This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Bergmann, S.
Right arrow Articles by Hammerschmidt, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Bergmann, S.
Right arrow Articles by Hammerschmidt, S.

 Previous Article  |  Next Article 

Infection and Immunity, April 2004, p. 2416-2419, Vol. 72, No. 4
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.4.2416-2419.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Glyceraldehyde-3-Phosphate Dehydrogenase of Streptococcus pneumoniae Is a Surface-Displayed Plasminogen-Binding Protein

Simone Bergmann,1 Manfred Rohde,2 and Sven Hammerschmidt1*

Research Center for Infectious Diseases, University of Würzburg, Würzburg,1 GBF-German Research Centre for Biotechnology, Braunschweig, Germany2

Received 18 August 2003/ Returned for modification 7 November 2003/ Accepted 22 December 2003


arrow
ABSTRACT
 
The recruitment of plasminogen endows the bacterial cell surface of Streptococcus pneumoniae with proteolytic activity. In this study we demonstrate specific plasmin- and plasminogen-binding activity for the glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase (GAPDH), which is located in the cytoplasm as well as on the surface of pneumococci. GAPDH exhibits a high affinity for plasmin and a significantly lower affinity for plasminogen.


arrow
TEXT
 
A prerequisite for the invasiveness of a pathogen is the pathogen's ability to breach epithelial as well as endothelial barriers in order to gain access to the submucosa and blood. A successful strategy used by pathogenic bacteria to degrade the extracellular matrix and to promote invasiveness is the recruitment of proteolytic activity to the bacterial cell surface (19, 21). Streptococcus pneumoniae, a common etiologic agent of respiratory tract diseases and life-threatening invasive diseases, is able to capture plasminogen on the bacterial cell surface. Subsequent activation by tissue-type and urokinase-type eukaryotic plasminogen activators allows the bacteria to acquire surface-associated proteolytic activity (10, 17). Plasminogen, a glycoprotein, is the zymogen of the serine protease plasmin, which is a key enzyme of the fibrinolytic pathway (7). The acquired plasmin activity promotes dissemination and transmigration of the pathogen through reconstituted basement membranes (6, 10, 21).

Analysis of plasminogen binding to viable pneumococci by the method described by Scatchard (25) indicated the presence of more than one plasminogen receptor on the pneumococcal cell surface. A blot overlay with soluble radioiodinated human plasminogen showed binding to eight pneumococcal components (2). {alpha}-Enolase (Eno) was identified as the major plasminogen- and plasmin-binding protein of S. pneumoniae (2). A further peptide sequence, obtained by an N-terminal sequence analysis of excised proteins positive for plasminogen binding, showed 100% homology to the N-terminal sequence of glyceraldehyde-3-phosphate dehydrogenase (GAPDH; GapA) in S. pneumoniae strains (http://www.tigr.org/tigr-scripts/CMR2/CMRGenomes.spl) (16, 26). These results identified the GAPDH of S. pneumoniae, which is an essential enzyme of the glycolytic pathway, as a putative plasminogen-binding protein. For expression cloning of gapA, the gene was amplified by PCR using the chromosomal DNA of S. pneumoniae serotype 2 (ATCC 11733) and oligonucleotide primers SB 13 (5'-GGATCCTTGCTTGCACACTTGTTGAAATAC-3'), incorporating an in-frame BamHI restriction site at the 5' end, and SB 14 (5'-AAGCTTTTATTTAGCAATTTTTGCGAAGTATT-3'), incorporating an in-frame HindIII restriction site at the 3' end. The BamHI- and HindIII-digested PCR product was cloned into the similarly digested expression vector pQE30 (Qiagen). The purification of His-tagged GAPDH under native conditions was conducted according to a standard protocol (Qiagen). In order to identify the subcellular localization of GAPDH by immunoblot analysis, polyclonal antibodies against purified recombinant GAPDH were raised in rabbits by routine immunogenic procedures (Eurogentec). Results indicated the presence of GAPDH in both the cytoplasmic fraction and the cell surface protein fraction of S. pneumoniae (Fig. 1). A sequence comparison performed with the algorithm of Lipman and Pearson (18) revealed 89.0% identity to the group A streptococcal GAPDH Plr/streptococcal surface dehydrogenase and 85.2% identity to GapC in Streptococcus equisimilis (14, 20, 24). Plasminogen- and plasmin-binding activity, which is most likely mediated via C-terminal lysyl residues (28), to both streptococcal proteins has been reported. The pneumococcal GAPDH contains two C-terminal lysine amino acids which are separated by isoleucine and alanine. The C-terminal sequences (>40 amino acids) of the above-mentioned GAPDH proteins are 100% identical. Moreover, sequence comparison revealed identical C termini in the GAPDHs of Streptococcus agalactiae, Streptococcus dysgalactiae, and Streptococcus mutans (Table 1). Interestingly, the GAPDHs of streptococci of groups A, C, and G were recently identified as extracellular targets for a broad spectrum of extracellular matrix proteins and especially for plasmin and plasminogen (20, 22).



