristian S.A., Kotb M., Feramisco J., Nizet V. DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr. Biol., 2006, vol. 16, no. 4, pp. 396– 400. doi: 10.1016/j.cub.2005.12.039.
  24. Burova L.A., Schalen C., Koroleva I.V., Svensson M.-L. Role of group a streptococcal IgG Fc-receptor in induction of anti-IgG by immunization in rabbit. FEMS Microb. Immunol., 1989, vol. 47, no. 8–9, pp. 443–448. doi: 10.1111/j.1574-6968.1989.tb02435.x
  25. Carlsson F., Berggard K., Stalhammar-Carlemalm M., Lindahl G. Evasion of phagocytosis through cooperation between two ligand-binding regions in Streptococcus pyogenes M protein. J. Exp. Med., 2003, vol. 198, no. 7, pp. 1057–1058 doi: 10.1084/jem.20030543
  26. Carlsson F., Sandin C., Lindahl G. Human fibrinogen bound to Streptococcus pyogenes M protein inhibits complement deposition via the classical pathway. Mol. Microbiol., 2005, vol. 56, no. 1, pp. 28–39. doi: 10.1111/j.1365-2958.2005.04527.x
  27. Cedervall T., Johansson M.U., Akerstrom B. Coiled-coil structure of group A streptococcal M proteins. Different temperature stability of class A and C proteins by gydrophobic-nongydrophobic amino acid substitutions at heptad positions a and d. Biochemistry, 1997, vol. 36, no. 16, pp. 4987–4994 doi: 10.1021/bi962971q
  28. Chang A., Khemlani A., Kang H., Proft T. Functional analysis of Streptococcus pyogenes nuclease A (SpnA), a novel group A streptococcal virulence factor. Mol. Microbiol., 2011, vol. 79, no. 6, pp. 1629–1642. doi: 10.1111/j.1365-2958.2011.07550.x
  29. Chaussee M.S., Phillips E.R., Ferretti J.J. Temporal production of streptococcal erythrogenic toxin B (streptococcal cysteine proteinase) in response to nutrient depletion. Infect. Immun., 1997, vol. 65, no. 5, pp. 1956–1959. doi: 10.1128/IAI.65.5.1956-1959.1997
  30. Cheng Q., Stafslien D., Purushothaman S.S., Cleary P.P. The group B streptococcal C5a peptidase is both a specific protease and an invasion. Infect. Immun., 2002, vol. 70, no. 5, pp. 2408–2413. doi: 10.1128/iai.70.5.2408-2413.2002
  31. Christensen P., Sramec J., Zatterstrom U. Binding of aggregated IgG in the presence of fresh serum: strong association with type 12 group A streptococci. Absence of binding among nephritogenic type 49 strains. APMIS, 1981, vol. 89, no. 2, pp. 87–91. doi: 10.1111/j.1699-0463.1981.tb00158_89b.x
  32. Cole J.N., Barnett T.C., Nizet V., Walker M.J. Molecular insight into invasive group A streptococcal disease. Nat. Rev. Microbiol., 2011, vol. 9, no. 10, pp. 724–736. doi: 10.1038/nrmicro2648
  33. Cole J.N., McArthur J.D., McKay F.C., Sanderson-Smith M.L., Cork A.J., Ranson M., Rohde M., Itzek A., Sun H., Ginsburg D., Kotb M., Nizet V., Chhatwal G.S., Walker M.J. Trigger for group A streptococcal M1T1 invasive disease. FASEB J., 2006, vol. 20, no. 10, pp. 1745–1747. doi: 10.1096/fj.06-5804fje
  34. Collin M., Olsén A. Effect of SpeB and EndoS from Streptococcus pyogenes on human immunoglobulins. Infect. Immun., 2001, vol. 69, no. 11, pp. 7187–7189. doi: 10.1128/IAI.69.11.7187-7189.2001
  35. Collin M., Olsén A. EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J., 2001, vol. 20, no. 12, pp. 3046–3055. doi: 10.1093/emboj/20.12.3046
  36. Collin M., Svensson M.D., Sjöholm A.G., Jensenius J.C., Sjöbring U., Olsén A. EndoS and SpeB from Streptococcus pyogenes inhibit immunoglobulin-mediated opsonophagocytosis. Infect. Immun., 2002, vol. 70, no. 12, pp. 6646–6651. doi: 10.1128/IAI.70.12.6646-6651.2002
  37. Commons R.J., Smeesters P.R., Proft T., Fraser J.D., Robins-Browne R., Curtis N. Streptococcal superantigens: categorization and clinical associations. Trends Mol. Med., 2014, vol. 20, no. 1, pp. 48–62. doi: 10.1016/j.molmed.2013.10.004
  38. Courtney H.S., Hasty D.L., Dale J.B. Molecular mechanisms of adhesion, colonization and invasion of group A streptococci. Ann. Med., 2002, vol. 34, no. 2, pp. 77–87. doi: 10.1080/07853890252953464
  39. Courtney H.S., von Hunolstein C., Dale J.B., Bronze M.S., Beachey E.H., Hasty D.L. Lipoteichoic acid and M protein: dual adhesions of group A streptococci. Microb. Pathog., 1992, vol. 12, no. 3, pp. 199–208. doi: 10.1016/0882-4010(92)90054-r
  40. Cunningham M.W. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev., 2000, vol. 13, no. 3, pp. 470–511. doi: 10.1128/cmr.13.3.470-511.2000
  41. Cywes C., Stamenkovic I., Wessels M.R. CD44 as a receptor for colonization of the pharynx by group A Streptococcus. J. Clin. Invest., 2000, vol. 106, no. 8, pp. 995–1002. doi: 10.1172/JCI10195
  42. Cywes C., Wessels M.R. Group A Streptococcus tissue invasion by CD44-mediated cell signaling. Nature, 2001, vol. 414, no. 6864, pp. 648–652. doi: 10.1038/414648a
  43. Dale J.B., Chiang E.Y., Hasty D.L., Courtney H.S. Antibodies against a synthetic peptide of SagA neutralize the cytolytic activity of streptolysin S from group A streptococci. Infect. Immun., 2002, vol. 70, no. 4, pp. 2166–2170. doi: 10.1128/iai.70.4.2166-2170.2002
  44. Dale J.B., Washburn R.G., Marques M.B., Wessels M.R. Hyaluronate capsule and surface M protein in resistance to opsonization of group A streptococci. Infect. Immun., 1996, vol. 64, no. 5, pp. 1495–1501. doi: 10.1128/IAI.64.5.1495-1501.1996.
