The nonideal coiled coil of M protein and its multifarious functions in pathogenesis.

Partho Ghosh
Author Information
  1. Partho Ghosh: Department of Chemistry and Biochemistry, University of California, San Diego, CA, 92093-0375, USA. pghosh@ucsd.edu

Abstract

The M protein is a major virulence factor of Streptococcus pyogenes (group A Streptococcus, GAS). This gram-positive bacterial pathogen is responsible for mild infections, such as pharyngitis, and severe invasive disease, like streptococcal toxic shock syndrome. M protein contributes to GAS virulence in multifarious ways, including blocking deposition of antibodies and complement, helping formation of microcolonies, neutralizing antimicrobial peptides, and triggering a proinflammatory and procoagulatory state. These functions are specified by interactions between M protein and many host components, especially C4BP and fibrinogen. The former interaction is conserved among many antigenically variant M protein types but occurs in a strikingly sequence-independent manner, and the latter is associated in the M1 protein type with severe invasive disease. Remarkably for a protein of such diverse interactions, the M protein has a relatively simple but nonideal α-helical coiled coil sequence. This sequence nonideality is a crucial feature of M protein. Nonideal residues give rise to specific irregularities in its coiled-coil structure, which are essential for interactions with fibrinogen and establishment of a proinflammatory state. In addition, these structural irregularities are reminiscent of those in myosin and tropomyosin, which are targets for crossreactive antibodies in patients suffering from autoimmune sequelae of GAS infection.

