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Research article

Metastasis-associated S100A4 is a specific amine donor and an activity-independent binding partner of transglutaminase-2

Beáta Biri, Bence Kiss, Róbert Király, Gitta Schlosser, Orsolya Láng, László Kőhidai, László Fésüs, László Nyitray
Biochemical Journal Dec 09, 2015, 473 (1) 31-42; DOI: 10.1042/BJ20150843
Beáta Biri
Department of Biochemistry, Eötvös Loránd University, 1117 Budapest, Hungary
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Bence Kiss
Department of Biochemistry, Eötvös Loránd University, 1117 Budapest, Hungary
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Róbert Király
Department of Biochemistry and Molecular Biology, University of Debrecen, 4032 Debrecen, Hungary
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Gitta Schlosser
MTA-ELTE Research Group of Peptide Chemistry, Hungarian Academy of Sciences, Eötvös Loránd University, 1117 Budapest, Hungary
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Orsolya Láng
Department of Genetics, Cell Biology and Immunobiology, Semmelweis University, 1089 Budapest, Hungary
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László Kőhidai
Department of Genetics, Cell Biology and Immunobiology, Semmelweis University, 1089 Budapest, Hungary
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László Fésüs
Department of Biochemistry and Molecular Biology, University of Debrecen, 4032 Debrecen, HungaryMTA-DE Stem Cell, Apoptosis and Genomics Research Group of Hungarian Academy of Sciences, University of Debrecen, 4032 Debrecen, Hungary
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László Nyitray
Department of Biochemistry, Eötvös Loránd University, 1117 Budapest, Hungary
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  • For correspondence: nyitray@elte.hu
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Abstract

Transglutaminase-2 (TG2) is best known as a Ca2+-dependent cross-linking enzyme; however, some of its extracellular matrix-related functions are independent of its catalytic activity and include matrix remodelling, adhesion and migration. S100A4 belongs to the Ca2+-binding EF-hand S100 protein family and acts both intra- and extra-cellularly through binding to various partners. It regulates cell migration and its overexpression is strongly associated with metastasis and poor survival in various cancers. It has recently been suggested that TG2 mediates S100A4-dependent tumour cell migration. In the present study we provide evidence that S100A4 is an interacting partner and also a specific amine donor of TG2. TG2 incorporates a glutamine donor peptide to Lys100 in the C-terminal random coil region of S100A4. Importantly, the enzyme activity is not necessary for the interaction: S100A4 also binds to TG2 in the presence of a specific inhibitor that keeps the enzyme in an open conformation, or to an enzymatically inactive mutant. We also found that S100A4 considerably enhances TG2-mediated adhesion of A431 epithelial carcinoma cells to the extracellular matrix. This role is independent of enzyme activity and requires the open conformation of TG2. We propose that S100A4 stabilizes the open conformation of TG2, which binds to its cell-surface receptor in this state and increases cell adhesion.

  • cell adhesion
  • metastasis
  • protein cross-linking
  • S100 proteins
  • S100A4
  • transglutaminase-2
  • Abbreviations

    DC,
    dansyl-cadaverine;
    DMC,
    N,N-dimethyl-casein;
    ECM,
    extracellular matrix;
    FP,
    fluorescence polarization;
    GTPγS,
    guanosine 5′-[γ-thio]triphosphate;
    HRP,
    horseradish peroxidase;
    ID,
    intrinsically disordered;
    NMIIA,
    non-muscle myosin IIA;
    PDGFR,
    platelet-derived growth factor receptor;
    TBST,
    TBS/Tween 20;
    TCEP,
    tris(2-carboxyethyl)phosphine;
    TEV,
    tobacco etch virus;
    TG2,
    transglutaminase-2
    • © 2016 Authors; published by Portland Press Limited
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    January 2016

    Volume: 473 Issue: 1

    Biochemical Journal: 473 (1)
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    Metastasis-associated S100A4 is a specific amine donor and an activity-independent binding partner of transglutaminase-2
    Beáta Biri, Bence Kiss, Róbert Király, Gitta Schlosser, Orsolya Láng, László Kőhidai, László Fésüs, László Nyitray
    Biochemical Journal Jan 2016, 473 (1) 31-42; DOI: 10.1042/BJ20150843
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    Metastasis-associated S100A4 is a specific amine donor and an activity-independent binding partner of transglutaminase-2
    Beáta Biri, Bence Kiss, Róbert Király, Gitta Schlosser, Orsolya Láng, László Kőhidai, László Fésüs, László Nyitray
    Biochemical Journal Jan 2016, 473 (1) 31-42; DOI: 10.1042/BJ20150843

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    Keywords

    cell adhesion
    metastasis
    protein cross-linking
    S100 proteins
    S100A4
    transglutaminase-2

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