  45. Degnan B.A., Palmer J.M., Robson T., Jones C.E., Fischer M., Glanville M., Mellor G.D., Diamond A.G., Kehoe M.A., Goodacre J.A. Inhibition of human peripheral blood mononuclear cell proliferation by Streptococcus pyogenes cell extract is associated with arginine deiminase activity. Infect. Immun., 1998, vol. 66, no. 7, pp. 3050–3058. doi: 10.1128/IAI.66.7.3050-3058.1998
  46. Dick G.F., Dick G.H. Landmark article Jan 26, 1924: The etiology of scarlet fever. JAMA, 1983, vol. 250, no. 22: 3096. doi: 10.1001/jama.250.22.3096
  47. Egesten A., Eliasson M., Johansson H.M., Olin A.I., Morgelin M., Mueller A., Pease J.E., Frick I.M., Bjorck L. The CXC chemokine MIG/CXCL9 is important in innate immunity against Streptococcus pyogenes. J. Infect. Dis., 2007, vol. 195, no. 5, pp. 684–693. doi: 10.1086/510857
  48. Feil S.C., Ascher D.B., Kuiper M.J., Tweten R.K., Parker M.W. Structural studies of Streptococcus pyogenes streptolysin O provide insights into the early steps of membrane penetration. J. Mol. Biol., 2014, vol. 426, no. 4, pp. 785–792. doi: 10.1016/j.jmb.2013.11.020.
  49. Fernie-King B.A., Seilly D.J., Binks M.J., Sriprakash K.S., Lachmann P.J. Streptococcal DRS (distantly related to SIC) and SIC inhibit antimicrobial peptides, components of mucosal innate immunity: a comparison of their activities. Microbes Infect., 2007, vol. 9, no. 3, pp. 300–307. doi: 10.1016/j.micinf.2006.12.006
  50. Fernie-King B.A., Seilly D.J., Davies A., Lachmann P.J. Streptococcal inhibitor of complement inhibits two additional components of the mucosal innate immune system: secretory leukocyte proteinase inhibitor and lysozyme. Infect. Immun., 2002, vol. 70, no. 9, pp. 4908–4916. doi: 10.1128/iai.70.9.4908-4916.2002.
  51. Fernie-King B.A., Seilly D.J., Willers C., Würzner R., Davies A., Lachmann P.J. Streptococcal inhibitor of complement (SIC) inhibits the membrane attack complex by preventing uptake of C567 onto cell membranes. Immunology, 2001, vol. 103, no. 3, pp. 390–398. doi: 10.1046/j.1365-2567.2001.01249.x
  52. Ferretti J.J., McScan W.M., Ajdic D., Savic G., Lyon K., Primeaux Ch., Sezate S., Suvorov A.N., Kenton S., Lai H.S., Lin S.P., Qian Y., Jia H.G., Najar F.Z., Ren Q., Zhu H., Song L., White J., Yuan X., Clifton S.W., Roe B.A., McLaughlin R. Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc. Natl. Acad. Sci. USA, 2001, vol. 98, no. 8, pp. 4658–4663. doi: 10.1073/pnas.071559398
  53. Fischetti V.A. M protein and other surface proteins on Streptococci. In: Streptococcus pyogenes: Basic Biology to Clinical Manifestations. Oklahoma City: University of Oklahoma Health Sciences Center, 2016. URL: https://www.ncbi.nlm.nih.gov/books/NBK333424
  54. Fischetti V.A. Streptococcal M protein: molecular design and biological behavior. Clin. Microbiol. Rev., 1989, vol. 2, no. 3, pp. 285–314. doi: 10.1128/cmr.2.3.285
  55. Fischetti V.A., Pancholi V., Schneewind O. Conservation of a hexapeptide sequence in the anchor region of the surface proteins of gram-positive cocci. Mol. Microbiol., 1990, vol. 4, no. 9, pp. 1603–1605. doi: 10.1111/j.1365-2958.1990.tb02072.x
  56. Flores A.R., Jewell B.E., Fittipaldi N., Beres S.B., Musser J.M. Human disease isolates of serotype m4 and m22 group a streptococcus lack genes required for hyaluronic acid capsule biosynthesis. mBio, 2012, vol. 3, no. 6: e00413–12. doi: 10.1128/mBio.00413-12
  57. Flores A.R., Jewell B.E., Olsen R.J., Shelburne S.A., Fittipaldi N., Beres S.B., Musser J.M. Asymptomatic carriage of group A streptococcus is associated with elimination of capsule production. Infect. Immun., 2014, vol. 82, no. 9, pp. 3958–3967. doi: 10.1128/IAI.01788-14.
  58. Foley M.J., Wood W.B. Jr. Studies on the pathogenicity of group A streptococci II. The antiphagocytic effects of the M protein and the capsular gel. J. Exp. Med., 1959, vol. 110, no. 4, pp. 617–628. doi: 10.1084/jem.110.4.617
  59. Forsgren A., Sjoquist J. “Protein A” from S. aureus. I. Pseudoimmune reaction with human gamma-globulin. J. Immunol., 1966, vol. 97, no. 6, pp. 822–827.