View larger version (8K):
[in this window]
[in a new window]
  		FIG. 1. Identification of the cellular distribution of the pneumococcal GAPDH. Immunoblot analysis, using anti-GAPDH antibodies, of the cell wall fraction (lane 1) and soluble fraction (lane 2) of S. pneumoniae R6x and of the soluble fraction of an S. pneumoniae eno internal deletion mutant expressing {alpha}-enolase with mutated plasminogen binding sites (lane 3).


View this table:
[in this window]
[in a new window]
  		TABLE 1. Comparison of GAPDH sequences and C-terminus identities among different streptococcal species

In order to demonstrate the plasminogen-binding activity of the pneumococcal GAPDH, total proteins of the serotype 2 strain and the serotype 2 eno internal deletion (enoint/del) mutant were incubated with immobilized plasminogen. The mutant expresses an {alpha}-enolase with a deletion of the C-terminal lysyl residues and amino acid substitutions in the internal plasminogen-binding motif of Eno. The Enoint/del mutant exhibited substantially reduced plasminogen-binding activity (3) and was used in order to avoid binding of the {alpha}-enolase to plasminogen. Plasminogen (obtained from Sigma or provided by K. Preissner, Giessen, Germany) was immobilized on a polyvinylidine fluoride membrane, and GAPDH binding was detected with polyclonal anti-GAPDH antiserum followed by horseradish peroxidase-conjugated anti-rabbit antibody. Results demonstrated a concentration-dependent GAPDH-plasminogen interaction, in which the protein-protein interaction depends on both the amount of immobilized plasminogen and the amount of soluble GAPDH (Fig. 2).



View larger version (12K):
[in this window]
[in a new window]
  		FIG. 2. Binding of pneumococcal GAPDH to plasminogen. Human plasminogen was immobilized in the different amounts indicated. GAPDH was purified under native conditions from the cytosolic compartment of the serotype 2 enoint/del mutant pneumococci (ATCC 11733). Rows 1 to 3, binding of GAPDH applied in serial dilutions (1:2).

In an attempt to visualize the subcellular localization of GAPDH and the binding of plasminogen to GAPDH protein, preembedding, labeling studies were carried out as recently demonstrated for Eno (2). The unencapsulated pneumococcal strain R6x and the encapsulated pneumococcal strains of serotypes 2 (ATCC 11733) and 35A (NCTC 10319) were prelabeled with polyclonal protein A-purified anti-GAPDH immunoglobulin G and 15-nm-diameter gold particles coupled to protein A before embedding. Ultrathin sections revealed that the GAPDH of S. pneumoniae resembles the {alpha}-enolase located on the bacterial cell surface of unencapsulated (Fig. 3B) and encapsulated (Fig. 3A and C) strains. These results indicate that the common surface disposition of GAPDH is independent of the state of capsular polysaccharide expression. The surface-located glycolytic enzymes of the Embden-Meyerhof-Parnas pathway and other surface-displayed proteins like PavA of S. pneumoniae (15) and FBP54 of Streptococcus pyogenes (8, 9) lack the classical secretion and anchoring mechanisms (11, 12, 27, 29) and thus constitute a novel class of exported proteins of gram-positive bacteria (5). The conditions and factors required for protein secretion, as well as the mechanism of anchoring these proteins, are not known. How plasminogen is bound to GAPDH or Eno through the capsule also remains unknown.



