Skip to main content
SpringerLink
Log in

The identification of six novel proteins with fibronectin or collagen type I binding activity from Streptococcus suis serotype 2

  • Microbial Pathogenesis and Host-Microbe Interaction
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Streptococcus suis, a major swine pathogen, is an emerging zoonotic agent that causes meningitis and septic shock. Bacterial cell wall and secreted proteins are often involved in interactions with extracellular matrix proteins (ECMs), which play important roles in the initial steps of pathogenesis. In this study, 2D SDS-PAGE, western blotting-based binding affinity measurements, and microtiter plate binding assays were used to identify cell wall and secreted proteins from S. suis that interact with fibronectin and collagen type I. We identified six proteins from S. suis, including three proteins (translation elongation factor G, oligopeptide-binding protein OppA precursor, and phosphoglycerate mutase) that show both fibronectin and collagen type I binding activity. To the best of our knowledge, these three newly identified proteins had no previously reported fibronectin or collagen type I binding activity. Overall, the aim in this study was to identify proteins with ECM binding activity from S. suis and it represents the first report of six new proteins from S. suis that interact with fibronectin or collagen type I.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Balasubramanian S., Kannan T.R., Hart P.J., and Baseman J.B. 2009. Amino acid changes in elongation factor Tu of Mycoplasma pneumoniae and Mycoplasma genitalium influence fibronectin binding. Infect. Immun. 77, 3533–3541.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Boone T.J., Burnham C.A., and Tyrrell G.J. 2011. Binding of group B streptococcal phosphoglycerate kinase to plasminogen and actin. Microb. Pathog. 51, 255–261.

    Article  CAS  PubMed  Google Scholar 

  • Boone T.J. and Tyrrell G.J. 2012. Identification of the actin and plasminogen binding regions of group B streptococcal phosphoglycerate kinase. J. Biol. Chem. 287, 29035–29044.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chanter N., Jones P.W., and Alexander T.J. 1993. Meningitis in pigs caused by Streptococcus suis-a speculative review. Vet. Microbiol. 36, 39–55.

    Article  CAS  PubMed  Google Scholar 

  • Cole J.N., Ramirez R.D., Currie B.J., Cordwell S.J., Djordjevic S.P., and Walker M.J. 2005. Surface analyses and immune reactivities of major cell wall-associated proteins of group A Streptococcus. Infect. Immun. 73, 3137–3146.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dallo S.F., Zhang B., Denno J., Hong S., Tsai A., Haskins W., Ye J.Y., and Weitao T. 2012. Association of Acinetobacter baumannii EF-Tu with cell surface, outer membrane vesicles, and fibronectin. TheScientificWorldJournal. 2012, 1287–5.

    Article  Google Scholar 

  • de Greeff A., Buys H., Verhaar R., Dijkstra J., van Alphen L., and Smith H.E. 2002. Contribution of fibronectin-binding protein to pathogenesis of Streptococcus suis serotype 2. Infect. Immun. 70, 1319–1325.

    Article  PubMed Central  PubMed  Google Scholar 

  • Delvecchio V.G., Connolly J.P., Alefantis T.G., Walz A., Quan M.A., Patra G., Ashton J.M., Whittington J.T., Chafin R.D., Liang X., Grewal P., Khan A.S., and Mujer C.V. 2006. Proteomic profiling and identification of immunodominant spore antigens of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis. Appl. Environ. Microbiol. 72, 6355–6363.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Esgleas M., Lacouture S., and Gottschalk M. 2005. Streptococcus suis serotype 2 binding to extracellular matrix proteins. FEMS Microbiol. Lett. 244, 33–40.

    Article  CAS  PubMed  Google Scholar 

  • Esgleas M., Li Y., Hancock M.A., Harel J., Dubreuil J.D., and Gottschalk M. 2008. Isolation and characterization of alphaenolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 154, 2668–2679.

    Article  CAS  PubMed  Google Scholar 

  • Fenno J.C., Tamura M., Hannam P.M., Wong G.W., Chan R.A., and McBride B.C. 2000. Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment. Infect. Immun. 68, 1884–1892.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Finlay B.B. 1990. Cell adhesion and invasion mechanisms in microbial pathogenesis. Curr. Opin. Cell. Biol. 2, 815–820.

