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Research article

Transglutaminase-2: a new endostatin partner in the extracellular matrix of endothelial cells

Clément Faye, Antonio Inforzato, Marine Bignon, Daniel J. Hartmann, Laurent Muller, Lionel Ballut, Bjorn R. Olsen, Anthony J. Day, Sylvie Ricard-Blum
Biochemical Journal May 01, 2010, 427 (3) 467-475; DOI: 10.1042/BJ20091594
Clément Faye
Institut de Biologie et Chimie des Protéines, UMR 5086 Centre National de la Recherche Scientifique, University Lyon 1, IFR 128 Biosciences Lyon-Gerland, 7 passage du Vercors 69367 Lyon Cedex 07, France
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Antonio Inforzato
Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Michael Smith Building, Oxford Road, Manchester M13 9PT, U.K.
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Marine Bignon
Inserm U833 Collège de France, 11 place Marcelin Berthelot, 75005 Paris, France
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Daniel J. Hartmann
UPSP 2007–03–135, Réparation Tissulaire, Interactions Biologiques et Biomatériaux, Institut des Sciences Pharmaceutiques et Biologiques, University Lyon 1, 8 avenue Rockefeller, 69373 Lyon Cedex 08, France
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Laurent Muller
Inserm U833 Collège de France, 11 place Marcelin Berthelot, 75005 Paris, France
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Lionel Ballut
Institut de Biologie et Chimie des Protéines, UMR 5086 Centre National de la Recherche Scientifique, University Lyon 1, IFR 128 Biosciences Lyon-Gerland, 7 passage du Vercors 69367 Lyon Cedex 07, France
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Bjorn R. Olsen
Department of Developmental Biology, Harvard School of Dental Medicine and Department of Cell Biology, Harvard Medical School, 188 Longwood Avenue, Boston, MA 02115, U.S.A.
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Anthony J. Day
Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Michael Smith Building, Oxford Road, Manchester M13 9PT, U.K.
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Sylvie Ricard-Blum
Institut de Biologie et Chimie des Protéines, UMR 5086 Centre National de la Recherche Scientifique, University Lyon 1, IFR 128 Biosciences Lyon-Gerland, 7 passage du Vercors 69367 Lyon Cedex 07, France
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  • For correspondence: s.ricard-blum@ibcp.fr
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Abstract

Endostatin, a C-terminal fragment of collagen XVIII, binds to TG-2 (transglutaminase-2) in a cation-dependent manner. Recombinant human endostatin binds to TG-2 with an affinity in the nanomolar range (Kd=6.8 nM). Enzymatic assays indicated that, in contrast with other extracellular matrix proteins, endostatin is not a glutaminyl substrate of TG-2 and is not cross-linked to itself by the enzyme. Two arginine residues of endostatin, Arg27 and Arg139, are crucial for its binding to TG-2. They are also involved in the binding to heparin [Sasaki, Larsson, Kreuger, Salmivirta, Claesson-Welsh, Lindahl, Hohenester and Timpl (1999) EMBO J. 18, 6240–6248], and to α5β1 and αvβ3 integrins [Faye, Moreau, Chautard, Jetne, Fukai, Ruggiero, Humphries, Olsen and Ricard-Blum (2009) J. Biol. Chem. 284, 22029–22040], suggesting that endostatin is not able to interact simultaneously with TG-2 and heparan sulfate, or with TG-2 and integrins. Inhibition experiments support the hypothesis that the GTP-binding site of TG-2 is a potential binding site for endostatin. Endostatin and TG-2 are co-localized in the extracellular matrix secreted by endothelial cells under hypoxia, which stimulates angiogenesis. This interaction, occurring in a cellular context, might participate in the concerted regulation of angiogenesis and tumorigenesis by the two proteins.

  • endostatin (ES)
  • extracellular matrix
  • protein–protein interaction
  • surface plasmon resonance (SPR) binding assays
  • transglutaminase-2 (TG-2)

Abbreviations: COL18A1, collagen XVIII, α1; EBNA, Epstein–Barr virus nuclear antigen; ERK, extracellular-signal-regulated kinase; FAK, focal adhesion kinase; HEK, human embryonic kidney; HIF, hypoxia-inducible factor; HUVEC, human umbilical vein endothelial cell; MAPK, mitogen-activated protein kinase; MMP, matrix metalloproteinase; MT1, membrane-type 1; NC1 domain, entire C-terminal globular domain of collagen XVIII; SPR, surface plasmon resonance; TBS, Tris-buffered-saline; TG-2, transglutaminase-2; TLR, Toll-like receptor; VEGF, vascular endothelial growth factor; VEGFR, VEGF receptor

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May 2010

Volume: 427 Issue: 3

Biochemical Journal: 427 (3)
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Transglutaminase-2: a new endostatin partner in the extracellular matrix of endothelial cells
Clément Faye, Antonio Inforzato, Marine Bignon, Daniel J. Hartmann, Laurent Muller, Lionel Ballut, Bjorn R. Olsen, Anthony J. Day, Sylvie Ricard-Blum
Biochemical Journal May 2010, 427 (3) 467-475; DOI: 10.1042/BJ20091594
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Transglutaminase-2: a new endostatin partner in the extracellular matrix of endothelial cells
Clément Faye, Antonio Inforzato, Marine Bignon, Daniel J. Hartmann, Laurent Muller, Lionel Ballut, Bjorn R. Olsen, Anthony J. Day, Sylvie Ricard-Blum
Biochemical Journal May 2010, 427 (3) 467-475; DOI: 10.1042/BJ20091594

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Keywords

endostatin (ES)
extracellular matrix
protein–protein interaction
surface plasmon resonance (SPR) binding assays
transglutaminase-2 (TG-2)

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