Abstract
Bacterial immunoglobulin-binding proteins expressed on the surface of group A streptococci represent a heterogeneous family of functionally related proteins. In this report, we describe efficient methods for extracting immunoglobulin-binding proteins and classifying them functionally and antigenically. A common characteristic of immunoglobulin-binding proteins expressed by group A streptococci appears to be the absence of internal methionine residues in the binding protein. This has enabled development of a rapid, efficient, cyanogen bromide-based extraction procedure for solubilizing these molecules from intact bacteria. Studies carried out with a series of monospecific polyclonal antibodies prepared in chickens have identified two major antigenic classes of immunoglobulin-binding proteins. The methods described in this report facilitate a rapid functional and serological screening of immunoglobulin-binding proteins that should now enable detailed epidemiological studies of the importance of these molecules in group A streptococcal infections and their relationship to other surface proteins, in particular, the antiphagocytic M protein.
Full text
PDF![3074](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/a740/270591/e9bd492fdcc9/jcm00036-0056.png)
![3075](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/a740/270591/a4d51cb2c592/jcm00036-0057.png)
![3076](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/a740/270591/197ed84d8883/jcm00036-0058.png)
![3077](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/a740/270591/f89b0450a0d9/jcm00036-0059.png)
![3078](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/a740/270591/81ebe5963884/jcm00036-0060.png)
![3079](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/a740/270591/b3040757f97c/jcm00036-0061.png)
![3080](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/a740/270591/1d97202d1143/jcm00036-0062.png)
![3081](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/a740/270591/9ab6be63b444/jcm00036-0063.png)
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Balber A. E., Sturtevant J. E. A surface glycoprotein of Trypanosoma lewisi binds immunoglobulin G from the serum of uninfected rats. Infect Immun. 1986 Aug;53(2):420–426. doi: 10.1128/iai.53.2.420-426.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bessen D. E., Fischetti V. A. Nucleotide sequences of two adjacent M or M-like protein genes of group A streptococci: different RNA transcript levels and identification of a unique immunoglobulin A-binding protein. Infect Immun. 1992 Jan;60(1):124–135. doi: 10.1128/iai.60.1.124-135.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bessen D., Fischetti V. A. A human IgG receptor of group A streptococci is associated with tissue site of infection and streptococcal class. J Infect Dis. 1990 Apr;161(4):747–754. doi: 10.1093/infdis/161.4.747. [DOI] [PubMed] [Google Scholar]
- 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]
- Blumenfeld W., Mandrell R. E., Jarvis G. A., Griffiss J. M. Localization of host immunoglobulin G to the surface of Pneumocystis carinii. Infect Immun. 1990 Feb;58(2):456–463. doi: 10.1128/iai.58.2.456-463.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bricker B. J., Tabatabai L. B., Mayfield J. E. Immunoglobulin G binding activity of Brucella abortus. Mol Immunol. 1991 Jan-Feb;28(1-2):35–39. doi: 10.1016/0161-5890(91)90084-w. [DOI] [PubMed] [Google Scholar]
- Caparon M. G., Scott J. R. Identification of a gene that regulates expression of M protein, the major virulence determinant of group A streptococci. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8677–8681. doi: 10.1073/pnas.84.23.8677. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fischetti V. A. Streptococcal M protein: molecular design and biological behavior. Clin Microbiol Rev. 1989 Jul;2(3):285–314. doi: 10.1128/cmr.2.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frithz E., Hedén L. O., Lindahl G. Extensive sequence homology between IgA receptor and M proteins in Streptococcus pyogenes. Mol Microbiol. 1989 Aug;3(8):1111–1119. doi: 10.1111/j.1365-2958.1989.tb00261.x. [DOI] [PubMed] [Google Scholar]
- Gomi H., Hozumi T., Hattori S., Tagawa C., Kishimoto F., Björck L. The gene sequence and some properties of protein H. A novel IgG-binding protein. J Immunol. 1990 May 15;144(10):4046–4052. [PubMed] [Google Scholar]