  60. Frick I.M., Akesson P., Cooney J., Sjobring U., Schmidt K.H., Gomi H., Hattori S., Tagawa C., Kashimoto F., Björck L. Protein H — a surface protein of Streptococcus pyogenes with separate binding sites for IgG and albumin. Mol. Microbiol., 1994, vol. 12, no. 1, pp. 143–151. doi: 10.1111/j.1365-2958.1994.tb01003.x
  61. Frick I.M., Shannon O., Åkesson P., Mörgelin M., Collin M., Schmidtchen A., Björck L. Antibacterial activity of the contact and complement systems is blocked by SIC, a protein secreted by Streptococcus pyogenes. J. Biol. Chem., 2011, vol. 286, no. 2, pp. 1331–1340. doi: 10.1074/jbc.M110.178350
  62. Gase K., Ferretti J.J., Primeaux C., McShan W.M. Identification, cloning, and expression of the CAMP factor gene (cfa) of group A streptococci. Infect. Immun., 1999, vol. 67, no. 9, pp. 4725–4731. doi: 10.1128/IAI.67.9.4725-4731.1999
  63. Gerlach D., Reichardt W., Fleischer B., Schmidt K.H. Separation of mitogenic and pyrogenic activities from so-called erythrogenic toxin type B (Streptococcal proteinase). Zentralbl. Bakteriol., 1994, vol. 280, no. 4, pp. 507–514. doi: 10.1016/s0934-8840(11)80510-4
  64. Ghosh J., Anderson P.J., Chandrasekaran S., Caparon M.G. Characterization of Streptococcus pyogenes beta-NAD + glycohydrolase: re-evaluation of enzymatic properties associated with pathogenesis. J. Biol. Chemist., 2010, vol. 285, no. 8, pp. 5683–5694. doi: 10.1074/jbc.M109.070300
  65. Ghosh J., Caparon M.G. Specificity of Streptococcus pyogenes NAD(+) glycohydrolase in cytolysin-mediated translocation. Mol. Microbiol., 2006, vol. 62, no. 4, pp. 1203–1214. doi: 10.1111/j.1365-2958.2006.05430.x
  66. Ginsburg I. Is streptolysin S of group A streptococci a virulence factor? APMIS, 1999, vol. 107, no. 12, pp. 1051–1059. doi: 10.1111/j.1699-0463.1999.tb01509.x
  67. Grifantini R., Toukoki C., Colaprico A., Gryllos I. Peroxide stimulon and role of PerR in group A Streptococcus. J. Bacterial., 2011, vol. 93, no. 23, pp. 6539–6551. doi: 10.1128/JB.05924-11
  68. Haanes E.J., Heath D.G., Cleary P.P. Architecture of the vir regulons of group A streptococci parallels opacity factor phenotype and M protein class. J. Bacteriol., 1992, vol. 174, no. 15, pp. 4967–4976. doi: 10.1128/jb.174.15.4967-4976.1992
  69. Hanski E., Caparon M. Protein F, a fibronectin-binding protein, is an adhesin of group A streptococcus Streptococcus pyogenes. Proc. Natl. Acad. Sci. USA, 1992, vol. 89, no. 13, pp. 6172–6176. doi: 10.1073/pnas.89.13.6172
  70. Harder J., Franchi L., Muñoz-Planillo R., Park J.H., Reimer T., Núñez G. Activation of the Nlrp3 inflammasome by Streptococcus pyogenes requires streptolysin O and NF-kappa B activation but proceeds independently of TLR signaling and P2X7 receptor. J. Immunol., 2009, vol. 183, no. 9, pp. 5823–5829. doi: 10.4049/jimmunol.0900444
  71. Heath D.G., Cleary P.P. Fc-receptor and M-protein genes of group A streptococci are products of gene duplication. Proc. Natl. Acad. Sci. USA, 1989, vol. 86, no. 12, pp. 4741–4745. doi: 10.1073/pnas.86.12.4741
  72. Herwald H., Collin M., Muller-Esterl W., Bjorck L. Streptococcal cysteine proteinase releases kinins: virulence mechanism. J. Exp. Med., 1996, vol. 184, no. 2, pp. 665–673. doi: 10.1084/jem.184.2.665
  73. Hoe N.P., Ireland R.M., DeLeo F.R., Gowen B.B., Dorward D.W., Voyich J.M., Liu M., Burns E.H. Jr, Culnan D.M., Bretscher A., Musser J.M. Insight into the molecular basis of pathogen abundance: group A Streptococcus inhibitor of complement inhibits bacterial adherence and internalization into human cells. Proc. Natl. Acad. Sci. USA, 2002, vol. 99, no. 11, pp. 7646–7651. doi: 10.1073/pnas.112039899
  74. Hollands A., Pence M.A., Timmer A.M., Osvath S.R., Turnbull L., Whitchurch C.B., Walker M.J., Nizet V. Genetic switch to hypervirulence reduces colonization phenotypes of the globally disseminated group A streptococcus M1T1 clone. J. Infect. Diseas., 2010, vol. 202, no. 1, pp. 11–19. doi: 10.1086/653124
  75. Hollingshead S.K., Arnold J., Readdy T.L., Bessen D.E. Molecular evolution of a multigene family in group A streptococci. Mol. Biol. Evol., 1994, vol. 11, no. 2, pp. 208–219. doi: 10.1093/oxfordjournals.molbev.a040103.
  76. Hollingshead S.K., Readdy T.L., Yung D.L., Bessen D.E. Structural heterogeneity of the emm gene cluster in group A streptococci. Mol. Microbiol., 1993, vol. 8, no. 4, pp. 707–717. doi: 10.1111/j.1365-2958.1993.tb01614.x
  77. Huang T.T., Malke H., Ferretti J.J. Heterogeneity of the streptokinase gene in group A streptococci. Infect. Immun., 1989, vol. 57, no. 2, pp. 502–506. doi: 10.1128/IAI.57.2.502-506.1989
  78. Hynes W., Johnson C., Stokes M. A single nucleotide mutation results in loss of enzymatic activity in the hyaluronate lyase gene of Streptococcus pyogenes. J. Microb. Pathog., 2009, vol. 47, no. 6, pp. 308–313. doi: 10.1016/j.micpath.2009.09.008
  79. Hynes W., Sloan M. Secreted extracellular virulence factors. In: Streptococcus pyogenes: Basic Biology to Clinical Manifestations. Oklahoma City: University of Oklahoma Health Sciences Center, 2016. URL: https://www.ncbi.nlm.nih.gov/books/NBK333424/
  80. Jacks-Weis J., Kim Y., Cleary P.P. Restricted deposition of C3 on M+ group A streptococci: correlation with resistance to phagocytosis. J. Immunol., 1982, vol. 128, no. 4, pp. 1897–1902.
