Sialic acid-dependent interactions between influenza viruses and Streptococcus suis affect the infection of porcine tracheal cells

Wu, Nan-Lin; Meng, Fanxiang; Seitz, Maren; Valentin‐Weigand, Peter; Herrler, Georg

doi:10.1099/jgv.0.000223

Cited by 24 publications

(26 citation statements)

References 27 publications

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“…This result is most likely due to the presence of sialic acid on the capsular polysaccharide of wt strain 10 and the 10Δsly mutant. Recent studies have shown that the sialic acid binding activities of influenza viruses recognize the capsular sialic acid of S. suis, resulting in bacterial adherence to influenza virus-infected cells (6,10,19,20). The 10Δsly mutant is encapsulated and, therefore, can benefit from this adherence mechanism, too.…”

Section: Resultsmentioning

confidence: 99%

“…Influenza virus infections may cause increased susceptibility to secondary bacterial pneumonia, resulting in increased morbidity and mortality rates in the human population; the mechanisms underlying this copathogenesis are not well understood (13,14). For S. suis, it has been shown that the interaction of influenza A virus hemagglutinins with capsular sialic acids results in the binding of streptococci to virus-infected cells (6,19,20). This adherence mechanism is more efficient than the binding mediated by bacterial adhesins (6,10).…”

Section: Discussionmentioning

confidence: 99%

“…The major advantage of the coinfection, however, is the enhanced adherence efficiency. The sialic acid-dependent interaction between encapsulated streptococci and influenza virus hemagglutinins expressed on the surface of virus-infected cells is a very effective way for the attachment of bacteria to differentiated epithelial cells (19). Though suilysin has a positive effect on the adherence of S. suis to uninfected airway epithelial cells, this binding is less efficient than that to virus-infected cells, which is evident from a comparison of the binding of suilysin-deficient bacteria to virus-infected cells and the binding of wt streptococci to uninfected cells.…”

Section: Discussionmentioning

confidence: 99%

“…Coinfections with influenza viruses may affect the course of Streptococcus suis infections, as has been shown recently in a precision-cut lung slice model and in immortalized cells (6,19,20). S. suis is an important bacterial pathogen causing a number of infectious disease syndromes in pigs worldwide, including arthritis, septicemia, meningitis, and pneumonia (21,22), and it has been described to be an emerging zoonotic pathogen posing a potential risk for global public health (21,23).…”

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confidence: 90%

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Viral Coinfection Replaces Effects of Suilysin on Streptococcus suis Adherence to and Invasion of Respiratory Epithelial Cells Grown under Air-Liquid Interface Conditions

et al. 2019

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Streptococcus suis is an important zoonotic pathogen which can infect humans and pigs worldwide, posing a potential risk to global public health. Suilysin, a pore-forming cholesterol-dependent cytolysin, is considered to play an important role in the pathogenesis of S. suis infections. It is known that infection with influenza A viruses may favor susceptibility to secondary bacterial infection, resulting in more severe disease and increased mortality. However, the molecular mechanisms underlying these coinfections are incompletely understood. Applying highly differentiated primary porcine respiratory epithelial cells grown under air-liquid interface (ALI) conditions, we analyzed the contribution of swine influenza viruses (SIV) to the virulence of S. suis, with a special focus on its cytolytic toxin, suilysin. We found that during secondary bacterial infection, suilysin of S. suis contributed to the damage of well-differentiated respiratory epithelial cells in the early stage of infection, whereas the cytotoxic effects induced by SIV became prominent at later stages of infection. Prior infection by SIV enhanced the adherence to and colonization of porcine airway epithelial cells by a wild-type (wt) S. suis strain and a suilysin-negative S. suis mutant in a sialic acid-dependent manner. A striking difference was observed with respect to bacterial invasion. After bacterial monoinfection, only the wt S. suis strain showed an invasive phenotype, whereas the mutant remained adherent. When the epithelial cells were preinfected with SIV, the suilysin-negative mutant also showed an invasion capacity. Therefore, we propose that coinfection with SIV may compensate for the lack of suilysin in the adherence and invasion process of suilysin-negative S. suis. FIG 4Invasion of the bronchiolar epithelium by S. suis after preinfection with SIV. PBEC were preinfected with 5 ϫ 10 4 TCID 50 /filter H3N2 for 24 h, subsequently inoculated with S. suis wt strain 10 or the 10Δsly mutant at 2.5 ϫ 10 7 /filter from the apical compartment for 4 h, and then washed thoroughly to remove nonadherent bacteria and further incubated under ALI conditions until 48 hpi. Before fixation, the infected cells were washed with PBS to remove nonadherent bacteria. PBEC monoinfected with S. suis wt strain 10, the 10Δsly mutant, or H3N2 and mock-infected cells served as controls. (A) Immunostaining detection for colocalization of streptococci with H3N2-infected cells in the bronchiolar epithelium. Streptococci are labeled in green, nucleoproteins of H3N2 are stained in red, and nuclei are shown in blue (DAPI). The areas in the squares in the center of the panels in the bottom row are magnified in the insets at the top left of those panels. Bars, 25 m. (B) Immunostaining detection for invasion of streptococci into the bronchiolar epithelium, with vertical sections of PBEC being shown. Streptococci are labeled in green, nucleoproteins of H3N2 are stained in red, and nuclei are shown in blue (DAPI). White arrows indicate tissue-invasive bacteria, and the dashed...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 90%

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Viral Coinfection Replaces Effects of Suilysin on Streptococcus suis Adherence to and Invasion of Respiratory Epithelial Cells Grown under Air-Liquid Interface Conditions

et al. 2019

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“…Lectin staining was performed with Sambucus nigra agglutinin (SNA) or Maackia amurensis agglutinin II (MAAII)34. The binding of biotinylated lectins was visualized by fluorescence microscopy using streptavidin-Cy3 (Sigma) or streptavidin-DyLight 488 (Vector laboratories).…”

Section: Methodsmentioning

confidence: 99%

The differentiated airway epithelium infected by influenza viruses maintains the barrier function despite a dramatic loss of ciliated cells

Yang

Beineke³

et al. 2016

Sci Rep

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108

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Virus-host interactions in the respiratory epithelium during long term influenza virus infection are not well characterized. Therefore, we developed an air-liquid interface culture system for differentiated porcine respiratory epithelial cells to study the effect of virus-induced cellular damage. In our well-differentiated cells, α2,6-linked sialic acid is predominantly expressed on the apical surface and the basal cells mainly express α2,3-linked sialic acid. During the whole infection period, release of infectious virus was maintained at a high titre for more than seven days. The infected epithelial cells were subject to apoptosis resulting in the loss of ciliated cells together with a thinner thickness. Nevertheless, the airway epithelium maintained trans-epithelial electrical resistance and retained its barrier function. The loss of ciliated cells was compensated by the cells which contained the KRT5 basal cell marker but were not yet differentiated into ciliated cells. These specialized cells showed an increase of α2,3-linked sialic acid on the apical surface. In sum, our results help to explain the localized infection of the airway epithelium by influenza viruses. The impairment of mucociliary clearance in the epithelial cells provides an explanation why prior viral infection renders the host more susceptible to secondary co-infection by another pathogen.

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Close Encounters of the Viral Kind: Cross‐Kingdom Synergies at the Host–Pathogen Interface

Rowe

Rosch

2019

BioEssays

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The synergies between viral and bacterial infections are well established. Most studies have been focused on the indirect mechanisms underlying this phenomenon, including immune modulation and alterations to the mucosal structures that promote pathogen outgrowth. A growing body of evidence implicates direct binding of virus to bacterial surfaces being an additional mechanism of synergy at the host-pathogen interface. These cross-kingdom interactions enhance bacterial and viral adhesion and can alter tissue tropism. These bacterial-viral complexes play unique roles in pathogenesis and can alter virulence potential. The bacterial-viral complexes may also play important roles in pathogen transmission. Additionally, the complexes are recognized by the host immune system in a distinct manner, thus presenting novel routes for vaccine development. These synergies are active for multiple species in both the respiratory and gastrointestinal tract, indicating that direct interactions between bacteria and virus to modulate host interactions are used by a diverse array of species.

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Sialic acid-dependent interactions between influenza viruses and Streptococcus suis affect the infection of porcine tracheal cells

Cited by 24 publications

References 27 publications

Viral Coinfection Replaces Effects of Suilysin on Streptococcus suis Adherence to and Invasion of Respiratory Epithelial Cells Grown under Air-Liquid Interface Conditions

Viral Coinfection Replaces Effects of Suilysin on Streptococcus suis Adherence to and Invasion of Respiratory Epithelial Cells Grown under Air-Liquid Interface Conditions

The differentiated airway epithelium infected by influenza viruses maintains the barrier function despite a dramatic loss of ciliated cells

Close Encounters of the Viral Kind: Cross‐Kingdom Synergies at the Host–Pathogen Interface

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