View larger version (99K):
[in this window]
[in a new window]
  		FIG. 3. Immunoelectron microscopic visualization of GAPDH on the surface of S. pneumoniae ATCC 11733 (type 2) (A), unencapsulated R6x (B), and S. pneumoniae NCTC 10319 (type 35A) (C). (A to C) GAPDH was visualized on the bacterial cell surfaces of ultrathin sections of preembedding labeled samples by using anti-GAPDH antibodies and protein A-15-nm-diameter gold particle studies. (D) Visualization of unspecific binding of protein A-15-nm-diameter gold particles to type 2 pneumococci.

The dynamics of GAPDH-plasminogen and GAPDH-plasmin complex formation and their dissociation were analyzed by surface plasmon resonance (SPR) technique. GAPDH was covalently immobilized on a BIAcore CM5 sensor chip as previously described (3, 23). The association and dissociation kinetics of Glu-plasminogen and plasmin (Sigma) to GAPDH were evaluated according to the heterogeneous ligand model (A + B1 {leftrightarrow} AB1; A + B2 {leftrightarrow} AB2). This revealed two equilibrium constants; for plasminogen, KD1 was equal to 4.3 x 10-7 M and KD2 was equal to 1.6 x 10-10 M, and for plasmin, KD1 was equal to 2.8 x 10-8 M and KD2 was equal to 5.2 x 10-8 M. Studies using SPR showed that the pneumococcal GAPDH had a higher affinity for the serine protease plasmin than for its zymogen plasminogen (Fig. 4), as has also been shown previously for the Plr/streptococcal surface dehydrogenase of group A streptococci (20). The differences between equilibrium constants are probably the result of conformationally dependent structure recognition by Plr of the plasmin or plasminogen molecule (4). The interaction of GAPDH and plasminogen produced lower equilibrium constants than the Eno-plasminogen dissociation and complex formation did (KD1, 8.6 x 10-8 M; KD2, 5.5 x 10-10 M) in S. pneumoniae (3), indicating a lower affinity of GAPDH for plasminogen. Pathogenic bacteria acquire proteolytic activity by the recruitment and subsequent activation of plasminogen. A recent study indicated that the nonglycolytic property of {alpha}-enolase contributes to the pathogenesis of pneumococci (3). The concerted action of both {alpha}-enolase and GAPDH on the bacterial cell surface might, therefore, result in an enhancement of the pathogen's ability to degrade the extracellular matrix and to invade host tissues.



View larger version (27K):
[in this window]
[in a new window]
  		FIG. 4. SPR measurements of GAPDH-plasminogen (A) and GAPDH-plasmin (B) interactions. Purified GAPDH protein was immobilized on a BIAcore CM5 sensor chip, and plasmin and plasminogen were used as the analyte. Binding kinetics and concentration dependence of binding of plasminogen and plasmin to GAPDH are shown as changes in plasmin resonance. Plasmin and plasminogen were used in concentrations of 500 (for plasminogen only), 250, 125, 62.5, 31.25, 15.625, 7.8, and 3.9 nM. The blank run was subtracted from the sensorgram. Pl and Plg, starts of injection; w, stop of injection; RU, relative units.


arrow
ACKNOWLEDGMENTS
 
We are grateful to U. Hentschel and J. Reidl for critical readings of the manuscript.

This work was partially supported by the Deutsche Forschungsgemeinschaft (Sonderforschungsbereich 587/479, Teilprojekt A6/A7 to S.H., and Ro 2407/1 to M.R.) and the Bundesministerium für Bildung und Forschung (CAPNetz to S. H.).