References

  1. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2489-93 [PMID: 7708671]
  2. Proc Natl Acad Sci U S A. 2005 Dec 27;102(52):18878-83 [PMID: 16365313]
  3. Clin Infect Dis. 2009 Oct 1;49(7):1044-50 [PMID: 19725785]
  4. Microbiol Mol Biol Rev. 1999 Mar;63(1):174-229 [PMID: 10066836]
  5. Nat Med. 2001 Oct;7(10):1123-7 [PMID: 11590435]
  6. Biochemistry. 1995 Oct 17;34(41):13688-98 [PMID: 7577960]
  7. FASEB J. 2006 Aug;20(10):1745-7 [PMID: 16790522]
  8. PLoS One. 2009 Oct 01;4(10):e7279 [PMID: 19794915]
  9. J Exp Med. 1976 Apr 1;143(4):759-71 [PMID: 768404]
  10. J Biol Chem. 1995 Apr 28;270(17):9862-7 [PMID: 7730368]
  11. Eur Respir J. 2008 Aug;32(2):405-12 [PMID: 18321926]
  12. Clin Microbiol Rev. 1989 Jul;2(3):285-314 [PMID: 2670192]
  13. Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5543-7 [PMID: 8202524]
  14. Microbiology (Reading). 2007 Aug;153(Pt 8):2458-2464 [PMID: 17660410]
  15. J Exp Med. 2000 Jun 5;191(11):1829-39 [PMID: 10839800]
  16. Emerg Infect Dis. 2008 Oct;14(10):1511-7 [PMID: 18826812]
  17. J Immunol. 1992 May 15;148(10):3238-43 [PMID: 1578147]
  18. PLoS Pathog. 2008 Sep 12;4(9):e1000149 [PMID: 18787689]
  19. Science. 2004 Aug 27;305(5688):1283-6 [PMID: 15333838]
  20. J Biol Chem. 2006 Feb 10;281(6):3690-7 [PMID: 16330538]
  21. J Exp Med. 1980 Mar 1;151(3):695-708 [PMID: 6987328]
  22. Clin Infect Dis. 2007 Oct 1;45(7):853-62 [PMID: 17806049]
  23. Mol Microbiol. 2000 Sep;37(6):1318-26 [PMID: 10998165]
  24. Mol Microbiol. 2005 Sep;57(6):1545-56 [PMID: 16135223]
  25. J Immunol. 1996 Dec 1;157(11):4935-9 [PMID: 8943398]
  26. Cell Host Microbe. 2007 Dec 13;2(6):427-34 [PMID: 18078694]
  27. Mol Microbiol. 2001 Oct;42(2):539-51 [PMID: 11703674]
  28. Scand J Immunol. 1995 Oct;42(4):433-41 [PMID: 7569776]
  29. J Exp Med. 1983 Nov 1;158(5):1727-32 [PMID: 6195292]
  30. Biochemistry. 2006 Apr 11;45(14):4559-68 [PMID: 16584191]
  31. Mol Microbiol. 2001 Aug;41(4):817-26 [PMID: 11532146]
  32. Mol Microbiol. 2008 Feb;67(3):482-92 [PMID: 18093092]
  33. J Immunol. 1998 Nov 1;161(9):4894-901 [PMID: 9794423]
  34. J Mol Biol. 2000 Jul 7;300(2):377-402 [PMID: 10873472]
  35. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6596-600 [PMID: 293746]
  36. Mol Microbiol. 2000 Sep;37(5):1232-47 [PMID: 10972839]
  37. Infect Immun. 2000 Nov;68(11):6362-9 [PMID: 11035746]
  38. Clin Diagn Lab Immunol. 2005 Jul;12(7):833-6 [PMID: 16002631]
  39. Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2858-63 [PMID: 10706638]
  40. Nature. 2003 Jul 17;424(6946):341-5 [PMID: 12867988]
  41. Cell Microbiol. 2008 Feb;10(2):404-14 [PMID: 17900297]
  42. Lancet Infect Dis. 2009 Oct;9(10):611-6 [PMID: 19778763]
  43. Mol Microbiol. 2005 Apr;56(1):28-39 [PMID: 15773976]
  44. J Immunol. 2001 Oct 1;167(7):3870-7 [PMID: 11564804]
  45. PLoS Pathog. 2006 May;2(5):e47 [PMID: 16733543]
  46. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4689-93 [PMID: 7029524]
  47. J Infect Dis. 2010 May 15;201(10):1580-8 [PMID: 20367460]
  48. J Immunol. 2006 Jul 15;177(2):1221-8 [PMID: 16818781]
  49. Mol Microbiol. 2007 Sep;65(5):1147-57 [PMID: 17662041]
  50. Cell. 2004 Feb 6;116(3):367-79 [PMID: 15016372]
  51. J Innate Immun. 2009;1(3):202-14 [PMID: 20375578]
  52. Infect Immun. 1991 May;59(5):1811-7 [PMID: 2019444]
  53. Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8496-501 [PMID: 11438684]
  54. Nature. 2006 Aug 24;442(7105):943-6 [PMID: 16929299]
  55. J Exp Med. 2003 Oct 6;198(7):1057-68 [PMID: 14517274]
  56. Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17713-7 [PMID: 17095604]
  57. Mol Microbiol. 2006 Jan;59(1):20-30 [PMID: 16359315]
  58. Clin Microbiol Rev. 2000 Jul;13(3):470-511 [PMID: 10885988]
  59. Science. 2008 Mar 7;319(5868):1405-8 [PMID: 18323455]
  60. Clin Infect Dis. 2002 Jan 1;34(1):28-38 [PMID: 11731942]
  61. J Exp Med. 1928 Jan 1;47(1):91-103 [PMID: 19869404]
  62. Protein Sci. 1999 Nov;8(11):2312-29 [PMID: 10595534]
  63. Biochemistry. 1997 Apr 22;36(16):4987-94 [PMID: 9125521]
  64. J Exp Med. 1988 Mar 1;167(3):1114-23 [PMID: 2450950]
  65. Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1320-4 [PMID: 1311095]
  66. Blood. 2002 Mar 1;99(5):1785-93 [PMID: 11861296]
  67. J Immunol. 1988 Nov 15;141(10):3592-9 [PMID: 2460540]
  68. Biochemistry. 1997 Jul 1;36(26):8107-13 [PMID: 9201959]

Grants

  1. R01 AI096837/NIAID NIH HHS

MeSH Term

Antigenic Variation
Antigens, Bacterial
Bacterial Outer Membrane Proteins
Carrier Proteins
Host-Pathogen Interactions
Humans
Models, Molecular
Protein Structure, Secondary
Streptococcal Infections
Streptococcus pyogenes
Virulence

Chemicals

Antigens, Bacterial
Bacterial Outer Membrane Proteins
Carrier Proteins
streptococcal M protein