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Infection and Immunity, January 2004, p. 606-610, Vol. 72, No. 1
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.1.606-610.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Acquisition of Host Plasmin Activity by the Swine Pathogen Streptococcus suis Serotype 2

Marie-Claude Jobin,¹ Julie Brassard,² Sylvain Quessy,^2,3 Marcelo Gottschalk,^2,3 and Daniel Grenier^1,3*

Groupe de Recherche en Écologie Buccale, Faculté de Médecine Dentaire, Université Laval, Quebec City,¹ Groupe de Recherche sur les Maladies Infectieuses du Porc,² Canadian Research Network on Bacterial Pathogens of Swine (Natural Sciences and Engineering Research Council of Canada), Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Quebec, Canada³

Received 23 July 2003/ Returned for modification 3 September 2003/ Accepted 8 October 2003

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In this study, the plasminogen-binding activity of Streptococcus suis serotype 2 was investigated. Bound human plasminogen was activated by purified streptokinase, urokinase, or Streptococcus dysgalactiae subsp. equisimilis culture supernatant. Both human and porcine plasminogen were bound by S. suis. Binding was inhibited by -aminocaproic acid, and the plasminogen receptor was heat and sodium dodecyl sulfate resistant. One of the receptors was identified as glyceraldehyde-3-phosphate dehydrogenase. S. suis-associated plasmin activity was capable of activating free plasminogen, which in turn could contribute to degradation of fibronectin. This is the first report on the plasminogen-binding activity of S. suis. Further studies may reveal a contribution of this activity to the virulence of S. suis.

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Streptococcus suis, an important swine pathogen worldwide, is made up of 35 serotypes (1 to 34 and 1/2) (12). Although all serotypes can cause infections, serotype 2 is the most prevalent one isolated from diseased pigs (9, 11). Septicemia, arthritis, meningitis, and sudden death are the most important clinical signs associated with S. suis infections (11). Cases of meningitis and endocarditis caused by S. suis have also been reported in workers associated with the pig industry (11). Although several S. suis virulence factors have been identified and characterized, the exact mechanisms by which this bacterium invades the host and causes infections are still unclear. The only factor considered essential for the pathogenicity of S. suis is the polysaccharide capsule (3). An important feature, which could play an important role in the pathogenicity of S. suis, is its ability to bind host proteins, which may camouflage it and thus protect it from the host immune system. Fibronectin (7), albumin (21), and immunoglobulin G (1, 23) receptors have been identified on the cell surface of S. suis and have been proposed as virulence factors.

Plasminogen is a 92-kDa protein that is an important component of the fibrinolytic system. Its activation into plasmin, a serine protease, is tightly regulated by the equilibrium between plasmin activators (urokinase plasmin activator [u-PA] as well as tissue plasminogen activator) and inhibitors (2-antiplasmin and 2-macroglobulin) (15). Plasminogen can also be activated by microbial products including streptokinase and staphylokinase produced by group A streptococci and Staphylococcus aureus, respectively (15). Many group A and C streptococci bind plasminogen on their cell surfaces (15). In a number of cases, the receptors have been characterized and identified as glyceraldehyde-3-phosphate dehydrogenase (GAPDH) or -enolase (17, 19, 20, 24). The plasmin activity generated on the bacterial cell surface is protected from host inhibitors and can activate latent u-PA and tissue plasminogen activator, which subsequently activate plasminogen (15). This mechanism of acquisition of a host proteinase activity increases the invasive potential of some pathogens, including Streptococcus pneumoniae (8). The purpose of the study reported here was to investigate the capacity of S. suis to bind plasminogen and acquire plasmin activity.