  81. Jantsch J., Gerlach R.G., Ensser A., Dahesh S., Popp I., Heeg C., Bleiziffer O., Merz T., Schulz T., Horch R.E., Bogdan C., Nizet V., van der Linden M. Severe soft tissue infection caused by a non-beta-hemolytic Streptococcus pyogenes strain harboring a premature stop mutation in the sagC gene. J. Clin. Microbiol., 2013, vol. 51, no. 6, pp. 1962–1965. doi: 10.1128/JCM.00175-13
  82. Jin H., Song Y.P., Boel G., Kochar J., Pancholi V. Group A streptococcal surface GAPDH, SDH, recognizes uPAR/CD87 as its receptor on the human pharyngeal cell and mediates bacterial adherence to host cells. Mol. Biol., 2005, vol. 350, no. 1, pp. 27–41. doi: 10.1016/j.jmb.2005.04.063
  83. Kalia A., Bessen D.E. Natural selection and evolution of streptococcal virulence genes involved in tissue-specific adaptations. J. Bacteriol., 2004, vol. 186, no. 1, pp. 110–121. doi: 10.1128/JB.186.1.110-121.2004
  84. Kamezawa Y., Nakahara T., Nakano S., Abe Y., Nozaki-Renard J., Isono T. Streptococcal mitogenic exotoxin Z, a novel acidic superantigenic toxin produced by a T1 strain of Streptococcus pyogenes. Infect. Immun., 1997, vol. 65, no. 9, pp. 3828–3833. doi: 10.1128/IAI.65.9.3828-3833.199
  85. Kanaoka M.C., Kawanaka T., Negoro Y., Fukita K.T., Agui H. Cloning and expression of the antitumor glycoprotein gene of Streptococcus pyogenes Su in Escherichia coli. Agric. Biol. Chem., 1987, vol. 51, pp. 2641–2648.
  86. Kass E.H., Seastone C.V. The role of the mucoid polysaccharide (hyaluronic acid) in the virulence of group A hemolytic streptococci. J. Exp. Med., 1944, vol. 79, no. 3, pp. 319–330. doi: 10.1084/jem.79.3.319
  87. Kawabata S., Tamura Y., Murakami J., Terao Y., Nakagawa I., Hamada S. A novel, anchorless streptococcal surface protein that binds to human immunoglobulins. Biochem. Biophys. Res. Commun., 2002, vol. 296, no. 5, pp. 1329–1333. doi: 10.1016/s0006-291x(02)02078-8
  88. Khil J., Im M., Heath A., Ringdahl U., Mundada L., Engleberg N.C., Fay W.P. Plasminogen enhances virulence of group A streptococci by streptokinase-dependent and streptokinase-independent mechanisms. J. Infect. Dis., 2003, vol. 188, no. 4, pp. 497–505. doi: 10.1086/377100
  89. Kim Y.B., Watson D.W. Apurified group A streptococcal pyrogenic exotoxin. Physiochemical and biological properties, including the enhancement of susceptibility to endotoxin lethal shock. J. Exp. Med., 1970, vol. 131, no. 3, pp. 611–622. doi: 10.1084/jem.131.3.611
  90. Krause R.M. A cartographer’s survey of streptococcal topography. In: Streptococcal diseases and the immune response. Ed. by S.E. Read, J.B. Zabriskie. New-York, London: Academic Press, 1980, pp. 97–110.
  91. Kronvall G. A surface component in group A, C, and G streptococci with non-immune reactivity for immunoglobulin G. J. Immunol., 1973, vol. 111, no. 5, pp. 1401–1406.
  92. Kwinn L.A., Nizet V. How group A Streptococcus circumvents host phagocyte defenses. Future Microbiol., 2007, vol. 2, no. 1, pp. 75–84. doi: 10.2217/17460913.2.1.75
  93. Lancefield R.C. A serological differentiation of human and other groups of hemolytic streptococci. J. Exp. Med., 1933, vol. 57, no. 4, pp. 571–595. doi: 10.1084/jem.57.4.571
  94. Lancefield R.C. Current knowledge of type-specific M antigens of group A streptococci. J. Immunol., 1962, vol. 89, pp. 307–313.
  95. Lawrenson R.A., Sriskandan S. Cell Envelope Proteinase A (Streptococcus). In: Handbook of Proteolytic Enzymes. Ed. by N.D. Rawlings, G. Salvesen. 3rd ed. Amsterdam: Elsevier, 2013, pp. 3195–3202.
  96. Lindahl G. An Odyssey in word of M proteins. In: Perspectives on receptins and resistance. Ed. by G. Kronvall. Stockholm, 2013, pp. 13–23.
  97. Liu M., Zhu H., Li J., Garcia C.C., Feng W., Kirpotina L.N., Hilmer J., Tavares L.P., Layton A.W., Quinn M.T., Bothner B., Teixeira M.M., Leiet B. Group A Streptococcus secreted esterase hydrolyzes platelet-activating factor to impede neutrophil recruitment and facilitate innate immune evasion. PLoS Pathog., 2012, vol. 8, no. 4: e1002624. doi: 10.1371/journal.ppat.100262
  98. Lukomski S., Nakashima K., Abdi I., Cipriano V.J., Ireland R.M., Reid S.D., Adams G.G., Musser J.M. Identification and characterization of the scl gene encoding a group A Streptococcus extracellular protein virulence factor with similarity to human collagen. Infect. Immun., 2000, vol. 68, no. 12, pp. 6542–6553. doi: 10.1128/iai.68.12.6542-6553.2000
  99. Lukomski S., Nakashima K., Abdi I., Cipriano V.J., Shelvin B.J., Graviss E.A., Musser J.M. Identification and characterization of a second extracellular collagen-like protein made by group A Streptococcus: control of production at the level of translation. Infect. Immun., 2001, vol. 69, no. 3, pp. 1729–1738. doi: 10.1128/IAI.69.3.1729-1738.2001
  100. Madden J.C., Ruiz N., Caparon M. Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in gram-positive bacteria. Cell, 2001, vol. 104, no. 1, pp. 143–152. doi: 10.1016/s0092-8674(01)00198-2
  101. Malke H., Ferretti J.J. Streptokinase: cloning, expression, and excretion by Escherichia coli. Proc. Natl. Acad. Sci. USA, 1984, vol. 81, no. 11, pp. 3557–3561. doi: 10.1073/pnas.81.11.3557
  102. McArthur J.D., McKay F.C., Ramachandran V., Shyam P., Cork A.J., Sanderson-Smith M.L., Cole J.N., Ringdahl U., Sjöbring U., Ranson M., Walker M.J. Allelic variants of streptokinase from Streptococcus pyogenes display functional differences in plasminogen activation. FASEB J., 2008, vol. 22, no. 9, pp. 3146–3153. doi: 10.1096/fj.08-109348.
