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. 1996 Oct;34(10):2511–2515. doi: 10.1128/jcm.34.10.2511-2515.1996

M proteins of group C streptococci isolated from patients with acute pharyngitis.

A L Bisno 1, C M Collins 1, J C Turner 1
PMCID: PMC229307  PMID: 8880511

Abstract

We studied 15 strains of group C (Streptococcus equi subsp. equisimilis) [corrected] isolated from the throats of college students with acute pharyngitis and 5 strains isolated from patients with noninfectious problems. Nineteen of the 20 strains resisted phagocytic killing during incubation in normal human blood, suggesting that they might express M proteins. Genomic DNA from all 20 strains hybridized with a probe corresponding to the carboxyterminal one-third of the group A M-protein gene emm24, a region that is highly conserved among M proteins of group A and group G streptococci. The DNA sequences of the N-terminal (variable) regions of the M-protein-encoding genes from two disease-associated group C isolates and one control isolate were determined. The predicted amino acid sequences of the two pharyngitis strains were identical and were 88% homologous to the amino acid sequence of a group G M-protein gene. The predicted terminal amino acid sequence of the control strain does not correspond to any such sequences in the GenBank database. All three strains studied possess the conserved region domain common to class I group A M-protein types epidemiologically associated with rheumatic fever. These studies demonstrate the presence of M proteins in strains of S. equi subsp. equisimilis [corrected] isolated in cases of endemically occurring acute pharyngitis. Certain of these proteins are similar to those of group G streptococci, while others may represent new M types. The similarity in structure and function between M proteins of nonrheumatogenic serogroups and those of rheumatogenic group A streptococci suggests that factors other than or in addition to M protein per se are likely involved in the pathogenesis of rheumatic fever.