Bacterial strains. The reference S. suis serotype 2 strain (S735) was used throughout this study. Other strains from serotype 2 (31533, 89-999, 94-623, 93-1330, 94-3037, and Reims), serotype 1 (S428), serotype 1/2 (2651), serotype 3 (4961), and serotype 5 (Amy12C and 4B) were tested for their plasminogen-binding capacity. The strains were grown at 37°C under aerobic conditions in Todd-Hewitt broth (THB; BBL Becton Dickinson, Cockeysville, Md.). An S. suis mutant lacking cell surface GAPDH activity, which was constructed for a previous study using Tn916, was also used (2). The mutant strain was grown in THB containing tetracycline (10 µg/ml) and streptomycin (80 µg/ml). Bacterial cells from a 6-h culture (late exponential growth phase) were harvested by centrifugation (10,000 x g for 15 min) and suspended in phosphate-buffered saline (50 mM, pH 7.2) to an optical density at 660 nm of 1.0, which corresponded to approximately 2.3 x 10⁹ bacteria/ml as determined using a Petroff-Hausser counting chamber.

Culture supernatants of Streptococcus agalactiae ATCC 13813, Streptococcus dysgalactiae subsp. dysgalactiae ATCC 27957, Streptococcus equi subsp. zooepidemicus ATCC 6580 and ATCC 43079, and Streptococcus dysgalactiae subsp. equisimilis ATCC 9542 were harvested to investigate the presence of plasminogen activator. Bacteria were grown overnight in THB at 37°C for 18 h. The supernatants were collected by centrifugation (10,000 x g for 15 min), and residual bacteria were removed by filtration through a 0.22-µm-pore-size filter.

ELISA for determining plasminogen-binding activity and the effect of various conditions and treatments. The plasminogen-binding activity of the S. suis cells was quantified using an enzyme-linked immunosorbent assay (ELISA). Bacterial suspensions (100 µl) were placed in the wells of a MaxiSorp Nunc Immuno plate (Nalge Nunc International, Roskilde, Denmark), which was covered and incubated overnight at 37°C. Nonattached cells were removed and unreacted sites were blocked prior to addition of 100 µl of human plasminogen (0.0294 U/ml; Sigma Chemical Co., St. Louis, Mo.). Human serum (ICN Biomedicals Inc., Irvine, Calif.) and plasma (Sigma) as well as pig serum (ICN) and plasma (Sigma) were also tested as sources of plasminogen. The bound plasminogen was detected with 100 µl of goat anti-human plasminogen polyclonal antibody (1/5,000; Sigma) or 100 µl of a rabbit anti-porcine plasminogen (1/4,000; Biogenesis, Kingston, N.H.) as primary antibody. The secondary antibody was an alkaline phosphatase-conjugated rabbit anti-goat immunoglobulin G antibody (1/30,000; Sigma) or alkaline phosphatase-conjugated goat anti-rabbit immunoglobulin G (1/2,500; Sigma). Detection was done in the presence of p-nitrophenyl phosphate in sodium carbonate buffer (50 mM, pH 9.5) and the absorbance at 405 nm (A₄₀₅) was measured using an ELISA microtiter plate reader.

The effect of pH was tested using 50 mM phosphate buffer adjusted to pHs ranging from 5 to 10 during the incubation of the plasminogen with the cells. The effect of salt concentration was tested using phosphate buffer (pH 7.2) containing 0, 0.075, 0.15, or 0.225 M NaCl. The effect of temperature was tested using bacterial cells treated for 30 min at various temperatures (37, 56, 75, and 100°C). Lastly, plasminogen-binding activity was evaluated in the presence of EDTA (10 mM), lysine analog -aminocaproic acid (EACA; 10 mM), human fibronectin, human fibrinogen, porcine fibrinogen, human immunoglobulin G, human albumin, and porcine albumin (100 µg/ml).

