A new role for host annexin A2 in establishing bacterial adhesion to vascular endothelial cells: lines of evidence from atomic force microscopy and an in vivo study

Lab Invest. 2019 Nov;99(11):1650-1660. doi: 10.1038/s41374-019-0284-z. Epub 2019 Jun 28.

Abstract

Understanding bacterial adhesion is challenging and critical to our understanding of the initial stages of the pathogenesis of endovascular bacterial infections. The vascular endothelial cell (EC) is the main target of Rickettsia, an obligately intracellular bacterium that causes serious systemic disease in humans and animals. But the mechanism(s) underlying bacterial adherence to ECs under shear stress from flowing blood prior to activation are unknown for any bacteria. Although host surface annexin a2 (ANXA2) has been identified to participate in efficient bacterial invasion of epithelial cells, direct evidence is lacking in the field of bacterial infections of ECs. In the present study, we employ a novel, anatomically based, in vivo quantitative bacterial-adhesion-to-vascular-EC system, combined with atomic force microscopy (AFM), to examine the role of endothelial luminal surface ANXA2 during rickettsial adherence to ECs. We also examined whether ANXA2 antibody affected binding of Staphylococcus aureus to ECs. We found that deletion of ANXA2 impeded rickettsial attachment to the ECs in vitro and blocked rickettsial adherence to the blood vessel luminal surface in vivo. The AFM studies established that EC surface ANXA2 acts as an adherence receptor for rickettsiae, and that rickettsial adhesin OmpB is the associated bacterial ligand. Furthermore, pretreatment of ECs with anti-ANXA2 antibody reduced EC surface-associated S. aureus. We conclude that the endothelial surface ANXA2 plays an important role in initiating pathogen-host interactions, ultimately leading to bacterial anchoring on the vascular luminal surface.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Annexin A2 / deficiency
  • Annexin A2 / genetics
  • Annexin A2 / physiology*
  • Bacterial Adhesion / physiology*
  • Bacterial Outer Membrane Proteins / genetics
  • Bacterial Outer Membrane Proteins / physiology
  • Biomechanical Phenomena
  • Disease Models, Animal
  • Endothelial Cells / microbiology*
  • Endothelial Cells / physiology*
  • Host Microbial Interactions / physiology
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • In Vitro Techniques
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Atomic Force
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Rickettsia / pathogenicity
  • Rickettsia / physiology
  • Rickettsia Infections / microbiology
  • Staphylococcus aureus / pathogenicity
  • Staphylococcus aureus / physiology

Substances

  • ANXA2 protein, human
  • Annexin A2
  • Anxa2 protein, mouse
  • Bacterial Outer Membrane Proteins
  • Recombinant Proteins

Supplementary concepts

  • Rickettsia australis