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Selected References

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  1. Barnham M., Thornton T. J., Lange K. Nephritis caused by Streptococcus zooepidemicus (Lancefield group C). Lancet. 1983 Apr 30;1(8331):945–948. doi: 10.1016/s0140-6736(83)92078-0. [DOI] [PubMed] [Google Scholar]
  2. Barson W. J. Group C streptococcal osteomyelitis. J Pediatr Orthop. 1986 May-Jun;6(3):346–348. doi: 10.1097/01241398-198605000-00016. [DOI] [PubMed] [Google Scholar]
  3. Benjamin J. T., Perriello V. A., Jr Pharyngitis due to group C hemolytic streptococci in children. J Pediatr. 1976 Aug;89(2):254–256. doi: 10.1016/s0022-3476(76)80459-3. [DOI] [PubMed] [Google Scholar]
  4. Bessen D. E., Fischetti V. A. Differentiation between two biologically distinct classes of group A streptococci by limited substitutions of amino acids within the shared region of M protein-like molecules. J Exp Med. 1990 Dec 1;172(6):1757–1764. doi: 10.1084/jem.172.6.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bessen D. E., Veasy L. G., Hill H. R., Augustine N. H., Fischetti V. A. Serologic evidence for a class I group A streptococcal infection among rheumatic fever patients. J Infect Dis. 1995 Dec;172(6):1608–1611. doi: 10.1093/infdis/172.6.1608. [DOI] [PubMed] [Google Scholar]
  6. Bessen D., Jones K. F., Fischetti V. A. Evidence for two distinct classes of streptococcal M protein and their relationship to rheumatic fever. J Exp Med. 1989 Jan 1;169(1):269–283. doi: 10.1084/jem.169.1.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bisno A. L. Alternate complement pathway activation by group A streptococci: role of M-protein. Infect Immun. 1979 Dec;26(3):1172–1176. doi: 10.1128/iai.26.3.1172-1176.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bisno A. L., Craven D. E., McCabe W. R. M proteins of group G streptococci isolated from bacteremic human infections. Infect Immun. 1987 Mar;55(3):753–757. doi: 10.1128/iai.55.3.753-757.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Boschwitz J. S., Timoney J. F. Inhibition of C3 deposition on Streptococcus equi subsp. equi by M protein: a mechanism for survival in equine blood. Infect Immun. 1994 Aug;62(8):3515–3520. doi: 10.1128/iai.62.8.3515-3520.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bradley S. F., Gordon J. J., Baumgartner D. D., Marasco W. A., Kauffman C. A. Group C streptococcal bacteremia: analysis of 88 cases. Rev Infect Dis. 1991 Mar-Apr;13(2):270–280. doi: 10.1093/clinids/13.2.270. [DOI] [PubMed] [Google Scholar]
  11. Campo R. E., Schultz D. R., Bisno A. L. M proteins of group G streptococci: mechanisms of resistance to phagocytosis. J Infect Dis. 1995 Mar;171(3):601–606. doi: 10.1093/infdis/171.3.601. [DOI] [PubMed] [Google Scholar]
  12. Carmeli Y., Ruoff K. L. Report of cases of and taxonomic considerations for large-colony-forming Lancefield group C streptococcal bacteremia. J Clin Microbiol. 1995 Aug;33(8):2114–2117. doi: 10.1128/jcm.33.8.2114-2117.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Carmeli Y., Schapiro J. M., Neeman D., Yinnon A. M., Alkan M. Streptococcal group C bacteremia. Survey in Israel and analytic review. Arch Intern Med. 1995 Jun 12;155(11):1170–1176. doi: 10.1001/archinte.155.11.1170. [DOI] [PubMed] [Google Scholar]
  14. Cimolai N., Elford R. W., Bryan L., Anand C., Berger P. Do the beta-hemolytic non-group A streptococci cause pharyngitis? Rev Infect Dis. 1988 May-Jun;10(3):587–601. doi: 10.1093/clinids/10.3.587. [DOI] [PubMed] [Google Scholar]
  15. Cleary P. P., Kaplan E. L., Livdahl C., Skjold S. DNA fingerprints of Streptococcus pyogenes are M type specific. J Infect Dis. 1988 Dec;158(6):1317–1323. doi: 10.1093/infdis/158.6.1317. [DOI] [PubMed] [Google Scholar]
  16. Collins C. M., Kimura A., Bisno A. L. Group G streptococcal M protein exhibits structural features analogous to those of class I M protein of group A streptococci. Infect Immun. 1992 Sep;60(9):3689–3696. doi: 10.1128/iai.60.9.3689-3696.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Coykendall A. L. Classification and identification of the viridans streptococci. Clin Microbiol Rev. 1989 Jul;2(3):315–328. doi: 10.1128/cmr.2.3.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Duca E., Teodorovici G., Radu C., Vî A., Talaşman-Niculescu P., Bernescu E., Feldi C., Roşca V. A new nephritogenic streptococcus. J Hyg (Lond) 1969 Dec;67(4):691–698. doi: 10.1017/s0022172400042145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Edwards A. T., Roulson M., Ironside M. J. A milk-borne outbreak of serious infection due to Streptococcus zooepidemicus (Lancefield Group C). Epidemiol Infect. 1988 Aug;101(1):43–51. doi: 10.1017/s0950268800029204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Efstratiou A., Teare E. L., McGhie D., Colman G. The presence of M proteins in outbreak strains of Streptococcus equisimilis T-type 204. J Infect. 1989 Sep;19(2):105–111. doi: 10.1016/s0163-4453(89)91789-1. [DOI] [PubMed] [Google Scholar]
  21. Fox K., Turner J., Fox A. Role of beta-hemolytic group C streptococci in pharyngitis: incidence and biochemical characteristics of Streptococcus equisimilis and Streptococcus anginosus in patients and healthy controls. J Clin Microbiol. 1993 Apr;31(4):804–807. doi: 10.1128/jcm.31.4.804-807.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Galloway A., Noel I., Efstratiou A., Saint E., White D. R. An outbreak of group C streptococcal infection in a maternity unit. J Hosp Infect. 1994 Sep;28(1):31–37. doi: 10.1016/0195-6701(94)90150-3. [DOI] [PubMed] [Google Scholar]