    Article  CAS  PubMed  Google Scholar 

  • Fittipaldi N., Segura M., Grenier D., and Gottschalk M. 2012. Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol. 7, 259–279.

    Article  CAS  PubMed  Google Scholar 

  • Francolini I. and Donelli G. 2010. Prevention and control of biofilm-based medical-device-related infections. FEMS Immunol. Med. Microbiol. 59, 227–238.

    CAS  PubMed  Google Scholar 

  • Higgins R. and Gottschalk M. 2000. Distribution of Streptococcus suis capsular types in 1999. Can. Vet. J. 41, 4–4.

    Google Scholar 

  • Jobin M.C., Brassard J., Quessy S., Gottschalk M., and Grenier D. 2004. Acquisition of host plasmin activity by the swine pathogen Streptococcus suis serotype 2. Infect. Immun. 72, 606–610.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ju C.X., Gu H.W., and Lu C.P. 2012. Characterization and functional analysis of atl, a novel gene encoding autolysin in Streptococcus suis. J. Bacteriol. 194, 1464–1473.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Khan M.N., Shukla D., Bansal A., Mustoori S., and Ilavazhagan G. 2009. Immunogenicity and protective efficacy of GroEL (hsp60) of Streptococcus pneumoniae against lethal infection in mice. FEMS Immunol. Med. Microbiol. 56, 56–62.

    Article  CAS  PubMed  Google Scholar 

  • Kim K.I., Park S.C., Kang S.H., Cheong G.W., and Chung C.H. 1999. Selective degradation of unfolded proteins by the self-compartmentalizing HtrA protease, a periplasmic heat shock protein in Escherichia coli. J. Mol. Biol. 294, 1363–1374.

    Article  CAS  PubMed  Google Scholar 

  • Kutz R. and Okwumabua O. 2008. Differentiation of highly virulent strains of Streptococcus suis serotype 2 according to glutamate dehydrogenase electrophoretic and sequence type. J.Clin. Microbiol. 46, 3201–3207.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lemos J.A., Luzardo Y., and Burne R.A. 2007. Physiologic effects of forced down-regulation of dnaK and groEL expression in Streptococcus mutans. J. Bacteriol. 189, 1582–1588.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ling E., Feldman G., Portnoi M., Dagan R., Overweg K., Mulholland F., Chalifa-Caspi V., Wells J., and Mizrachi-Nebenzahl Y. 2004. Glycolytic enzymes associated with the cell surface of Streptococcus pneumoniae are antigenic in humans and elicit protective immune responses in the mouse. Clin. Exp. Immunol. 138, 290–298.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nepomuceno R.S., Tavares M.B., Lemos J.A., Griswold A.R., Ribeiro J.L., Balan A., Guimaraes K.S., Cai S., Burne R.A., Ferreira L.C., and Ferreira R.C. 2007. The oligopeptide (opp) gene cluster of Streptococcus mutans: Identification, prevalence, and characterization. Oral Microbiol. Immun. 22, 277–284.

    Article  CAS  Google Scholar 

  • Okwumabua O., Persaud J.S., and Reddy P.G. 2001. Cloning and characterization of the gene encoding the glutamate dehydrogenase of Streptococcus suis serotype 2. Clin. Diagn. Lab. Immunol. 8, 251–257.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Patti J.M., Jonsson H., Guss B., Switalski L.M., Wiberg K., Lindberg M., and Hook M. 1992. Molecular characterization and expression of a gene encoding a Staphylococcus aureus collagen adhesin. J. Biol. Chem. 267, 4766–4772.

    CAS  PubMed  Google Scholar 

  • Quessy S., Busque P., Higgins R., Jacques M., and Dubreuil J.D. 1997. Description of an albumin binding activity for Streptococcus suis serotype 2. FEMS Microbiol. Lett. 147, 245–250.

    Article  CAS  PubMed  Google Scholar 

  • Savini V., Catavitello C., Astolfi D., Balbinot A., Masciarelli G., Pompilio A., Quaglietta A.M., Accorsi P., Di Bonaventura G., D’Amario C., and et al. 2010. Bacterial contamination of platelets and septic transfusions: Review of the literature and discussion on recent patents about biofilm treatment. Recent Pat Antiinfect. Drug Discov. 5, 168–176.