Purification of S. suis GAPDH and analysis of its plasminogen-binding activity. S. suis S735 GAPDH was cloned and overexpressed in Escherichia coli M15 [pREP4-pQE-301] as previously described (2). Following cell lysis, the supernatant was saved for the purification of the (His)₆GAPDH by Ni²⁺-nitrilotriacetic acid affinity chromatography as described in the QIAexpress manual provided by the manufacturer (Qiagen, Mississauga, Ontario, Canada). The fractions containing (His)₆GAPDH were pooled and stored at -20°C. Purified GAPDH (5 µg) was loaded on a sodium dodecyl sulfate (SDS)-10% polyacrylamide gel. Electrophoresis was performed at room temperature with the buffer system of Laemmli (14), and the proteins were transferred to a nitrocellulose membrane. The membrane was blocked and incubated with plasminogen. Bound plasminogen was detected with the antibodies described above. Reactions were detected using a solution of nitroblue tetrazolium chloride and 5-bromo-4-chloro-3-indolylphosphate toluidine salt in carbonate buffer.

Activation of plasminogen bound to S. suis and detection of plasmin activity. S. suis cells were incubated for 2 h with human plasminogen (0.15 U/ml) or were suspended in whole human serum (ICN) at 37°C with gentle shaking. The bacteria were then washed prior to addition of streptokinase (25 U/ml; Sigma) or urokinase (0.15 U/ml; Sigma). Following a 1-h incubation at 37°C, the cells were harvested by centrifugation (10,000 x g for 15 min), washed to remove any residual plasminogen activator, and suspended in phosphate-buffered saline. Activation of plasminogen bound to S. suis by culture supernatants of S. agalactiae, S. dysgalactiae subsp. dysgalactiae, S. equi subsp. zooepidemicus, and S. dysgalactiae subsp. equisimilis was also tested by suspending S. suis cells coated with plasminogen in the supernatant. Plasmin activity was determined by zymography as described previously (26), with some modifications. Gelatin (final concentration of 0.03%) was incorporated into a 10% polyacrylamide gel containing SDS. Cell samples were mixed with electrophoresis buffer, and the electrophoresis was carried out on ice at a constant voltage of 100 V. The gels were washed with washing buffer (0.05 M Tris-HCl, pH 7.5) and then incubated in equilibration buffer (0.05 M Tris-HCl, 0.1 M NaCl, 2.5% Triton X-100, pH 7.5). The equilibration buffer was replaced by the washing buffer for 15 min. Reaction buffer (0.05 M Tris, 0.1 M NaCl, 0.01 M CaCl₂, pH 7.5) was added, and the gels were incubated overnight at 37°C with gentle shaking. Proteolysis zones were detected by Coomassie blue R-250 staining and destaining (2:3:15 methanol/acetic acid/water ratio).

The effect of providing additional free plasminogen to S. suis cells coated with plasminogen, subsequently activated with streptokinase, was investigated. Plasminogen was added to a concentration of 0.15 U/ml to 100 µl of bacteria that were covered with plasminogen prior to addition of 20 µl of the chromogenic peptide Val-Leu-Lys-p-nitroanilide (2 mg/ml). The mixture was incubated at 37°C for 1.5 h and centrifuged to remove the cells, and the A₄₀₅ of the supernatant was measured. Similarly, the degradation of human fibronectin, type IV collagen, and laminin (0.5 mg/ml) was evaluated following the addition of free plasminogen to S. suis cells coated with plasminogen and activated or not with streptokinase. The mixture was incubated for 4 h at 37°C, and the cells were removed. The supernatant was loaded on a 7.5% polyacrylamide gel, and the electrophoresis was performed as described above. Proteins were stained with Coomassie blue R-250.

Binding of plasminogen to the cell surface of S. suis S735 was clearly demonstrated by an ELISA using commercial human plasminogen (Fig. 1). In the control assay where the incubation step with plasminogen was omitted, weak nonspecific attachment of goat anti-human plasminogen antibody to S. suis was detected. When immobilized S. suis cells were incubated with either human or pig serum or plasma instead of commercial human plasminogen, cell-bound plasminogen was also detected (data not shown). Other strains of S. suis serotype 2 (virulent and nonvirulent in an animal model) and serotypes 1, 1/2, 3, and 5 were tested, and all had the capacity to bind human and pig plasminogen (data not shown).

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FIG. 1. Determination of the plasminogen-binding activity of S. suis by ELISA and the effects of various inhibitors and conditions.

