Serine-rich repeat adhesins mediate shear-enhanced streptococcal binding to platelets

Olga Yakovenko, Jamie Nunez, Barbara Bensing, Hai Yu, Jonathan Mount, Jie Zeng, Jasmine Hawkins, Xi Chen, Paul M. Sullam, Wendy Thomas

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

The binding of bacteria to platelets is thought to be a central event in the pathogenesis of infective endocarditis. The serine-rich repeat (SRR) glycoproteins of viridans group streptococci have been shown to mediate platelet binding in vitro and to contribute to virulence in animal models. However, it is not known whether SRR adhesins can mediate streptococcal binding under the high fluidic shear stress conditions present on the endocardial surface. We found that three streptococcal SRR adhesins (GspB, Hsa, and SrpA) with differing structures and sialoglycan binding specificities nevertheless exhibited similar biomechanical properties. All three adhesins mediated shear-enhanced streptococcal binding to immobilized platelets through the platelet receptor GPIbα. Shear-enhanced adhesion was manifested in three ways. First, the number of circulating streptococci binding via SRR adhesins to immobilized platelet receptors peaked at 1 dyn/cm2. Second, bound streptococci switched from weak rolling to strong stationary adhesion as shear stress increased to 10 dyn/cm2. Third, while a few streptococci detached each time the flow was increased, the majority of streptococci bound to platelets remained firmly attached through 20 to 80 dyn/cm2 (shear levels typical of arteries and the endocardium). Thus, all three adhesins mediated shear-enhanced streptococcal binding to platelets under the flow conditions found in heart valves. The ability of the SRR adhesins to mediate shear-enhanced binding strongly suggests that they form catch bonds that are activated by tensile force and provides a mechanism for the selective targeting of bacteria to platelet receptors immobilized on the endocardial surface.

Original languageEnglish (US)
Article numbere00160-18
JournalInfection and Immunity
Volume86
Issue number6
DOIs
StatePublished - Jun 1 2018

Fingerprint

Serine
Blood Platelets
Streptococcus
Viridans Streptococci
Bacteria
Endocardium
Heart Valves
Endocarditis
Virulence
Glycoproteins
Animal Models
Arteries

Keywords

  • Adhesins
  • Biomechanics
  • Bloodstream infections
  • Infective endocarditis
  • Platelets
  • Shear stress
  • Streptococcus

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Infectious Diseases

Cite this

Yakovenko, O., Nunez, J., Bensing, B., Yu, H., Mount, J., Zeng, J., ... Thomas, W. (2018). Serine-rich repeat adhesins mediate shear-enhanced streptococcal binding to platelets. Infection and Immunity, 86(6), [e00160-18]. https://doi.org/10.1128/IAI.00160-18

Serine-rich repeat adhesins mediate shear-enhanced streptococcal binding to platelets. / Yakovenko, Olga; Nunez, Jamie; Bensing, Barbara; Yu, Hai; Mount, Jonathan; Zeng, Jie; Hawkins, Jasmine; Chen, Xi; Sullam, Paul M.; Thomas, Wendy.

In: Infection and Immunity, Vol. 86, No. 6, e00160-18, 01.06.2018.

Research output: Contribution to journalArticle

Yakovenko, O, Nunez, J, Bensing, B, Yu, H, Mount, J, Zeng, J, Hawkins, J, Chen, X, Sullam, PM & Thomas, W 2018, 'Serine-rich repeat adhesins mediate shear-enhanced streptococcal binding to platelets', Infection and Immunity, vol. 86, no. 6, e00160-18. https://doi.org/10.1128/IAI.00160-18
Yakovenko, Olga ; Nunez, Jamie ; Bensing, Barbara ; Yu, Hai ; Mount, Jonathan ; Zeng, Jie ; Hawkins, Jasmine ; Chen, Xi ; Sullam, Paul M. ; Thomas, Wendy. / Serine-rich repeat adhesins mediate shear-enhanced streptococcal binding to platelets. In: Infection and Immunity. 2018 ; Vol. 86, No. 6.
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