  23. Galán J. E., Timoney J. F. Immunologic and genetic comparison of Streptococcus equi isolates from the United States and Europe. J Clin Microbiol. 1988 Jun;26(6):1142–1146. doi: 10.1128/jcm.26.6.1142-1146.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hayden G. F., Murphy T. F., Hendley J. O. Non-group A streptococci in the pharynx. Pathogens or innocent bystanders? Am J Dis Child. 1989 Jul;143(7):794–797. doi: 10.1001/archpedi.1989.02150190044018. [DOI] [PubMed] [Google Scholar]
  25. Jean-François M. J., Poskitt D. C., Turnbull S. J., Macdonald L. M., Yasmeen D. Protection against Streptococcus equi infection by monoclonal antibodies against an M-like protein. J Gen Microbiol. 1991 Sep;137(9):2125–2133. doi: 10.1099/00221287-137-9-2125. [DOI] [PubMed] [Google Scholar]
  26. Jones K. F., Fischetti V. A. Biological and immunochemical identity of M protein on group G streptococci with M protein on group A streptococci. Infect Immun. 1987 Mar;55(3):502–506. doi: 10.1128/iai.55.3.502-506.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Keiser P., Campbell W. 'Toxic strep syndrome' associated with group C Streptococcus. Arch Intern Med. 1992 Apr;152(4):882–884. doi: 10.1001/archinte.152.4.882a. [DOI] [PubMed] [Google Scholar]
  28. LANCEFIELD R. C. Current knowledge of type-specific M antigens of group A streptococci. J Immunol. 1962 Sep;89:307–313. [PubMed] [Google Scholar]
  29. LANCEFIELD R. C. Occurrence of R antigen specific for Group A type 3 streptococci. J Exp Med. 1958 Sep 1;108(3):329–341. doi: 10.1084/jem.108.3.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Maxted W. R., Potter E. V. The presence of type 12 M-protein antigen in group G streptococci. J Gen Microbiol. 1967 Oct;49(1):119–125. doi: 10.1099/00221287-49-1-119. [DOI] [PubMed] [Google Scholar]
  31. Meier F. A., Centor R. M., Graham L., Jr, Dalton H. P. Clinical and microbiological evidence for endemic pharyngitis among adults due to group C streptococci. Arch Intern Med. 1990 Apr;150(4):825–829. [PubMed] [Google Scholar]
  32. Ruoff K. L. Streptococcus anginosus ("Streptococcus milleri"): the unrecognized pathogen. Clin Microbiol Rev. 1988 Jan;1(1):102–108. doi: 10.1128/cmr.1.1.102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schnitzler N., Podbielski A., Baumgarten G., Mignon M., Kaufhold A. M or M-like protein gene polymorphisms in human group G streptococci. J Clin Microbiol. 1995 Feb;33(2):356–363. doi: 10.1128/jcm.33.2.356-363.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schwartz R. H., Knerr R. J., Hermansen K., Wientzen R. L. Acute epiglottitis caused by beta-hemolytic group C Streptococci. Am J Dis Child. 1982 Jun;136(6):558–559. doi: 10.1001/archpedi.1982.03970420082024. [DOI] [PubMed] [Google Scholar]
  36. Simpson W. J., Musser J. M., Cleary P. P. Evidence consistent with horizontal transfer of the gene (emm12) encoding serotype M12 protein between group A and group G pathogenic streptococci. Infect Immun. 1992 May;60(5):1890–1893. doi: 10.1128/iai.60.5.1890-1893.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Singh K. P., Morris A., Lang S. D., MacCulloch D. M., Bremner D. A. Clinically significant Streptococcus anginosus (Streptococcus milleri) infections: a review of 186 cases. N Z Med J. 1988 Dec 14;101(859):813–816. [PubMed] [Google Scholar]
  38. Sobrino J., Bosch X., Wennberg P., Villalta J., Grau J. M. Septic arthritis secondary to group C streptococcus typed as Streptococcus equisimilis. J Rheumatol. 1991 Mar;18(3):485–486. [PubMed] [Google Scholar]
  39. Stamm A. M., Cobbs C. G. Group C streptococcal pneumonia: report of a fatal case and review of the literature. Rev Infect Dis. 1980 Nov-Dec;2(6):889–898. doi: 10.1093/clinids/2.6.889. [DOI] [PubMed] [Google Scholar]
  40. Timoney J. F., Walker J., Zhou M., Ding J. Cloning and sequence analysis of a protective M-like protein gene from Streptococcus equi subsp. zooepidemicus. Infect Immun. 1995 Apr;63(4):1440–1445. doi: 10.1128/iai.63.4.1440-1445.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Turner J. C., Fox A., Fox K., Addy C., Garrison C. Z., Herron B., Brunson C., Betcher G. Role of group C beta-hemolytic streptococci in pharyngitis: epidemiologic study of clinical features associated with isolation of group C streptococci. J Clin Microbiol. 1993 Apr;31(4):808–811. doi: 10.1128/jcm.31.4.808-811.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Turner J. C., Hayden G. F., Kiselica D., Lohr J., Fishburne C. F., Murren D. Association of group C beta-hemolytic streptococci with endemic pharyngitis among college students. JAMA. 1990 Nov 28;264(20):2644–2647. [PubMed] [Google Scholar]
  43. Whiley R. A., Beighton D., Winstanley T. G., Fraser H. Y., Hardie J. M. Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus (the Streptococcus milleri group): association with different body sites and clinical infections. J Clin Microbiol. 1992 Jan;30(1):243–244. doi: 10.1128/jcm.30.1.243-244.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Whiley R. A., Fraser H., Hardie J. M., Beighton D. Phenotypic differentiation of Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus strains within the "Streptococcus milleri group". J Clin Microbiol. 1990 Jul;28(7):1497–1501. doi: 10.1128/jcm.28.7.1497-1501.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Yuen K. Y., Seto W. H., Choi C. H., Ng W., Ho S. W., Chau P. Y. Streptococcus zooepidemicus (Lancefield group C) septicaemia in Hong Kong. J Infect. 1990 Nov;21(3):241–250. doi: 10.1016/0163-4453(90)93885-v. [DOI] [PubMed] [Google Scholar]

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