  103. McMillan D.J., Davies M.R., Good M.F., Sriprakash K.S. Immune response to superoxide dismutase in group A streptococcal infection. FEMS Immunol. Med. Microb., 2004, vol. 40, no. 3, pp. 249–256. doi: 10.1016/S0928-8244(04)00003-3
  104. Michos A., Gryllos I., Håkansson A., Srivastava A., Kokkotou E., Wessels M.R. Enhancement of streptolysin O activity and intrinsic cytotoxic effects of the group A streptococcal toxin, NAD-glycohydrolase. J. Biol. Chem., 2006, vol. 281, no. 12, pp. 8216– 8223. doi: 10.1074/jbc.M511674200
  105. Mills J.O., Ghosh P. Nonimmune antibody interactions of group A Streptococcus M and M-like proteins. PLoS Pathog., 2021, vol. 17, no. 2: e1009248. doi: 10.1371/journal.ppat.1009248 E
  106. Minami M., Ohmori D., Tatsuno I., Isaka M., Kawamura Y., Ohta M., Hasegawa T. The streptococcal inhibitor of complement (SIC) protects Streptococcus pyogenes from bacteriocin-like inhibitory substance (BLIS) from Streptococcus salivarius. FEMS Microbiol. Lett., 2009, vol. 298, no. 1, pp. 67–73. doi: 10.1111/j.1574-6968.2009.01696.x
  107. Mollick J.A., Miller G.G., Musser J.M., Cook R.G., Grossman D., Rich R.R. A novel superantigen isolated from pathogenic strains of Streptococcus pyogenes with aminoterminal homology to staphylococcal enterotoxins B and C. J. Clin. Invest., 1993, vol. 92, no. 2, pp. 710–719. doi: 10.1172/JCI116641
  108. Molloy E.M., Cotter P.D., Hill C., Mitchell D.A., Ross R.P. Streptolysin S-like virulence factors: the continuing sagA. Nat. Rev. Microbiol., 2011, vol. 9, no. 9, pp. 670–681. doi: 10.1038/nrmicro2624
  109. Myhre E.B., Kronvall G. Heterogeneity of nonimmune immunoglobulin Fc reactivity among gram-positive cocci. Description of three major types of receptors for human immunoglobulin G. Infect. Immun., 1977, vol. 17, no. 3, pp. 475–482. doi: 10.1128/IAI.17.3.475-482.1977
  110. Nasser W., Beres S.B., Olsen R.J., Dean M.A., Rice K.A., Long S.W., Kristinsson K.G., Gottfredsson M., Vuopio J., Raisanen K., Caugant D.A., Steinbakk M., Low D.E., McGeer A., Darenberg J., Henriques-Normark B., Van Beneden C.A., Hoffmann S., Musser J.M. Evolutionary pathway to increased virulence and epidemic group A Streptococcus disease derived from 3,615 genome sequences. Proc. Natl. Acad. Sci. USA, 2014, vol. 111, no. 17, pp. E1768–E1776. doi: 10.1073/pnas.1403138111
  111. Nelson D.C., Garbe G., Collin M. Cysteine proteinase SpeB from Streptococcus pyogenes — a potent modifier of immunologically important host and bacterial proteins. Biol. Chem., 2011, vol. 392, no. 12, pp. 1077–1088. doi: 10.1515/BC.2011.208
  112. Nilsson M., Sørensen O.E., Mörgelin M., Weineisen M., Sjöbring U., Herwald H. Activation of human polymorphonuclear neutrophils by streptolysin O from Streptococcus pyogenes leads to the release of proinflammatory mediators. Thromb Haemost., 2006, vol. 95, no. 6, pp. 982–990. doi: 10.1160/TH05-08-0572
  113. Nobbs A.H., Lamont R.J., Jenkinson H.F. Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev., 2009, vol. 73, no. 3, pp. 407–450. doi: 10.1128/MMBR.00014-09
  114. Noh E.J., Kang S.W., Shin Y.J., Kim D.C., Park I.S., Kim M.Y., Chun B.G., Min B.H. Characterization of mycoplasma arginine deiminase expressed in E. coli and its inhibitory regulation of nitric oxide synthesis. Mol. Cells, 2002, vol. 13, no. 1, pp. 137–143.
  115. Nordstrand A., Norgren M., Ferretti J.J., Holm S.E. Streptokinase as a mediator of acute post-streptococcal glomerulonephritis in an experimental mouse model. Infect. Immun., 1998, vol. 66, no. 1, pp. 315–321. doi: 10.1128/IAI.66.1.315-321.1998.
  116. Norrby-Teglund A., Nepom G.T., Kotb M. Differential presentation of group A streptococcal superantigens by HLA class II DQ and DR alleles. Eur. J. Immunol., 2002, vol. 32, no. 9, pp. 2570–2577. doi: 10.1002/15214141(200209)32:9<2570::AID-IMMU2570>3.0.CO;2-E
  117. Norrby-Teglund A., Newton D., Kotb M., Holm S.E., Norgren M. Superantigenic properties of the group A streptococcal exotoxin SpeF (MF). Infect. Immun., 1994, vol. 62, no. 12, pp. 5227–5233. doi: 10.1128/IAI.62.12.5227-5233.1994
  118. O’Connor S.P., Cleary P.P. Localization of the strеptococcal C5a peptidase to the surface of group A streptococci. Infect. Immun., 1986, vol. 53, no. 2, pp. 432–434. doi: 10.1128/IAI.53.2.432-434.1986
  119. Ohkuni H., Todome Y., Yoshimura K., Yamamoto T., Suzuki H., Yokomuro K., Johnston K.N., Zabriskie J.B. Detection of nephritis strain-associated streptokinase by monoclonal antibodies. J. Med. Microbiol., 1991, vol. 35, no. 1, pp. 60–63. doi: 10.1099/00222615-35-1-60
  120. Okada K., Katano T., Kamogashira T., Zahn R.J., Morimito Y., Kagami S., Yasutomo K., Kuhara T., Kuroda Y. Streptokinase gene variable region classification in Streptococci: lack of correlation with post-streptococcal glomerulonephritis. Clin. Nephrol., 1995, vol. 44, no. 1, pp. 8–13.
