Repeating structures of the major staphylococcal autolysin are essential for the interaction with human thrombospondin 1 and vitronectin

J Biol Chem. 2014 Feb 14;289(7):4070-82. doi: 10.1074/jbc.M113.521229. Epub 2013 Dec 26.

Abstract

Human thrombospondin 1 (hTSP-1) is a matricellular glycoprotein facilitating bacterial adherence to and invasion into eukaryotic cells. However, the bacterial adhesin(s) remain elusive. In this study, we show a dose-dependent binding of soluble hTSP-1 to Gram-positive but not Gram-negative bacteria. Diminished binding of soluble hTSP-1 to proteolytically pretreated staphylococci suggested a proteinaceous nature of potential bacterial adhesin(s) for hTSP-1. A combination of separation of staphylococcal surface proteins by two-dimensional gel electrophoresis with a ligand overlay assay with hTSP-1 and identification of the target protein by mass spectrometry revealed the major staphylococcal autolysin Atl as a bacterial binding protein for hTSP-1. Binding experiments with heterologously expressed repeats of the AtlE amidase from Staphylococcus epidermidis suggest that the repeating sequences (R1ab-R2ab) of the N-acetyl-muramoyl-L-alanine amidase of Atl are essential for binding of hTSP-1. Atl has also been identified previously as a staphylococcal vitronectin (Vn)-binding protein. Similar to the interaction with hTSP-1, the R1ab-R2ab repeats of Atl are shown here to be crucial for the interaction of Atl with the complement inhibition and matrix protein Vn. Competition assays with hTSP-1 and Vn revealed the R1ab-R2ab repeats of AtlE as the common binding domain for both host proteins. Furthermore, Vn competes with hTSP-1 for binding to Atl repeats and vice versa. In conclusion, this study identifies the Atl repeats as bacterial adhesive structures interacting with the human glycoproteins hTSP-1 and Vn. Finally, this study provides insight into the molecular interplay between hTSP-1 and Vn, respectively, and a bacterial autolysin.

Keywords: Adhesion; Autolysin; Extracellular Matrix Proteins; Pathogenesis; Repeats; Staphylococcus; Thrombospondin; Vitronectin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Humans
  • N-Acetylmuramoyl-L-alanine Amidase / chemistry*
  • N-Acetylmuramoyl-L-alanine Amidase / genetics
  • N-Acetylmuramoyl-L-alanine Amidase / metabolism
  • Protein Binding
  • Protein Structure, Tertiary
  • Staphylococcus aureus / enzymology
  • Staphylococcus aureus / genetics
  • Staphylococcus epidermidis / enzymology*
  • Thrombospondin 1 / chemistry*
  • Thrombospondin 1 / genetics
  • Thrombospondin 1 / metabolism
  • Vitronectin / chemistry*
  • Vitronectin / genetics
  • Vitronectin / metabolism

Substances

  • Bacterial Proteins
  • Thrombospondin 1
  • Vitronectin
  • N-Acetylmuramoyl-L-alanine Amidase