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Research Center for Infectious Diseases, University of Würzburg, Röntgenring 11, 97070 Würzburg, Germany. Phone: 0049-931-312153. Fax: 0049-931-312578 E-mail: s.hammerschmidt{at}mail.uni-wuerzburg.de. Back

Editor: V. J. DiRita


arrow
REFERENCES
 
    1
  1. Ajdic, D., W. M. McShan, R. E. McLaughlin, G. Savic, J. Chang, M. B. Carson, C. Primeaux, R. Tian, S. Kenton, H. Jia, S. Lin, Y. Qian, S. Li, H. Zhu, F. Najar, H. Lai, J. White, B. A. Roe, and J. J. Ferretti. 2002.Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc. Natl. Acad. Sci. USA 99:14434-14439.[Abstract/Free Full Text]
    2. 2
  2. Bergmann, S., M. Rohde, G. S. Chhatwal, and S. Hammerschmidt. 2001. {alpha}-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol. Microbiol. 40:1273-1287.[CrossRef][Medline]
    3. 3
  3. Bergmann, S., D. Wild, O. Diekmann, R. Frank, D. Bracht, G. S. Chhatwal, and S. Hammerschmidt. 2003. Identification of a novel plasmin(ogen)-binding motif in surface displayed {alpha}-enolase of Streptococcus pneumoniae. Mol. Microbiol. 49:411-423.[CrossRef][Medline]
    4. 4
  4. Broder, C. C., R. Lottenberg, and M. D. P. Boyle. 1989. Mapping of the human plasmin domain recognized by the unique plasmin receptor of group A streptococci. Infect. Immun. 57:2597-2605.[Abstract/Free Full Text]
    5. 5
  5. Chhatwal, G. S. 2002. Anchorless adhesins and invasins of Gram-positive bacteria: a new class of virulence factors. Trends Microbiol. 10:205-208.[CrossRef][Medline]
    6. 6
  6. Coleman, J. L., E. J. Roemer, and J. L. Benach. 1999. Plasmin-coated Borrelia burgdorferi degrades soluble and insoluble components of the mammalian extracellular matrix. Infect. Immun. 67:3929-3936.[Abstract/Free Full Text]
    7. 7
  7. Collen, D., and M. Verstraete. 1975. Molecular biology of human plasminogen. II. Metabolism in physiological and some pathological conditions in man. Thromb. Diath. Haemorrh. 34:403-408.[Medline]
    8. 8
  8. Courtney, H. S., J. B. Dale, and D. L. Hasty. 1996. Differential effects of the streptococcal fibronectin-binding protein, FBP54, on adhesion of group A streptococci to human buccal cells and HEp-2 tissue culture cells. Infect. Immun. 64:2415-2419.[Abstract]
    9. 9
  9. Courtney, H. S., Y. Li, J. B. Dale, and D. L. Hasty. 1994. Cloning, sequencing, and expression of a fibronectin/fibrinogen-binding protein from group A streptococci. Infect. Immun. 62:3937-3946.[Abstract/Free Full Text]
    10. 10
  10. Eberhard, T., G. Kronvall, and M. Ullberg. 1999. Surface bound plasmin promotes migration of Streptococcus pneumoniae through reconstituted basement membranes. Microb. Pathog. 26:175-181.[CrossRef][Medline]
    11. 11
  11. Fischetti V. A., V. Pancholi, and O. Schneewind. 1991. Common characteristics of the surface proteins from gram-positive cocci, p. 290-294. In G. M. Dunny, P. P. Cleary, and L. L. McKay (ed.), Genetics and molecular biology of streptococci, lactococci, and enterococci. American Society for Microbiology, Washington, D.C.
    12. 12
  12. Fischetti, V. A., V. Pancholi, and O. Schneewind. 1990. Conservation of a hexapeptide sequence in the anchor region of surface proteins from gram-positive cocci. Mol. Microbiol. 4:1603-1605.[Medline]
    13. 13
  13. Fontaine, M. C., J. Perez-Casal, X.-M. Song, J. Shelford, P. J. Willson, and A. A. Potter. 2002. Immunisation of dairy cattle with recombinant Streptococcus uberis GapC or a chimeric CAMP antigen confers protection against heterologous bacterial challenge. Vaccine 20:2278-2286.[CrossRef][Medline]
    14. 14
  14. Gase, K., A. Gase, H. Schirmer, and H. Malke. 1996. Cloning, sequencing and functional overexpression of the Streptococcus equisimilis H46A gapC gene encoding a glyceraldehyde-3-phosphate dehydrogenase that also functions as a plasmin(ogen)-binding protein. Purification and biochemical characterization of the protein. Eur. J. Biochem. 239:42-51.[Medline]
    15. 15