  121. Okamoto S., Tamura Y., Terao Y., Hamada S., Kawabata S. Systemic immunization with streptococcal immunoglobulin-binding protein Sib 35 induces protective immunity against group A Streptococcus challenge in mice. Vaccine, 2005, vol. 23, no. 40, pp. 4852–4859. doi: 10.1016/j.vaccine.2005.02.035
  122. Okamoto S., Terao Y., Hasuike K., Hamada S., Kawabata S. A novel streptococcal leucine zipper protein (Lzp) binds to human immunoglobulins. Bioch. Bioph. Res. Commun., 2008, vol. 377, no. 4, pp. 1128–1134. doi: 10.1016/j.bbrc.2008.10.126
  123. Okamoto S., Terao Y., Tamura Y., Hamada S., Kawabata S. Streptococcal immunoglobulin-binding protein Sib35 exerts stimulatory and mitogenic effects toward mouse B lymphocytes. FEMS Microbiol. Lett., 2008, vol. 281, no. 1, pp. 73–80. doi: 10.1111/j.1574-6968.2008.01078.x
  124. O’Seaghdha M., Wessels M.R. Streptolysin O and its co-toxin NAD-glycohydrolase protect group A Streptococcus from Xenophagic killing. PLoS Pathog., 2013, vol. 9, no. 6: e1003394. doi: 10.1371/journal.ppat.100339
  125. Paillot R., Darby A.C., Robinson C., Wright N.L., Steward K.F., Anderson E., Webb K., Holden M.T.G., Efstratiou A., Broughton K., Jolley K.A., Priestnall S.L., Marotti Campi M.C., Hughes M.A., Radford A., Kerstin Erles K., Waller A.S. Identification of three novel superantigen-encoding genes in Streptococcus equi subsp. zooepidemicus, szeF, szeN, and szeP. Infect. Immun., 2010, vol. 78, no. 11, pp. 4817–4827. doi: 10.1128/IAI.00751-10
  126. Persson H., Vindebro R., von Pawel-Rammingen U. The streptococcal cysteine protease SpeB is not a natural immunoglobulin-cleaving enzyme. Infect. Immun., 2013, vol. 81, no. 6, pp. 2236–2241. doi: 10.1128/IAI.00168-13
  127. Phillips G.N. Jr, Flicker P.F., Cohen C., Manjula B.N., Fischetti V.A. Streptococcal M protein: alpha-helical coiled structure and arrangement on the cell surface. Proc. Natl. Acad. Sci. USA, 1981, vol. 78, no. 8, pp. 4689–4693. doi: 10.1073/pnas.78.8.4689
  128. Podbielski A., Flosdorff A., Weber-Heynemann J. The group A streptococcal virR49 gene controls expression of four structural vir regulon genes. Infect. Immun., 1995, vol. 63, no. 1, pp. 9–20. doi: 10.1128/IAI.63.1.9-20.1995
  129. Proft T., Fraser J. Streptococcal superantigens: biological properties and potential role in disease. In: Streptococcus pyogenes: Basic Biology to Clinical Manifestations. Oklahoma City: University of Oklahoma Health Sciences Center, 2016. URL: https://www.ncbi.nlm.nih.gov/books/NBK333424/
  130. Rasmussen M., Muller H.P., Bjorck L. Protein GRAB of Streptococcus pyogenes regulates proteolysis at the bacterial surface by binding α2-macroglobulin. J. Biol. Chem., 1999, vol. 274, no. 22, pp. 15336–15344. doi: 10.1074/jbc.274.22.15336.
  131. Reglinski M., Sriskandan S. The contribution of group A streptococcal virulence eterminants to the pathogenesis of sepsis. Virulence, 2014, vol. 5, no. 1, pp. 127–136. doi: 10.4161/viru.26400
  132. Riddle D.J., Bessen D.E., Caparon M.G. Variation in Streptococcus pyogenes NAD+ glycohydrolase is associated with tissue tropism. J. Bacteriol., 2010, vol. 192, no. 14, pp. 3735–3746. doi: 10.1128/JB.00234-10
  133. Ryan P.A., Juncosa B. Group A streptococcal adherence. In: Streptococcus pyogenes: Basic Biology to Clinical Manifestations. Oklahoma City: University of Oklahoma Health Sciences Center, 2016. URL: https://www.ncbi.nlm.nih.gov/books/NBK333424
  134. Schalen C., Kurl D.N., Christensen P. Independent binding of native and aggregated IgG in group A streptococci. AMIS, 1986, vol. 94, no. 5, pp. 333–338. doi: 10.1111/j.1699-0463.1986.tb03062.x
  135. Schmitt R., Stahl A.L., Olin A.I., Kristofferson A.C., Robertz J., Novak J., Lindahl G., Karpman D. The combined role of galactose-deficient IgA1 and streptococcal IgA-binding M proteins in inducing IL-6 and C3 secretion from human mesangial cells: implications for IgA nephropathy. J. Immunol., 2014, vol. 193, no. 1, pp. 317–326. doi: 10.4049/jimmunol.1302249
  136. Schrager H.M., Albertí S., Cywes C., Dougherty G.J., Wessels M.R. Hyaluronic acid capsule modulates M protein-mediated adherence and acts as a ligand for attachment of group A Streptococcus to CD44 on human keratinocytes. J. Clin. Invest., 1998, vol. 101, no. 8, pp. 1708–1716. doi: 10.1172/JCI2121.
  137. Shea P.R., Beres S.B., Flores A.R., Ewbank A.L., Gonzalez-Lugo J.H., Martagon-Rosado A.J., Martinez-Gutierrez J.C., Rehman N.A., Serrano-Gonzalez M., Fittipaldi N., Ayers S.D., Webb P., Willey B.M., Low D.E., Musser J.M. Distinct signatures of diversifying selection revealed by genome analysis of respiratory tract and invasive bacterial populations. Proc. Natl. Acad. Sci. USA, 2011, vol. 108, no. 12, pp. 5039–5044. doi: 10.1073/pnas.1016282108
  138. Sheeler R.D., Houston M.S., Radke S., Dale J.C., Adamson S.C. Accuracy of rapid strep testing in patients who have had recent streptococcal pharyngitis. J. Am. Board. Fam. Pract., 2002, vol. 15, no. 4, pp. 261–265.
