A unique serpin P1′ glutamate and a conserved β-sheet C arginine are key residues for activity, protease recognition and stability of serpinA12 (vaspin)

Biochemical Journal

Volumn 470, Issue 3, 2015, Pages 357-367

  Ulbricht, David ^a   Pippel, Jan ^a   Schultz, Stephan ^a   Meier, René ^a   Sträter, Norbert ^a   Heiker, John T ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Adipokine; Crystal structure; Exosite; Kallikrein 7; Reactive centre loop; Serpin; Vaspin

Indexed keywords

ADIPOCYTOKINE; ANTITHROMBIN III; ARGININE; GLUTAMIC ACID; HEPARIN; PROTEINASE; RECOMBINANT PROTEIN; SERINE PROTEINASE INHIBITOR; STRATUM CORNEUM CHYMOTRYPTIC ENZYME; THERMOLYSIN; VASPIN; KALLIKREIN; KLK7 PROTEIN, HUMAN; SERPINA12 PROTEIN, HUMAN;

ARTICLE; BETA SHEET; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; HUMAN; MUTAGENESIS; OBESITY; PEPTIDE SYNTHESIS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEINASE INHIBITION; SUBSTRATE CONCENTRATION; THERMOSTABILITY; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; KINETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY; X RAY CRYSTALLOGRAPHY;

ARGININE; BINDING SITES; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; GLUTAMIC ACID; HEPARIN; HUMANS; KALLIKREINS; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SERPINS; STATIC ELECTRICITY;

EID: 84941364197     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20150643     Document Type: Article

References (50)