    Article  CAS  PubMed  Google Scholar 

  • Staats J.J., Feder I., Okwumabua O., and Chengappa M.M. 1997. Streptococcus suis: Past and present. Vet. Res. Commun. 21, 381–407.

    Article  CAS  PubMed  Google Scholar 

  • Tang J., Wang C., Feng Y., Yang W., Song H., Chen Z., Yu H., Pan X., Zhou X., Wang H., and et al. 2006. Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med. 3, e151.

    Article  Google Scholar 

  • Wang Y., Yi L., Wu Z., Shao J., Liu G., Fan H., Zhang W., and Lu C. 2012. Comparative proteomic analysis of Streptococcus suis biofilms and planktonic cells that identified biofilm infection-related immunogenic proteins. PLoS ONE 7, e33371.

    Article  Google Scholar 

  • Wu Z., Zhang W., and Lu C. 2008a. Comparative proteome analysis of secreted proteins of Streptococcus suis serotype 9 isolates from diseased and healthy pigs. Microb. Pathog. 45, 159–166.

    Article  CAS  PubMed  Google Scholar 

  • Wu Z., Zhang W., and Lu C. 2008b. Immunoproteomic assay of surface proteins of Streptococcus suis serotype 9. FEMS Immunol. Med. Microbiol. 53, 52–59.

    Article  CAS  PubMed  Google Scholar 

  • Wu Z., Zhang W., Shao J., Wang Y., Lu Y., and Lu C. 2011. Immunoproteomic assay of secreted proteins of Streptococcus suis serotype 9 with convalescent sera from pigs. Folia Microbiol. 56, 423–430.

    Article  CAS  Google Scholar 

  • Yang X.J., He Y.M., Wu Y.W., Zhang B., Hui J., Jiang T.B., Song J.P., Liu Z.H., and Jiang W.P. 2008. Hypoxia imaging of patients with acute myocardial infarction by using dual isotopes of 201Tl and 99mTc-HL91. Nucl. Med. Commun. 29, 230–238.

    Article  PubMed  Google Scholar 

  • Yao H., Chen G., and Lu C. 1999. The identification of swine streptococcus isolates of jiangsu province in 1998. J. Nanjing Agricultural University 22, 67–70.

    CAS  Google Scholar 

  • Yu H., Jing H., Chen Z., Zheng H., Zhu X., Wang H., Wang S., Liu L., Zu R., Luo L., and et al. 2006. Human Streptococcus suis outbreak, sichuan, China. Emerg. Infect. Dis. 12, 914–920.

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang X.H., He K.W., Duan Z.T., Zhou J.M., Yu Z.Y., Ni Y.X., and Lu C.P. 2009. Identification and characterization of inosine 5-monophosphate dehydrogenase in Streptococcus suis type 2. Microb. Pathog. 47, 267–273.

    Article  CAS  PubMed  Google Scholar 

  • Zhang W. and Lu C.P. 2007. Immunoproteomics of extracellular proteins of Chinese virulent strains of Streptococcus suis type 2. Proteomics 7, 4468–4476.

    Article  CAS  PubMed  Google Scholar 

  • Zhang H., Ma Z., Li Y., Zheng J., Yi L., Fan H., and Lu C. 2013. Identification of a novel collagen type capital I-binding protein from Streptococcus suis serotype 2. Vet. J. 197, 406–414.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, P. R. China

    Hui Zhang, Junxi Zheng, Li Yi, Yue Li, Zhe Ma, Hongjie Fan & Chengping Lu

  2. China Animal Health and Epidemiology Center, Qingdao, P. R. China

    Hui Zhang

  3. Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009, P. R. China

    Hongjie Fan & Chengping Lu

Authors
  1. Hui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Junxi Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yue Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhe Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hongjie Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chengping Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hongjie Fan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, H., Zheng, J., Yi, L. et al. The identification of six novel proteins with fibronectin or collagen type I binding activity from Streptococcus suis serotype 2. J Microbiol. 52, 963–969 (2014). https://doi.org/10.1007/s12275-014-4311-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-014-4311-x

Keywords

Search

Navigation