  139. Shelburne S.A., Granville C., Tokuyama M., Sitkiewicz I., Patel P., Musser J.M. Growth characteristics of and virulence factor production by group A Streptococcus during cultivation in human saliva. Infect. Immun., 2005, vol. 73, no. 8, pp. 4723–4731. doi: 10.1128/IAI.73.8.4723-4731.2005
  140. Sierig G., Cywes C., Wessels M.R., Ashbaugh C.D. Cytotoxic effects of streptolysin O and streptolysin S enhance the virulence of poorly encapsulated group A streptococci. Infect. Immun., 2003, vol. 71, no. 1, pp. 446–455. doi: 10.1128/iai.71.1.446-455.2003
  141. Smoot L.M., McCormick J.K., Smoot J.C., Hoe N.P., Strickland I., Cole R.L., Barbian K.D., Earhart C.A., Ohlendorf D.H., Veasy L.G., Hill H.R., Leung D., Schlievert P.M., Musser J.M. Characterization of two novel pyrogenic toxin superantigens made by an acute rheumatic fever clone of Streptococcus pyogenes associated with multiple disease outbreaks. Infect. Immun., 2002, vol. 70, no. 12, pp. 7095–7104. doi: 10.1128/iai.70.12.7095-7104.2002
  142. Sriskandan S., Unnikrishnan M., Krausz T., Cohen J. Mitogenic factor (MF) is the major DNase of serotype M89 Streptococcus pyogenes. Microbiology, 2000, vol. 146, no. 11, pp. 2785–2792. doi: 10.1099/00221287-146-11-2785
  143. Stalhammar-Carlemalm M., Areschoug T., Larsson C., Lindhal G. The R28 protein of Streptococcus pyogenes is related to several group B streptococcal surface proteins, confers protective immunity and promotes binding to human epithelial cells. Mol. Microbiol., 1999, vol. 33, no. 1, pp. 208–219. doi: 10.1046/j.1365-2958.1999.01470.x
  144. Stevens D.L. Group A beta-hemolytic streptococci: virulence factors, pathogenesis and spectrum of clinical infections. In: Streptococcal Infections. Ed. by D.L. Stevens, E.L. Kaplan. Oxford, England: Oxford University Press, 2000, pp. 19–36.
  145. Stevens D.L., Bryant A.L. Streptolysin O modulates cytokine synthesis in human peripheral blood mononuclear cells. In: Streptococci and the Host. Ed. by T. Horaud, A. Bouvet, R. Leclercq, H. De Montclos, M. Sicard. New York: Plenum Press, 1997, pp. 925–927.
  146. Stollerman G.H., Rytel M., Ortiz J. Accessory plasma factors involved in the bactericidal test for type-specific antibody to group A streptococci. II. Human plasma cofactors enhancing opsonization of encapsulated organisms. J. Exp. Med., 1963, vol. 117, no. 1, pp. 1–17. doi: 10.1084/jem.117.1.1
  147. Su Y.F., Chuang W.J., Wang S.M., Chen W.Y., Chiang Ni C., Lin Y.S., Wu J-J., Liu Ch. The deficient cleavage of M protein-bound IgG by IdeS: insight into the escape of Streptococcus pyogenes from antibody-mediated immunity. Mol. Immunol., 2011, vol. 49, no. 1–2, pp. 134–142. doi: 10.1016/j.molimm.2011.08.002
  148. Sumby P., Zhang S., Whitney A.R., Falugi F., Grandi G., Graviss E.A., Deleo F.R., Musser J.M. A chemokine-degrading extracellular protease made by group A Streptococcus alters pathogenesis by enhancing evasion of the innate immune response. Infect. Immun., 2008, vol. 76, no. 3, pp. 978–985. doi: 10.1128/IAI.01354-07
  149. Sun H., Ringdahl U., Homeister J.W., Fay W.P., Engleberg N.C., Yang A.Y., Rozek L.S., Wang X., Sjöbring U., Ginsburg D. Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science, 2004, vol. 305, no. 5688, pp. 1283– 1286. doi: 10.1126/science.1101245
  150. Sun H., Xu Y., Sitkiewicz I., Ma Y., Wang X., Yestrepsky B.D., Huang Y., Lapadatescu M.C., Larsen M.J., Larsen S.D., James M., Musser J.M., Ginsburg D. Inhibitor of streptokinase gene expression improves survival after group A streptococcus infection in mice. Proc. Natl. Acad. Sci. USA, 2012, vol. 109, no. 9, pp. 3469–3474. doi: 10.1073/pnas.1201031109
  151. Svensson M.D., Scaramuzzino D.A., Sjöbring U., Olsén A., Frank C., Bessen D.E. Role for a secreted cysteine proteinase in the establishment of host tissue tropism by group A streptococci. Mol. Microbiol., 2000, vol. 38, no. 2, pp. 242–253. doi: 10.1046/j.1365-2958.2000.02144.x
  152. Tamayo E., Montes M., García-Medina G., García-Arenzana J.M., Pérez-Trallero E. Spread of a highly mucoid Streptococcus pyogenes emm3/ST15 clone. BMC Infect. Dis., 2010, 10: 233. doi: 10.1186/1471-2334-10-233
  153. Terao Y., Kamabata S., Kunitoma E., Murakami J., Nakagawa I., Hamada S. Fba, a novel fibronectin-binding protein from Streptococcus pyogenes, promotes bacterial entry into epithelial cells and fba gene is positively transcribed under the Mga regulator. Mol. Microbiol., 2001, vol. 42, no. 1, pp. 75–86. doi: 10.1046/j.1365-2958.2001.02579.x
  154. Thern A., Wastfelt M., Lindahl G. Expression of two different antiphagocytic M-proteins by Streptococcus pyogenes of the OF+ lineage. J. Immunol., 1998, vol. 160, no. 2, pp. 860–869.