Plasminogen kringle domains often mediate interactions with lysine residues in receptors (15). To evaluate the involvement of these domains in the interaction of plasminogen with S. suis, the binding assay was carried out in the presence of EACA, a lysine analog. EACA was an efficient inhibitor (85 to 90% inhibition) of plasminogen binding to S. suis (Fig. 1), suggesting that the kringle domains are involved in the binding process. The interaction did not require cations since EDTA had no inhibitory effect on binding (Fig. 1). Several plasma proteins were tested for their ability to reduce plasminogen binding, since previous studies reported that S. suis binds immunoglobulin G, fibronectin, and albumin (7, 21, 23). No plasma proteins significantly interfered with plasminogen binding, suggesting that there is a specific plasminogen receptor. However, it is possible that the receptors on the S. suis surface possess a higher affinity for plasminogen than for the other proteins tested. The receptor was also resistant to heating (Fig. 1), as are the S. suis immunoglobulin G and fibronectin receptors previously reported (7, 23). The interaction of plasminogen with S. suis S735 was not affected at the pHs (5 to 10) or salt concentrations (0 to 0.225 M) tested (data not shown). The plasminogen-binding capabilities of Borrelia burgdorferi (13), Streptococcus uberis (16), Mycoplasma fermentans (27), and Fusobacterium nucleatum (5) are also inhibited by EACA, but not EDTA. There is thus a strong similarity between the receptors of these pathogens and that of S. suis.

GAPDH is a known plasminogen receptor in group A streptococci (20, 24). GAPDH was cloned from the S. suis genome, overexpressed in E. coli, and tested for its capacity to bind human plasminogen by SDS-polyacrylamide gel electrophoresis (PAGE) and Western immunoblotting analyses. As shown in Fig. 2, bound plasminogen was clearly detected as a band with a molecular mass of 37 kDa, which corresponds to purified GAPDH. The method used (SDS-PAGE and Western immunoblotting) confirmed that the receptor is highly stable (heat and SDS stability). An S. suis S735 mutant lacking surface-associated GAPDH activity was tested for its capability to bind plasminogen in the ELISA. A 25% reduction in binding compared to the wild-type S. suis S735 strain was observed, suggesting that there is likely more than one type of plasminogen receptor on the bacterial surface. Interestingly, proteomic analysis identified eight major plasminogen-binding proteins in cell wall protein extracts of the human pathogenic fungus Candida albicans (4). Further studies are required to identify additional S. suis plasminogen receptors.

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FIG. 2. Demonstration of the plasminogen-binding activity of purified S. suis GAPDH by SDS-PAGE and Western immunoblotting analyses. The purified GAPDH was made to migrate by electrophoresis, and the nitrocellulose membrane was incubated (lane 2) or not (lane 1) with human plasminogen. Bound plasminogen was detected as described in the text.

Under the conditions tested, no plasminogen activators were produced by S. suis. However, the gelatinase bands observed in Fig. 3 (lanes 6, 9, and 12) indicate that the plasminogen bound to S. suis following incubation of bacteria in human serum could be activated by an external activator including streptokinase, urokinase, or supernatant from S. dysgalactiae subsp. equisimilis, a bacterium that cohabits with S. suis. Studies in progress in our laboratory are investigating whether S. suis can upregulate u-PA production by host cells, as previously demonstrated with S. aureus (28). The secretion of u-PA by human monocytes is regulated by interleukin-1 (12). Interestingly, Segura et al. (22) demonstrated that S. suis induces an increase in interleukin-1 production by human monocytic THP-1 cells. This phenomenon might thus promote the production of u-PA in vivo, which in turn would activate plasminogen bound to S. suis.

