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DOI: 10.1160/TH08-09-0605
Coagulation factor XIII serves as protein disulfide isomerase
Financial support: This work was supported in part by the Hungarian National Research Fund Grant (OTKA-NKTH NI>69238).
Publication History
Received:
18 September 2008
Accepted after major revision:
12 February 2009
Publication Date:
24 November 2017 (online)
Summary
Tissue transglutaminase was reported to act as protein disulfide isomerase (PDI). We studied whether plasma transglutaminase – coagulation factor XIII (FXIII) – has PDI activity as well. PDI activity was measured by determining the ability to renature reduced-denatured RNase (rdRNase). We found that FXIII can re-nature rdRNase, with efficiency comparable to commercial PDI. This PDI activity was inhibited by bacitracin. Like tissue transglu-taminase, FXIII-mediated PDI activity is independent of its transglutaminase activity and is located on the A subunit. Surface-associated PDI has been previously shown to catalyse two distinct functions: transnitrosation with subsequent release of intracellular nitric oxide and disulfide bond rearrangement during platelet integrin ligation. Our results imply that FXIII-PDI activity may have a role in platelet function.
* These authors contributed equally.
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References
- 1 Muszbek L, Yee VC, Hevessy Z. Blood coagulation factor XIII: structure and function. Thromb Res 1999; 94: 271-305.
- 2 Inbal A, Lubetsky A, Krapp T. et al. Impaired wound healing in factor XIII deficient mice. Thromb Haemost 2005; 94: 432-437.
- 3 Dardik R, Solomon A, Loscalzo J. et al. Novel proangiogenic effect of factor XIII associated with suppression of thrombospondin 1 expression. Arterioscler Thromb Vasc Biol 2003; 23: 1472-1477.
- 4 Dardik R, Krapp T, Rosental E. et al. Effect of factor XIII on monocyte and fibroblast function. Cell Physiol Biochem 2007; 19: 113-120.
- 5 Greenberg CS, Birckbichler PJ, Rice RH. Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues. FASEB J 1991; 05: 3071-3077.
- 6 Ikura K, Nasu T, Yokota H. et al. Amino acid sequence of guinea pig liver transglutaminase from its c-DNA sequence. Biochem 1988; 27: 2898-2905.
- 7 Hasegawa G, Suwa M, Ichikawa Y. et al. A novel function of tissue transglutaminase: protein disulphide isomerase. Biochem J 2003; 373: 793-803.
- 8 Ferrari D, Soling HD. The protein disulphide isomerase family : unravelling a string of folds. Biochem J 1999; 339: 1-10.
- 9 Turano C, Coppari S, Altieri F. et al. Proteins of the PDI family: Unpredicted Non-ER location and function. J Cell Physiol 2002; 193: 154-163.
- 10 Lahav J, Gofer-Dadosh N, Luboshitz J. et al. Protein disulfide isomerase mediates integrin-dependent adhesion. FEBS Lett 2000; 475: 89-92.
- 11 Lahav J, Jurk K, Hess O. et al. Sustained integrin ligation involves extracellular free sulfhydryls and enzymatically catalyzed disulfide exchange. Blood 2002; 100: 2472-2478.
- 12 Lahav J, Wijnen EM, Hess O. et al. Enzymatically catalyzed disulfide exchange is required for platelet adhesion to collagen via integrin alpha2beta1. Blood 2003; 102: 2085-2092.
- 13 Bennett TA, Edwards BS, Sklar LA. et al. Sulfhydryl regulation of L-selectin shedding: Phenylarsine oxide promotes activation-independent L-selectin shedding from leukocytes. J Immunol 2000; 164: 4120-4129.
- 14 Gallina A, Hanley TM, Mandel R. et al. Inhibitors of protein disulfide isomerase prevent cleavage of disulfide bonds in receptor-bound Glycoprotein 120 and prevent HIV-1 entry. J Biol Chem 2002; 277: 50579-50588.
- 15 Zai A, Rudd MA, Scribner AW. et al. Cell-surface protein disulfide isomerase catalyzes transnitrosation and regulates intracellular transfer of nitric oxide. J Clin Invest 1999; 103: 393-399.
- 16 Ruoppolo M, Freedman RB. Protein-S-S-glut-athione mixed disulfides as models of unfolded proteins. Biochemistry 1994; 33: 7654-7662.
- 17 Riddles PW, Blakeley RL, Zerner B. Reassessment of Ellman’s reagent. Methods Enzymol 1983; 91: 49-60.
- 18 Polgár J, Hidasi V, Muszbek L. Non-proteolytic activation of cellular protransglutaminase (placental macrophage factor XIII). Biochem J 1990; 267: 557-560.
- 19 Lorand L, Credo RB, Janus TG. Factor XIII (fibrin stabilizing factor). Methods Enzymol 1981; 80: 333-341.
- 20 Kárpáti L, Penke B, Katona E. et al. A modified, optimized kinetic photometric assay for the determination of blood coagulation factor XIII activity in plasma. Clin Chem 2000; 46: 1946-1955.
- 21 Smyth DG, Stein WH, Moore S. The sequence of amino acid residues in bovine pancreatic ribonuclease: revisions and confirmations. J Biol Chem 1963; 238: 227-234.
- 22 Vilahur G, Segales E, Casani L. et al. A novel anti-ischemic nitric oxide donor inhibits thrombosis without modifying heamodynamic parameters. Thromb Heamost 2004; 91: 1035-1043.
- 23 Essex DW, Chen K, Swiatkowska M. Localization of the protein disulfide isomerase to the external surface of the platelet plasma membrane. Blood 1995; 86: 2168-2173.
- 24 Bernassola F, Rossi A, Melino G. Regulation of transglutaminases by nitric oxide. Ann NY Acad Sci 1999; 887: 83-91.