  155. Todd E.W., Lancefield R.C. Variants of hemolytic streptococci; their relation to type specific substance, virulence, and toxin. J. Exp. Med., 1928, vol. 48, no. 6, pp. 51–76. doi: 10.1084/jem.48.6.751
  156. Trastoy B., Lomino J.V., Pierce B.G., Carter L.G., Günther S., Giddens J.P., Snyder G.A., Weiss T.M., Weng Z., Wang L-X., Sundberget E.J. Crystal structure of Streptococcus pyogenes EndoS, an immunomodulatory endoglycosidase specific for human IgG antibodies. Proc. Natl. Acad. Sci. USA, 2014, vol. 111, no. 18, pp. 6714–6719. doi: 10.1073/pnas.1322908111
  157. Turner C.E., Kurupati P., Jones M.D., Edwards R.J., Sriskandan S. Emerging role of the interleukin-8 cleaving enzyme SpyCEP in clinical Streptococcus pyogenes infection. J. Infect. Dis., 2009, vol. 200, no. 4, pp. 555–563. doi: 10.1086/603541
  158. Veasy L.G., Tani L.Y., Daly J.A., Korgenski K., Miner L., Bale J., Kaplan E.L, Musser J.M., Hillet H.R. Temporal association of the appearance of mucoid strains of Streptococcus pyogenes with a continuing high incidence of rheumatic fever in Utah. Pediatrics, 2004, vol. 113, no. 1, pp. e168–e172. doi: 10.1542/peds.113.3.e168
  159. Von Pawel-Rammingen U., Johansson B.P., Björck L. IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. EMBO J., 2002, vol. 21, no. 7, pp. 1607–1615. doi: 10.1093/emboj/21.7.1607
  160. Walker M.J., Barnett T.C., McArthur J.D., Cole J.N., Gillen C.M., Henningham A., Sriprakash K.S., Sanderson-Smith M.L., Nizet V. Disease manifestations and pathogenic mechanisms of group A streptococcus. Clin. Microbiol. Rev., 2014, vol. 27, no. 2, pp. 264–301. doi: 10.1128/CMR.00101-13
  161. Walker M.J., McArthur J.D., McKay F., Ranson M. Is plasminogen deployed as a Streptococcus pyogenes virulence factor? Trends Microbiol., 2005, vol. 13, no. 7, pp. 308–313. doi: 10.1016/j.tim.2005.05.006
  162. Wang X., Lin X., Loy J.A., Tang J., Zhang X.C. Crystal structure of the catalytic domain of human plasmin complexed with streptokinase. Science, 1998, vol. 281, no. 5383, pp. 1662–1665. doi: 10.1126/science.281.5383.1662
  163. Ward I.B. Teichoic and teichuronic acids: biosynthesis, assembly and location. Microb. Rev., 1981, vol. 45, no. 2, pp. 211–243.
  164. Watson D.W. Host-parasite factors in group A streptococcal infections. Pyrogenic and other effects of immunologic distinct exotoxins related to scarlet fever toxins. J. Exp. Med., 1960, vol. 111, no. 2, pp. 255–284. doi: 10.1084/jem.111.2.255
  165. Wessels M.R. Capsular polysaccharide of group A Streptococcus. In: Gram-Positive Pathogens. Ed. by Fischetti V.A. Washington USA: American Society for Microbiology, 2000, pp. 34–42.
  166. Wessels M.R. Cell wall and surface molecules: capsule. In: Streptococcus pyogenes: basic biology to clinical manifestations. Oklahoma City: University of Oklahoma Health Sciences Center, 2016. URL: https://www.ncbi.nlm.nih.gov/books/NBK333424
  167. Wessels M.R., Moses A.E., Goldberg J.B., DiCesare T.J. Hyaluronoc acid capsule is a virulence factor for mucoid group A streptococci. Proc. Natl. Acad. Sci. USA, 1991, vol. 88, no. 19, pp. 8317–8321. doi: 10.1073/pnas.88.19.8317
  168. Wexler D.E., Chenoweth D.E., Cleary P.P. Mechanism of action of the group A streptrococcal C5a inactivator. Proc. Natl. Acad. Sci. USA, 1985, vol. 82, no. 23, pp. 8144–8148. doi: 10.1073/pnas.82.23.8144
  169. Whatmore A.M., Kehoe M.A. Horizontal gene transfer in the evolution of group A streptococcal emm-like genes: gene mosaics and variation in vir regulons. Mol. Microbiol., 1994, vol. 11, no. 2, pp. 363–374. doi: 10.1111/j.1365-2958.1994.tb00316.x
  170. Whitnack E., Beachey E.H. Antiopsonic activity of fibrinogen bound to M protein on the surface of group A streptococci. J. Clin. Invest., 1982, vol. 69, no. 4, pp. 1042–1045. doi: 10.1172/jci110508
  171. Wicken A.J., Knox K.W. Lipoteichoic acides a new class of bacterial antigen. Science, 1975, vol. 187, no. 4182, pp. 1161–1167. doi: 10.1126/science.46620
  172. Wirawan E., Vanden Berghe T., Lippens S., Agostinis P., Vandenabeele P. Autophagy: for better or for worse. Cell Res., 2012, vol. 22, no. 1, pp. 43–61. doi: 10.1038/cr.2011.152
  173. Yoon J.Y., An D.R., Yoon H.J., Kim H.S., Lee S.J., Im H.N., Jang J.Y., Suh S.W. High-resolution crystal structure of Streptococcus pyogenes γ-NAD+ glycohydrolase in complex with its endogenous inhibitor IFS reveals a highly water-rich interface. J. Synchrotron Radiat., 2013, vol. 20, no. 6, pp. 962–967. doi: 10.1107/S0909049513020803
  174. Yoshida J., Takamura S., Suzuki S. Cell growth inhibitory action of SAGP, an antitumor glycoprotein from Streptococcus pyogenes (Su strain). Jpn J. Pharmacol., 1987, vol. 5, no. 2, pp. 143–147.
  175. Yoshino M., Murayama S.Y., Sunaoshi K., Wajima T., Takahasi M., Masaki J., Kurokawa I., Ubukata K. Nonhemolytic Streptococcus pyogenes isolates that lack large regions of the sag operon mediating streptolysin S production. J. Clinic. Microbiol., 2010, vol. 48, no. 2, pp. 635–638. doi: 10.1128/JCM.01362-09
  176. Yu C.E., Ferretti J.J. Frequency of the erythrogenic toxin B and C genes (speB and speC) among clinical isolates of group A streptococci. Infect. Immun., 1991, vol. 59, no. 1, pp. 211–215. doi: 10.1128/IAI.59.1.211-215.1991
  177. Zhang Y., Liang Z., Glinton K., Ploplis V.A., Castellino F.J. Functional differences between Streptococcus pyogenes cluster 1 and cluster 2b streptokinases are determined by their beta-domains. FEBS Lett., 2013, vol. 587, no. 9, pp. 1304–1309. doi: 10.1016/j.febslet.2013.02.033
  178. Zhu H., Liu M., Sumby P., Lei B. The secreted esterase of group a streptococcus is important for invasive skin infection and dissemination in mice. Infect. Immun., 2009, vol. 77, no. 12, pp. 5225–5232. doi: 10.1128/IAI.00636-09
  179. Zingaretti C., Falugi F., Nardi-Dei V., Pietrocola G., Mariani M., Liberatori S., Gallotta M., Tani Ch., Speziale P., Grandi G., Margarit I. Streptococcus pyogenes SpyCEP: a chemokine-inactivating protease with unique structural and biochemical features. FASEB J., 2010, vol. 24, no. 8, pp. 2839–2848. doi: 10.1096/fj.09-145631

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2021 Burova L.A., Totolian A.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies