Identification of the thiol isomerase-binding peptide, Mastoparan, as a novel inhibitor of shear-induced transforming growth factor β1 (TGF-β1) Activation

Journal of Biological Chemistry

Volumn 288, Issue 15, 2013, Pages 10628-10639

  Brophy, Teresa M ^a   Coller, Barry S ^a   Ahamed, Jasimuddin ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY COLUMN; CHAPERONE ACTIVITY; HOMODIMERIC PROTEINS; INHIBITORY EFFECT; PROTEIN DISULFIDE ISOMERASES; THIOL-DISULFIDE EXCHANGES; TRANSFORMING GROWTH FACTORS; VON WILLEBRAND FACTOR;

ENZYMES; GLYCOPROTEINS; PLATELETS;

PEPTIDES;

BINDING PROTEIN; CELL PROTEIN; CHAPERONE; CLUSTERIN; DISULFIDE ISOMERASE; ISOMERASE; LARGE LATENT COMPLEX PROTEIN; MASTOPARAN; MULTIMERIN 1; PROTEIN; PROTEIN ANTIBODY; PROTEIN DISULFIDE ISOMERASE; PROTEIN ERP5; PROTEIN ERP57; PROTEIN ERP72; RECOMBINANT LARGE LATENT COMPLEX PROTEIN; RECOMBINANT PROTEIN; TGF BETA BINDING PROTEIN 1; THIOL ISOMERASE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; OXIDATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SHEAR STRESS;

BLOOD PLATELETS; BLOOD PROTEINS; CELL LINE; CLUSTERIN; DISULFIDES; FEMALE; HUMANS; LATENT TGF-BETA BINDING PROTEINS; MALE; PEPTIDES; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASES; TRANSFORMING GROWTH FACTOR BETA1; VON WILLEBRAND FACTOR; WASP VENOMS;

EID: 84876266481     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.439034     Document Type: Article

References (51)