- Haanes E. J., Cleary P. P. Identification of a divergent M protein gene and an M protein-related gene family in Streptococcus pyogenes serotype 49. J Bacteriol. 1989 Dec;171(12):6397–6408. doi: 10.1128/jb.171.12.6397-6408.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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 Aug;174(15):4967–4976. doi: 10.1128/jb.174.15.4967-4976.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heath D. G., Cleary P. P. Cloning and expression of the gene for an immunoglobulin G Fc receptor protein from a group A streptococcus. Infect Immun. 1987 May;55(5):1233–1238. doi: 10.1128/iai.55.5.1233-1238.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones K. F., Manjula B. N., Johnston K. H., Hollingshead S. K., Scott J. R., Fischetti V. A. Location of variable and conserved epitopes among the multiple serotypes of streptococcal M protein. J Exp Med. 1985 Mar 1;161(3):623–628. doi: 10.1084/jem.161.3.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lindahl G., Stenberg L. Binding of IgA and/or IgG is a common property among clinical isolates of group A streptococci. Epidemiol Infect. 1990 Aug;105(1):87–93. doi: 10.1017/s0950268800047683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller J. F., Mekalanos J. J., Falkow S. Coordinate regulation and sensory transduction in the control of bacterial virulence. Science. 1989 Feb 17;243(4893):916–922. doi: 10.1126/science.2537530. [DOI] [PubMed] [Google Scholar]
- Musser J. M., Hauser A. R., Kim M. H., Schlievert P. M., Nelson K., Selander R. K. Streptococcus pyogenes causing toxic-shock-like syndrome and other invasive diseases: clonal diversity and pyrogenic exotoxin expression. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2668–2672. doi: 10.1073/pnas.88.7.2668. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Otten R. A., Raeder R., Heath D. G., Lottenberg R., Cleary P. P., Boyle M. D. Identification of two type IIa IgG-binding proteins expressed by a single group A streptococcus. J Immunol. 1992 May 15;148(10):3174–3182. [PubMed] [Google Scholar]
- Perez-Casal J., Caparon M. G., Scott J. R. Mry, a trans-acting positive regulator of the M protein gene of Streptococcus pyogenes with similarity to the receptor proteins of two-component regulatory systems. J Bacteriol. 1991 Apr;173(8):2617–2624. doi: 10.1128/jb.173.8.2617-2624.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Podbielski A., Melzer B., Lütticken R. Application of the polymerase chain reaction to study the M protein(-like) gene family in beta-hemolytic streptococci. Med Microbiol Immunol. 1991;180(4):213–227. doi: 10.1007/BF00215250. [DOI] [PubMed] [Google Scholar]
- Poirier T. P., Kehoe M. A., Whitnack E., Dockter M. E., Beachey E. H. Fibrinogen binding and resistance to phagocytosis of Streptococcus sanguis expressing cloned M protein of Streptococcus pyogenes. Infect Immun. 1989 Jan;57(1):29–35. doi: 10.1128/iai.57.1.29-35.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raeder R., Faulmann E. L., Boyle M. D. Evidence for functional heterogeneity in IgG Fc-binding proteins associated with group A streptococci. J Immunol. 1991 Feb 15;146(4):1247–1253. [PubMed] [Google Scholar]
- Reis K. J., Yarnall M., Ayoub E. M., Boyle M. D. Effect of mouse passage on Fc receptor expression by group A streptococci. Scand J Immunol. 1984 Nov;20(5):433–439. doi: 10.1111/j.1365-3083.1984.tb01022.x. [DOI] [PubMed] [Google Scholar]
- Robbins J. C., Spanier J. G., Jones S. J., Simpson W. J., Cleary P. P. Streptococcus pyogenes type 12 M protein gene regulation by upstream sequences. J Bacteriol. 1987 Dec;169(12):5633–5640. doi: 10.1128/jb.169.12.5633-5640.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmidt K. H., Wadström T. A secreted receptor related to M1 protein of Streptococcus pyogenes binds to fibrinogen, IgG, and albumin. Zentralbl Bakteriol. 1990 Jun;273(2):216–228. doi: 10.1016/s0934-8840(11)80252-5. [DOI] [PubMed] [Google Scholar]
- Scott J. R., Guenthner P. C., Malone L. M., Fischetti V. A. Conversion of an M- group A streptococcus to M+ by transfer of a plasmid containing an M6 gene. J Exp Med. 1986 Nov 1;164(5):1641–1651. doi: 10.1084/jem.164.5.1641. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simpson W. J., LaPenta D., Chen C., Cleary P. P. Coregulation of type 12 M protein and streptococcal C5a peptidase genes in group A streptococci: evidence for a virulence regulon controlled by the virR locus. J Bacteriol. 1990 Feb;172(2):696–700. doi: 10.1128/jb.172.2.696-700.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stannard L. M., Hardie D. R. An Fc receptor for human immunoglobulin G is located within the tegument of human cytomegalovirus. J Virol. 1991 Jun;65(6):3411–3415. doi: 10.1128/jvi.65.6.3411-3415.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yarnall M., Boyle M. D. Identification of a unique receptor on a group A streptococcus for the Fc region of human IgG3. J Immunol. 1986 Apr 1;136(7):2670–2673. [PubMed] [Google Scholar]
- Yarnall M., Boyle M. D. Isolation and characterization of type IIa and type IIb Fc receptors from a group A streptococcus. Scand J Immunol. 1986 Nov;24(5):549–557. doi: 10.1111/j.1365-3083.1986.tb02170.x. [DOI] [PubMed] [Google Scholar]