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FIG. 3. Detection of plasmin activity by zymography. S. suis cells were untreated (lane 1) or incubated with human plasminogen (lane 2), human serum (lane 3), urokinase (lane 4), human plasminogen and then urokinase (lane 5), human serum and then urokinase (lane 6), streptokinase (lane 7), human plasminogen and then streptokinase (lane 8), human serum and then streptokinase (lane 9), S. dysgalactiae subsp. equisimilis supernatant (lane 10), human plasminogen and then S. dysgalactiae subsp. equisimilis supernatant (lane 11), or human serum and then S. dysgalactiae subsp. equisimilis supernatant (lane 12).

Plasminogen bound to S. suis and subsequently activated into plasmin may interact with the extracellular matrix (6). Free unactivated plasminogen was added to S. suis cells coated with plasminogen subsequently activated by streptokinase, urokinase, or S. dysgalactiae subsp. equisimilis culture supernatant to determine the ability of the cells to activate unbound plasminogen. The results presented in Fig. 4 show that large amounts of unbound plasminogen were activated by streptokinase-activated plasminogen-coated cells. The activation was strongest in the case of streptokinase, for which the plasmin activity observed after 1.5 h with the chromogenic plasmin substrate was equivalent to the value obtained after 18 h of incubation without additional plasminogen. No further activation of free plasminogen by urokinase-activated plasminogen-coated S. suis was observed (data not shown). Among the matrix proteins tested, only fibronectin was degraded by S. suis cells coated with plasminogen treated with streptokinase and for which free plasminogen was added (Fig. 5). If such a phenomenon occurs in vivo, it may promote alteration of the basal membrane integrity and enhance bacterial penetration of infected tissues. The degradation of fibronectin observed in the present study may also have an impact on the inflammatory process. Indeed, fibronectin fragments are chemotactic for human monocytes (18) and may enhance matrix metalloproteinase production (25). These two consequences of fibronectin degradation, leading to an enhanced degradation of host tissues, may thus participate in the dissemination of S. suis and should thus be further investigated.

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FIG. 4. Activation of free plasminogen by the plasmin activity associated with S. suis. S. suis was incubated with streptokinase plus additional plasminogen (A), plasminogen and then streptokinase (B), plasminogen and then streptokinase plus additional plasminogen (C), S. dysgalactiae subsp. equisimilis culture supernatant plus additional plasminogen (D), plasminogen and then S. dysgalactiae subsp. equisimilis culture supernatant (E), plasminogen and then S. dysgalactiae subsp. equisimilis culture supernatant plus additional plasminogen (F), or plasminogen (G).

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FIG. 5. Degradation of human fibronectin by S. suis coated with plasminogen and treated with streptokinase and for which free plasminogen was added. Lanes 1 to 3, S. suis incubated with plasminogen and then streptokinase plus additional plasminogen, streptokinase plus additional plasminogen, or plasminogen and then streptokinase, respectively; lane 4, control (fibronectin alone).

In this study, we demonstrated the capacity of S. suis to bind human and pig plasminogens and identified one of the receptors as GAPDH. The fact that all strains tested (virulent and nonvirulent in an animal model) were capable of binding plasminogen does not exclude participation of this activity in the pathogenic process of S. suis infections. Indeed, pathogenicity is often the result of multiple virulence factors, which may be shared by virulent and nonvirulent strains. We also showed that the bound plasminogen could be activated into plasmin by an exogenous activator, thus increasing the proteolytic potential of S. suis. As with other pathogens, this interaction with plasminogen may contribute to tissue invasion and destruction by S. suis. Further studies are needed to determine the pathological and physiological functions of the plasminogen-binding activity of S. suis.

 
This work was supported by the Canadian Research Network on Bacterial Pathogens of Swine (Natural Sciences and Engineering Research Council of Canada).

 
* Corresponding author. Mailing address: Groupe de Recherche en Écologie Buccale, Faculté de Médecine Dentaire, Université Laval, Quebec City, Quebec, Canada G1K 7P4. Phone: (418) 656-7341. Fax: (418) 656-2861. E-mail: Daniel.Grenier{at}greb.ulaval.ca.

Editor: W. A. Petri, Jr.

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Infection and Immunity, January 2004, p. 606-610, Vol. 72, No. 1
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.1.606-610.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

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