  15. Holmes, A. R., R. McNab, K. W. Millsap, M. Rohde, S. Hammerschmidt, J. L. Mawdsley, and H. F. Jenkinson. 2001. The pavA gene of Streptococcus pneumoniae encodes a fibronectin-binding protein that is essential for virulence. Mol. Microbiol. 41:1395-1408.[CrossRef][Medline]
    16. 16
  16. Hoskins, J., W. E. Alborn, Jr., J. Arnold, L. C. Blaszczak, S. Burgett, B. S. DeHoff, S. T. Estrem, L. Fritz, D.-J. Fu, W. Fuller, C. Geringer, R. Gilmour, J. S. Glass, H. Khoja, A. R. Kraft, R. E. Lagace, D. J. LeBlanc, L. N. Lee, E. J. Lefkowitz, J. Lu, P. Matsushima, S. M. McAhren, M. McHenney, K. McLeaster, C. W. Mundy, T. I. Nicas, F. H. Norris, M. O'Gara, R. B. Peery, G. T. Robertson, P. Rockey, P.-M. Sun, M. E. Winkler, Y. Yang, M. Young-Bellido, G. Zhao, C. A. Zook, R. H. Baltz, S. R. Jaskunas, P. R. Rosteck, Jr., P. L. Skatrud, and J. I. Glass. 2001. Genome of the bacterium Streptococcus pneumoniae strain R6. J. Bacteriol. 183:5709-5717.[Abstract/Free Full Text]
    17. 17
  17. Kuusela, P., M. Ullberg, O. Saksela, and G. Kronvall. 1992. Tissue-type plasminogen activator-mediated activation of plasminogen on the surface of group A, C, and G streptococci. Infect. Immun. 60:196-201.[Abstract/Free Full Text]
    18. 18
  18. Lipman, D. J., and W. R. Pearson. 1985. Rapid and sensitive protein similarity searches. Science 227:1435-1441.[Abstract/Free Full Text]
    19. 19
  19. Lottenberg, R. 1997. A novel approach to explore the role of plasminogen in bacterial pathogenesis. Trends Microbiol. 5:466-468.[CrossRef][Medline]
    20. 20
  20. Lottenberg, R., C. C. Broder, M. D. P. Boyle, S. J. Kain, B. L. Schroeder, and R. Curtiss III. 1992. Cloning, sequence analysis, and expression in Escherichia coli of a streptococcal plasmin receptor. J. Bacteriol. 174:5204-5210.[Abstract/Free Full Text]
    21. 21
  21. Lottenberg, R., D. Minning-Wenz, and M. D. Boyle. 1994. Capturing host plasmin(ogen): a common mechanism for invasive pathogens? Trends Microbiol. 2:20-24.[CrossRef][Medline]
    22. 22
  22. Modun, B., and P. Williams. 1999. The staphylococcal transferrin-binding protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase. Infect. Immun. 67:1086-1092.[Abstract/Free Full Text]
    23. 23
  23. Nice, E. C., T. L. McInerney, and D. C. Jackson. 1996. Analysis of the interaction between a synthetic peptide of influenza virus hemagglutinin and monoclonal antibody using an optical biosensor. Mol. Immunol. 33:659-670.[CrossRef][Medline]
    24. 24
  24. Pancholi, V., and V. A. Fischetti. 1992. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J. Exp. Med. 176:415-426.[Abstract/Free Full Text]
    25. 25
  25. Scatchard, G. 1949. The attraction of proteins for small molecules and ions. Ann. N. Y. Acad. Sci. 51:660-672.[CrossRef]
    26. 26
  26. Tettelin, H., K. E. Nelson, I. T. Paulsen, J. A. Eisen, T. D. Read, S. Peterson, J. Heidelberg, R. T. DeBoy, D. H. Haft, R. J. Dodson, A. S. Durkin, M. Gwinn, J. F. Kolonay, W. C. Nelson, J. D. Peterson, L. A. Umayam, O. White, S. L. Salzberg, M. R. Lewis, D. Radune, E. Holtzapple, H. Khouri, A. M. Wolf, T. R. Utterback, C. L. Hansen, L. A. McDonald, T. V. Feldblyum, S. Angiuoli, T. Dickinson, E. K. Hickey, I. E. Holt, B. J. Loftus, F. Yang, H. O. Smith, J. C. Venter, B. A. Dougherty, D. A. Morrison, S. K. Hollingshead, and C. M. Fraser. 2001. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293:498-506.[Abstract/Free Full Text]
    27. 27
  27. von Heijne, G. 1986. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14:4683-4690.[Abstract/Free Full Text]
    28. 28
  28. Winram, S. B., and R. Lottenberg. 1998. Site-directed mutagenesis of streptococcal plasmin receptor protein (Plr) identifies the C-terminal Lys334 as essential for plasmin binding, but mutation of the plr gene does not reduce plasmin binding to group A streptococci. Microbiology 144:2025-2035.[Abstract/Free Full Text]
    29. 29
  29. Yother, J., and J. M. White. 1994. Novel surface attachment mechanism of the Streptococcus pneumoniae protein PspA. J. Bacteriol. 176:2976-2985.[Abstract/Free Full Text]

