A single malaria merozoite serine protease mediates shedding of multiple surface proteins by juxtamembrane cleavage

J Biol Chem. 2003 Jun 27;278(26):23890-8. doi: 10.1074/jbc.M302160200. Epub 2003 Apr 9.

Abstract

Erythrocyte invasion by the malaria merozoite is accompanied by the regulated discharge of apically located secretory organelles called micronemes. Plasmodium falciparum apical membrane antigen-1 (PfAMA-1), which plays an indispensable role in invasion, translocates from micronemes onto the parasite surface and is proteolytically shed in a soluble form during invasion. We have previously proposed, on the basis of incomplete mass spectrometric mapping data, that PfAMA-1 shedding results from cleavage at two alternative positions. We now show conclusively that the PfAMA-1 ectodomain is shed from the merozoite solely as a result of cleavage at a single site, just 29 residues away from the predicted transmembrane-spanning sequence. Remarkably, this cleavage is mediated by the same membrane-bound parasite serine protease as that responsible for shedding of the merozoite surface protein-1 (MSP-1) complex, an abundant, glycosylphosphatidylinositol-anchored multiprotein complex. Processing of MSP-1 is essential for invasion. Our results indicate the presence on the merozoite surface of a multifunctional serine sheddase with a broad substrate specificity. We further demonstrate that translocation and shedding of PfAMA-1 is an actin-independent process.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Antigens, Protozoan*
  • Membrane Proteins / metabolism
  • Merozoite Surface Protein 1 / metabolism
  • Molecular Sequence Data
  • Plasmodium falciparum / enzymology*
  • Plasmodium falciparum / physiology
  • Plasmodium falciparum / ultrastructure
  • Protein Processing, Post-Translational
  • Protein Transport
  • Protozoan Proteins / metabolism*
  • Serine Endopeptidases / metabolism
  • Serine Endopeptidases / physiology*
  • Spectrometry, Mass, Electrospray Ionization

Substances

  • Antigens, Protozoan
  • Membrane Proteins
  • Merozoite Surface Protein 1
  • Protozoan Proteins
  • apical membrane antigen I, Plasmodium
  • Serine Endopeptidases