1. Blobe, G. C., Schiemann, W. P., and Lodish, H. F. (2000) Role of transforming growth factor β in human disease. N. Engl. J. Med. 342, 1350-1358
2. Assoian, R. K., Komoriya, A., Meyers, C. A., Miller, D. M., and Sporn, M. B. (1983) Transforming growth factor-β in human platelets. Identification of a major storage site, purification, and characterization. J. Biol. Chem. 258, 7155-7160
3. Wakefield, L. M., Smith, D. M., Flanders, K. C., and Sporn, M. B. (1988) Latent transforming growth factor-β from human platelets. A high molecular weight complex containing precursor sequences. J. Biol. Chem. 263, 7646-7654
4. Labelle, M., Begum, S., and Hynes, R. O. (2011) Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell 20, 576-590
5. Meyer, A., Wang, W., Qu, J., Croft, L., Degen, J. L., Coller, B. S., and Ahamed, J. (2012) Platelet TGF-β1 contributions to plasma TGF-β1, cardiac fibrosis, and systolic dysfunction in a mouse model of pressure overload. Blood 119, 1064-1074
6. Gleizes, P. E., Beavis, R. C., Mazzieri, R., Shen, B., and Rifkin, D. B. (1996) Identification and characterization of an eight-cysteine repeat of the latent transforming growth factor-β binding protein-1 that mediates bonding to the latent transforming growth factor-β1. J. Biol. Chem. 271, 29891-29896
7. Munger, J. S., Huang, X., Kawakatsu, H., Griffiths, M. J., Dalton, S. L., Wu, J., Pittet, J. F., Kaminski, N., Garat, C., Matthay, M. A., Rifkin, D. B., and Sheppard, D. (1999) The integrin αvβ6 binds and activates latent TGFβ1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96, 319-328
8. Shi, M., Zhu, J., Wang, R., Chen, X., Mi, L., Walz, T., and Springer, T. A. (2011) Latent TGF-β structure and activation. Nature 474, 343-349
9. Murphy-Ullrich, J. E., and Poczatek, M. (2000) Activation of latent TGF-by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev. 11, 59-69
10. Jenkins, G. (2008) The role of proteases in transforming growth factor-β activation. Int. J. Biochem. Cell Biol. 40, 1068-1078
11. Jobling, M. F., Mott, J. D., Finnegan, M. T., Jurukovski, V., Erickson, A. C., Walian, P. J., Taylor, S. E., Ledbetter, S., Lawrence, C. M., Rifkin, D. B., and Barcellos-Hoff, M. H. (2006) Isoform-specific activation of latent transforming growth factorβ (LTGF-β) by reactive oxygen species. Radiat. Res. 166, 839-848
12. Ahamed, J., Burg, N., Yoshinaga, K., Janczak, C. A., Rifkin, D. B., and Coller, B. S. (2008) In vitro and in vivo evidence for shear-induced activation of latent transforming growth factor-β1. Blood 112, 3650-3660
13. Ahamed, J., Janczak, C. A., Wittkowski, K. M., and Coller, B. S. (2009) In vitro and in vivo evidence that thrombospondin-1 (TSP-1) contributes to stirring-and shear-dependent activation of platelet-derived TGF-β1. PLoS One 4, e6608
14. Raturi, A., and Mutus, B. (2007) Characterization of redox state and reductase activity of protein disulfide isomerase under different redox environments using a sensitive fluorescent assay. Free Radic. Biol. Med. 43, 62-70
15. Kikuchi, M., Doi, E., Tsujimoto, I., Horibe, T., and Tsujimoto, Y. (2002) Functional analysis of human P5, a protein disulfide isomerase homologue. J. Biochem. 132, 451-455
16. Choi, H., Aboulfatova, K., Pownall, H. J., Cook, R., and Dong, J. F. (2007) Shear-induced disulfide bond formation regulates adhesion activity of von Willebrand factor. J. Biol. Chem. 282, 35604-35611
17. Huang, E. M., Detwiler, T. C., Milev, Y., and Essex, D. W. (1997) Thioldisulfide isomerization in thrombospondin: effects of conformation and protein disulfide isomerase. Blood 89, 3205-3212
18. Klappa, P., Ruddock, L. W., Darby, N. J., and Freedman, R. B. (1998) The b' domain provides the principal peptide-binding site of protein disulfide isomerase but all domains contribute to binding of misfolded proteins. EMBO J. 17, 927-935
