The mucin-selective protease StcE enables molecular and functional analysis of human cancer-associated mucins

Proc Natl Acad Sci U S A. 2019 Apr 9;116(15):7278-7287. doi: 10.1073/pnas.1813020116. Epub 2019 Mar 25.

Abstract

Mucin domains are densely O-glycosylated modular protein domains that are found in a wide variety of cell surface and secreted proteins. Mucin-domain glycoproteins are known to be key players in a host of human diseases, especially cancer, wherein mucin expression and glycosylation patterns are altered. Mucin biology has been difficult to study at the molecular level, in part, because methods to manipulate and structurally characterize mucin domains are lacking. Here, we demonstrate that secreted protease of C1 esterase inhibitor (StcE), a bacterial protease from Escherichia coli, cleaves mucin domains by recognizing a discrete peptide- and glycan-based motif. We exploited StcE's unique properties to improve sequence coverage, glycosite mapping, and glycoform analysis of recombinant human mucins by mass spectrometry. We also found that StcE digests cancer-associated mucins from cultured cells and from ascites fluid derived from patients with ovarian cancer. Finally, using StcE, we discovered that sialic acid-binding Ig-type lectin-7 (Siglec-7), a glycoimmune checkpoint receptor, selectively binds sialomucins as biological ligands, whereas the related receptor Siglec-9 does not. Mucin-selective proteolysis, as exemplified by StcE, is therefore a powerful tool for the study of mucin domain structure and function.

Keywords: O-glycosylation; Siglec; glycoproteomics; mucin; protease.

Publication types

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

MeSH terms

  • Amino Acid Motifs
  • Antigens, CD / chemistry*
  • Antigens, Differentiation, Myelomonocytic / chemistry*
  • Escherichia coli / enzymology*
  • Escherichia coli Proteins / chemistry*
  • Humans
  • Lectins / chemistry*
  • Mass Spectrometry
  • Metalloendopeptidases / chemistry*
  • Mucins / chemistry*
  • Neoplasm Proteins / chemistry*
  • Sialic Acid Binding Immunoglobulin-like Lectins / chemistry*
  • Substrate Specificity

Substances

  • Antigens, CD
  • Antigens, Differentiation, Myelomonocytic
  • Escherichia coli Proteins
  • Lectins
  • Mucins
  • Neoplasm Proteins
  • SIGLEC7 protein, human
  • SIGLEC9 protein, human
  • Sialic Acid Binding Immunoglobulin-like Lectins
  • Metalloendopeptidases
  • StcE protein, E coli