Infection and Immunity, April 2004, p. 2416-2419, Vol. 72, No. 4
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.4.2416-2419.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Nobbs, A. H., Lamont, R. J., Jenkinson, H. F. (2009). Streptococcus Adherence and Colonization. Microbiol. Mol. Biol. Rev. 73: 407-450 [Abstract] [Full Text]  
  • Furuya, H., Ikeda, R. (2009). Interaction of triosephosphate isomerase from the cell surface of Staphylococcus aureus and {alpha}-(1->3)-mannooligosaccharides derived from glucuronoxylomannan of Cryptococcus neoformans. Microbiology 155: 2707-2713 [Abstract] [Full Text]  
  • Lama, A., Kucknoor, A., Mundodi, V., Alderete, J. F. (2009). Glyceraldehyde-3-Phosphate Dehydrogenase Is a Surface-Associated, Fibronectin-Binding Protein of Trichomonas vaginalis. Infect. Immun. 77: 2703-2711 [Abstract] [Full Text]  
  • Cron, L. E., Bootsma, H. J., Noske, N., Burghout, P., Hammerschmidt, S., Hermans, P. W. M. (2009). Surface-associated lipoprotein PpmA of Streptococcus pneumoniae is involved in colonization in a strain-specific manner. Microbiology 155: 2401-2410 [Abstract] [Full Text]  
  • Yamaguchi, M., Terao, Y., Mori, Y., Hamada, S., Kawabata, S. (2008). PfbA, a Novel Plasmin- and Fibronectin-binding Protein of Streptococcus pneumoniae, Contributes to Fibronectin-dependent Adhesion and Antiphagocytosis. J. Biol. Chem. 283: 36272-36279 [Abstract] [Full Text]  
  • Attali, C., Durmort, C., Vernet, T., Di Guilmi, A. M. (2008). The Interaction of Streptococcus pneumoniae with Plasmin Mediates Transmigration across Endothelial and Epithelial Monolayers by Intercellular Junction Cleavage. Infect. Immun. 76: 5350-5356 [Abstract] [Full Text]  
  • Mundodi, V., Kucknoor, A. S., Alderete, J. F. (2008). Immunogenic and Plasminogen-Binding Surface-Associated {alpha}-Enolase of Trichomonas vaginalis. Infect. Immun. 76: 523-531 [Abstract] [Full Text]  
  • Attali, C., Frolet, C., Durmort, C., Offant, J., Vernet, T., Di Guilmi, A. M. (2008). Streptococcus pneumoniae Choline-Binding Protein E Interaction with Plasminogen/Plasmin Stimulates Migration across the Extracellular Matrix. Infect. Immun. 76: 466-476 [Abstract] [Full Text]  
  • Wang, L., Makino, S., Subedee, A., Bogdanove, A. J. (2007). Novel Candidate Virulence Factors in Rice Pathogen Xanthomonas oryzae pv. oryzicola as Revealed by Mutational Analysis. Appl. Environ. Microbiol. 73: 8023-8027 [Abstract] [Full Text]  
  • Yavlovich, A., Rechnitzer, H., Rottem, S. (2007). {alpha}-Enolase Resides on the Cell Surface of Mycoplasma fermentans and Binds Plasminogen. Infect. Immun. 75: 5716-5719 [Abstract] [Full Text]  
  • Kunert, A., Losse, J., Gruszin, C., Huhn, M., Kaendler, K., Mikkat, S., Volke, D., Hoffmann, R., Jokiranta, T. S., Seeberger, H., Moellmann, U., Hellwage, J., Zipfel, P. F. (2007). Immune Evasion of the Human Pathogen Pseudomonas aeruginosa: Elongation Factor Tuf Is a Factor H and Plasminogen Binding Protein. J. Immunol. 179: 2979-2988 [Abstract] [Full Text]  