19. Denisov, A. Y., Määttänen, P., Dabrowski, C., Kozlov, G., Thomas, D. Y., and Gehring, K. (2009) Solution structure of the bb' domains of human protein disulfide isomerase. FEBS J. 276, 1440-1449
20. Raturi, A., and Ruf, W. (2010) Effect of protein disulfide isomerase chaperone activity inhibition on tissue factor activity. J. Thromb. Haemost. 8, 1863-1865
21. Jones, S., and Howl, J. (2006) Biological applications of the receptor mimetic peptide mastoparan. Curr. Protein Pept. Sci. 7, 501-508
22. Argiolas, A., and Pisano, J. J. (1983) Facilitation of phospholipase A2 activity by mastoparans, a new class of mast cell degranulating peptides from wasp venom. J. Biol. Chem. 258, 13697-13702
23. Barnette, M. S., Daly, R., and Weiss, B. (1983) Inhibition of calmodulin activity by insect venom peptides. Biochem. Pharmacol. 32, 2929-2933
24. Higashijima, T., Uzu, S., Nakajima, T., and Ross, E. M. (1988) Mastoparan, a peptide toxin from wasp venom, mimics receptors by activating GTPbinding regulatory proteins (G proteins). J. Biol. Chem. 263, 6491-6494
25. Pfeiffer, D. R., Gudz, T. I., Novgorodov, S. A., and Erdahl, W. L. (1995) The peptide mastoparan is a potent facilitator of the mitochondrial permeability transition. J. Biol. Chem. 270, 4923-4932
26. Hirai, Y., Yasuhara, T., Yoshida, H., Nakajima, T., Fujino, M., and Kitada, C. (1979) A new mast cell degranulating peptide "mastoparan" in the venom of Vespula lewisii. Chem. Pharm. Bull. 27, 1942-1944
27. Ozaki, Y., Matsumoto, Y., Yatomi, Y., Higashihara, M., Kariya, T., and Kume, S. (1990) Mastoparan, a wasp venom, activates platelets via pertussis toxin-sensitive GTP-binding proteins. Biochem. Biophys. Res. Commun. 170, 779-785
28. Wheeler-Jones, C. P., Saermark, T., Kakkar, V. V., and Authi, K. S. (1992) Mastoparan promotes exocytosis and increases intracellular cyclic AMP in human platelets. Evidence for the existence of a Ge-like mechanism of secretion. Biochem. J. 281, 465-472
29. Hatahet, F., and Ruddock, L. W. (2009) Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid. Redox Signal. 11, 2807-2850
30. Serve, O., Kamiya, Y., Maeno, A., Nakano, M., Murakami, C., Sasakawa, H., Yamaguchi, Y., Harada, T., Kurimoto, E., Yagi-Utsumi, M., Iguchi, T., Inaba, K., Kikuchi, J., Asami, O., Kajino, T., Oka, T., Nakasako, M., and Kato, K. (2010) Redox-dependent domain rearrangement of protein disulfide isomerase coupled with exposure of its substrate-binding hydrophobic surface. J. Mol. Biol. 396, 361-374
31. Wang, C., Yu, J., Huo, L., Wang, L., Feng, W., and Wang, C. C. (2012) Human protein-disulfide isomerase is a redox-regulated chaperone activated by oxidation of domain a'. J. Biol. Chem. 287, 1139-1149
32. Byrne, L. J., Sidhu, A., Wallis, A. K., Ruddock, L. W., Freedman, R. B., Howard, M. J., and Williamson, R. A. (2009) Mapping of the ligand-binding site on the b' domain of human PDI: interaction with peptide ligands and the x-linker region. Biochem. J. 423, 209-217
33. Chen, K., Lin, Y., and Detwiler, T. C. (1992) Protein disulfide isomerase activity is released by activated platelets. Blood 79, 2226-2228
34. Jordan, P. A., Stevens, J. M., Hubbard, G. P., Barrett, N. E., Sage, T., Authi, K. S., and Gibbins, J. M. (2005) A role for the thiol isomerase protein ERP5 in platelet function. Blood 105, 1500-1507
35. Holbrook, L. M., Watkins, N. A., Simmonds, A. D., Jones, C. I., Ouwehand, W. H., and Gibbins, J. M. (2010) Platelets release novel thiol isomerase enzymes which are recruited to the cell surface following activation. Br. J. Haematol. 148, 627-637
36. Jordan, P. A., and Gibbins, J. M. (2006) Extracellular disulfide exchange and the regulation of cellular function. Antioxid. Redox Signal. 8, 312-324
37. Burgess, J. K., Hotchkiss, K. A., Suter, C., Dudman, N. P., Szöllösi, J., Chesterman, C. N., Chong, B. H., and Hogg, P. J. (2000) Physical proximity and functional association of glycoprotein 1b and protein-disulfide isomerase on the platelet plasma membrane. J. Biol. Chem. 275, 9758-9766
38. Lahav, J., Gofer-Dadosh, N., Luboshitz, J., Hess, O., and Shaklai, M. (2000) Protein disulfide isomerase mediates integrin-dependent adhesion. FEBS letters 475, 89-92
39. Essex, D. W., and Li, M. (1999) Protein disulphide isomerase mediates platelet aggregation and secretion. Br. J. Haematol. 104, 448-454
40. Reinhardt, C., von Brühl, M. L., Manukyan, D., Grahl, L., Lorenz, M., Altmann, B., Dlugai, S., Hess, S., Konrad, I., Orschiedt, L., Mackman, N., Ruddock, L., Massberg, S., and Engelmann, B. (2008) Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J. Clin. Invest. 118, 1110-1122
41. Hawkins, H. C., and Freedman, R. B. (1991) The reactivities and ionization properties of the active-site dithiol groups of mammalian protein disulphide-isomerase. Biochem. J. 275, 335-339
42. Wu, Y., Ahmad, S. S., Zhou, J., Wang, L., Cully, M. P., and Essex, D. W. (2012) The disulfide isomerase ERp57 mediates platelet aggregation, hemostasis, and thrombosis. Blood 119, 1737-1746
43. Alanen, H. I., Salo, K. E., Pirneskoski, A., and Ruddock, L. W. (2006) pH dependence of the peptide thiol-disulfide oxidase activity of six members of the human protein disulfide isomerase family. Antioxid. Redox Signal. 8, 283-291
44. Tschopp, J., Jenne, D. E., Hertig, S., Preissner, K. T., Morgenstern, H., Sapino, A. P., and French, L. (1993) Human megakaryocytes express clusterin and package it without apolipoprotein A-1 into-granules. Blood 82, 118-125
45. Jessop, C. E., Chakravarthi, S., Garbi, N., Hämmerling, G. J., Lovell, S., and Bulleid, N. J. (2007) ERp57 is essential for efficient folding of glycoproteins sharing common structural domains. EMBO J. 26, 28-40
46. Lenferink, A. E., Cantin, C., Nantel, A., Wang, E., Durocher, Y., Banville, M., Paul-Roc, B., Marcil, A., Wilson, M. R., and O'Connor-McCourt, M. D. (2010) Transcriptome profiling of a TGF-β-induced epithelial- tomesenchymal transition reveals extracellular clusterin as a target for therapeutic antibodies. Oncogene 29, 831-844
47. Jung, G. S., Kim, M. K., Jung, Y. A., Kim, H. S., Park, I. S., Min, B. H., Lee, K. U., Kim, J. G., Park, K. G., and Lee, I. K. (2012) Clusterin attenuates the development of renal fibrosis. J. Am. Soc. Nephrol. 23, 73-85
48. Hayward, C. P., Bainton, D. F., Smith, J. W., Horsewood, P., Stead, R. H., Podor, T. J., Warkentin, T. E., and Kelton, J. G. (1993) Multimerin is found in the -granules of resting platelets and is synthesized by a megakaryocytic cell line. J. Clin. Invest. 91, 2630-2639
49. Jeimy, S. B., Tasneem, S., Cramer, E. M., and Hayward, C. P. (2008) Multimerin 1. Platelets 19, 83-95
50. Zacchigna, L., Vecchione, C., Notte, A., Cordenonsi, M., Dupont, S., Maretto, S., Cifelli, G., Ferrari, A., Maffei, A., Fabbro, C., Braghetta, P., Marino, G., Selvetella, G., Aretini, A., Colonnese, C., Bettarini, U., Russo, G., Soligo, S., Adorno, M., Bonaldo, P., Volpin, D., Piccolo, S., Lembo, G., and Bressan, G. M. (2006) Emilin1 links TGF-maturation to blood pressure homeostasis. Cell 124, 929-942
51. Schiavinato, A., Becker, A. K., Zanetti, M., Corallo, D., Milanetto, M., Bizzotto, D., Bressan, G., Guljelmovic, M., Paulsson, M., Wagener, R., Braghetta, P., and Bonaldo, P. (2012) EMILIN-3, peculiar member of elastin microfibril interface-located protein (EMILIN) family, has distinct expression pattern, forms oligomeric assemblies, and serves as transforming growth factor β (TGF-β) antagonist. J. Biol. Chem. 287, 11498-11515