  • Ikeda, R., Saito, F., Matsuo, M., Kurokawa, K., Sekimizu, K., Yamaguchi, M., Kawamoto, S. (2007). Contribution of the Mannan Backbone of Cryptococcal Glucuronoxylomannan and a Glycolytic Enzyme of Staphylococcus aureus to Contact-Mediated Killing of Cryptococcus neoformans. J. Bacteriol. 189: 4815-4826 [Abstract] [Full Text]  
  • Antikainen, J., Kupannen, V., Lahteenmaki, K., Korhonen, T. K. (2007). pH-Dependent Association of Enolase and Glyceraldehyde-3-Phosphate Dehydrogenase of Lactobacillus crispatus with the Cell Wall and Lipoteichoic Acids. J. Bacteriol. 189: 4539-4543 [Abstract] [Full Text]  
  • Knaust, A., Weber, M. V. R., Hammerschmidt, S., Bergmann, S., Frosch, M., Kurzai, O. (2007). Cytosolic Proteins Contribute to Surface Plasminogen Recruitment of Neisseria meningitidis. J. Bacteriol. 189: 3246-3255 [Abstract] [Full Text]  
  • Madureira, P., Baptista, M., Vieira, M., Magalhaes, V., Camelo, A., Oliveira, L., Ribeiro, A., Tavares, D., Trieu-Cuot, P., Vilanova, M., Ferreira, P. (2007). Streptococcus agalactiae GAPDH Is a Virulence-Associated Immunomodulatory Protein. J. Immunol. 178: 1379-1387 [Abstract] [Full Text]  
  • Kolberg, J., Aase, A., Bergmann, S., Herstad, T. K., Rodal, G., Frank, R., Rohde, M., Hammerschmidt, S. (2006). Streptococcus pneumoniae enolase is important for plasminogen binding despite low abundance of enolase protein on the bacterial cell surface.. Microbiology 152: 1307-1317 [Abstract] [Full Text]  
  • Allegrucci, M., Hu, F. Z., Shen, K., Hayes, J., Ehrlich, G. D., Post, J. C., Sauer, K. (2006). Phenotypic Characterization of Streptococcus pneumoniae Biofilm Development.. J. Bacteriol. 188: 2325-2335 [Abstract] [Full Text]  
  • Bergmann, S., Hammerschmidt, S. (2006). Versatility of pneumococcal surface proteins. Microbiology 152: 295-303 [Abstract] [Full Text]  
  • Hermans, P. W. M., Adrian, P. V., Albert, C., Estevao, S., Hoogenboezem, T., Luijendijk, I. H. T., Kamphausen, T., Hammerschmidt, S. (2006). The Streptococcal Lipoprotein Rotamase A (SlrA) Is a Functional Peptidyl-prolyl Isomerase Involved in Pneumococcal Colonization. J. Biol. Chem. 281: 968-976 [Abstract] [Full Text]  
  • Guiral, S., Mitchell, T. J., Martin, B., Claverys, J.-P. (2005). From The Cover: Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: Genetic requirements. Proc. Natl. Acad. Sci. USA 102: 8710-8715 [Abstract] [Full Text]  
  • Green, B. A., Zhang, Y., Masi, A. W., Barniak, V., Wetherell, M., Smith, R. P., Reddy, M. S., Zhu, D. (2005). PppA, a Surface-Exposed Protein of Streptococcus pneumoniae, Elicits Cross-Reactive Antibodies That Reduce Colonization in a Murine Intranasal Immunization and Challenge Model. Infect. Immun. 73: 981-989 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Bergmann, S.
Right arrow Articles by Hammerschmidt, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Bergmann, S.
Right arrow Articles by Hammerschmidt, S.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»