1. Hida, K., Wada, J., Eguchi, J., Zhang, H., Baba, M., Seida, A., Hashimoto, L., Okada, T., Yasuhara, A., Nakatsuka, A. et al. (2005) Visceral adipose tissue-derived serine protease inhibitor: a unique insulin-sensitizing adipocytokine in obesity. Proc. Natl. Acad. Sci. U.S.A. 102, 10610-10615 CrossRef PubMed
2. Klöting, N., Berndt, J., Kralisch, S., Kovacs, P., Fasshauer, M., Schon, M.R., Stumvoll, M. and Blüher, M. (2006) Vaspin gene expression in human adipose tissue: association with obesity and type 2 diabetes. Biochem. Biophys. Res. Commun. 339, 430-436 CrossRef PubMed
3. Youn, B.S., Klöting, N., Kratzsch, J., Lee, N., Park, J.W., Song, E.S., Ruschke, K., Oberbach, A., Fasshauer, M., Stumvoll, M. and Blüher, M. (2008) Serum vaspin concentrations in human obesity and type 2 diabetes. Diabetes 57, 372-377 CrossRef PubMed
4. Blüher, M. (2012) Vaspin in obesity and diabetes: pathophysiological and clinical significance. Endocrine 41, 176-182 CrossRef PubMed
5. Heiker, J.T. (2014) Vaspin (serpinA12) in obesity, insulin resistance, and inflammation. J. Pept. Sci. 20, 299-306 CrossRef PubMed
6. Nakatsuka, A., Wada, J., Iseda, I., Teshigawara, S., Higashio, K., Murakami, K., Kanzaki, M., Inoue, K., Terami, T., Katayama, A. et al. (2012) Vaspin is an adipokine ameliorating ER stress in obesity as a ligand for cell-surface GRP78/MTJ-1 complex. Diabetes 61, 2823-2832 CrossRef PubMed
7. Klöting, N., Kovacs, P., Kern, M., Heiker, J.T., Fasshauer, M., Schon, M.R., Stumvoll, M., Beck-Sickinger, A.G. and Blüher, M. (2011) Central vaspin administration acutely reduces food intake and has sustained blood glucose-lowering effects. Diabetologia 54, 1819-1823 CrossRef PubMed
8. Heiker, J.T., Klöting, N., Kovacs, P., Kuettner, E.B., Sträter, N., Schultz, S., Kern, M., Stumvoll, M., Blüher, M. and Beck-Sickinger, A.G. (2013) Vaspin inhibits kallikrein 7 by serpin mechanism. Cell. Mol. Life Sci. 70, 2569-2583 CrossRef PubMed
9. Eissa, A. and Diamandis, E.P. (2008) Human tissue kallikreins as promiscuous modulators of homeostatic skin barrier functions. Biol. Chem. 389, 669-680 CrossRef PubMed
10. Schultz, S., Saalbach, A., Heiker, J.T., Meier, R., Zellmann, T., Simon, J.C. and Beck-Sickinger, A.G. (2013) Proteolytic activation of prochemerin by kallikrein 7 breaks an ionic linkage and results in C-terminal rearrangement. Biochem. J. 452, 271-280 CrossRef PubMed
11. Saalbach, A., Vester, K., Rall, K., Tremel, J., Anderegg, U., Beck-Sickinger, A.G., Blüher, M. and Simon, J.C. (2012) Vaspin: a link of obesity and psoriasis? Exp. Dermatol. 21, 309-312 CrossRef PubMed
12. Hansson, L., Backman, A., Ny, A., Edlund, M., Ekholm, E., Ekstrand Hammarstrom, B., Tornell, J., Wallbrandt, P., Wennbo, H. and Egelrud, T. (2002) Epidermal overexpression of stratum corneum chymotryptic enzyme in mice: a model for chronic itchy dermatitis. J. Invest. Dermatol. 118, 444-449 CrossRef PubMed
13. Ny, A. and Egelrud, T. (2004) Epidermal hyperproliferation and decreased skin barrier function in mice overexpressing stratum corneum chymotryptic enzyme. Acta Derm. Venereol. 84, 18-22 CrossRef PubMed
14. Psyrri, A., Kountourakis, P., Scorilas, A., Markakis, S., Camp, R., Kowalski, D., Diamandis, E.P. and Dimopoulos, M.A. (2008) Human tissue kallikrein 7, a novel biomarker for advanced ovarian carcinoma using a novel in situquantitative method of protein expression. Ann. Oncol. 19, 1271-1277 CrossRef PubMed
15. Talieri, M., Diamandis, E.P., Gourgiotis, D., Mathioudaki, K. and Scorilas, A. (2004) Expression analysis of the human kallikrein 7 (KLK7) in breast tumors: a new potential biomarker for prognosis of breast carcinoma. Thromb. Haemost. 91, 180-186 PubMed
16. Santin, A.D., Cane, S., Bellone, S., Bignotti, E., Palmieri, M., De Las Casas, L.E., Roman, J.J., Anfossi, S., O'Brien, T. and Pecorelli, S. (2004) The serine protease stratum corneum chymotryptic enzyme (kallikrein 7) is highly overexpressed in squamous cervical cancer cells. Gynecol. Oncol. 94, 283-288 CrossRef PubMed
17. Oliveira, J.R., Bertolin, T.C., Andrade, D., Oliveira, L.C., Kondo, M.Y., Santos, J.A., Blaber, M., Juliano, L., Severino, B., Caliendo, G. et al. (2015) Specificity studies on Kallikrein-related peptidase 7 (KLK7) and effects of osmolytes and glycosaminoglycans on its peptidase activity. Biochim. Biophys. Acta 1854, 73-83 CrossRef PubMed
18. Baglin, T.P., Carrell, R.W., Church, F.C., Esmon, C.T. and Huntington, J.A. (2002) Crystal structures of native and thrombin-complexed heparin cofactor II reveal a multistep allosteric mechanism. Proc. Natl. Acad. Sci. U.S.A. 99, 11079-11084 CrossRef PubMed
19. Chen, V.C., Chao, L. and Chao, J. (2000) A positively charged loop on the surface of kallistatin functions to enhance tissue kallikrein inhibition by acting as a secondary binding site for kallikrein. J. Biol. Chem. 275, 40371-40377 CrossRef PubMed
20. Kabsch, W. (2010) Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 CrossRef PubMed
21. Evans, P.R. and Murshudov, G.N. (2013) How good are my data and what is the resolution? Acta Crystallogr. D Biol. Crystallogr. 69, 1204-1214 CrossRef
22. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 CrossRef PubMed
23. Murshudov, G.N., Skubak, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R.A., Winn, M.D., Long, F. and Vagin, A.A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367 CrossRef PubMed
24. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 CrossRef PubMed
25. Reference deleted PubMed
26. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 CrossRef PubMed
27. Painter, J. and Merritt, E.A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 62, 439-450 CrossRef PubMed
28. Painter, J. and Merritt, E.A. (2006) TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr. 39, 109-111 CrossRef
29. Chen, V.B., Arendall, 3rd, W.B., Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 CrossRef PubMed
30. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 CrossRef PubMed
31. Afonine, P.V., Moriarty, N.W., Mustyakimov, M., Sobolev, O.V., Terwilliger, T.C., Turk, D., Urzhumtsev, A. and Adams, P.D. (2015) FEM: feature-enhanced map. Acta Crystallogr. D Biol. Crystallogr. 71, 646-666 CrossRef PubMed
32. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The Protein Data Bank. Nucleic Acids Res. 28, 235-242 CrossRef PubMed
33. Horvath, A.J., Irving, J.A., Rossjohn, J., Law, R.H., Bottomley, S.P., Quinsey, N.S., Pike, R.N., Coughlin, P.B. and Whisstock, J.C. (2005) The murine orthologue of human antichymotrypsin: a structural paradigm for clade A3 serpins. J. Biol. Chem. 280, 43168-43178 CrossRef PubMed
34. Ksiazek, M., Mizgalska, D., Enghild, J.J., Scavenius, C., Thogersen, I.B. and Potempa, J. (2014) Miropin, a novel bacterial serpin from the periodontopathogen Tannerella forsythia, inhibits a broad range of proteases by using different peptide bonds within the reactive center loop. J. Biol. Chem. 290, 658-670 CrossRef PubMed
35. Schechter, N.M., Jordan, L.M., James, A.M., Cooperman, B.S., Wang, Z.M. and Rubin, H. (1993) Reaction of human chymase with reactive site variants of α1-antichymotrypsin: modulation of inhibitor versus substrate properties. J. Biol. Chem. 268, 23626-23633 PubMed
36. Greenfield, N.J. (1996) Methods to estimate the conformation of proteins and polypeptides from circular dichroism data. Anal. Biochem. 235, 1-10 CrossRef PubMed
37. Gettins, P.G. (2002) Serpin structure, mechanism, and function. Chem. Rev. 102, 4751-4804 CrossRef PubMed
38. Gettins, P.G. and Olson, S.T. (2009) Exosite determinants of serpin specificity. J. Biol. Chem. 284, 20441-20445 CrossRef PubMed
39. Chen, V.C., Chao, L., Pimenta, D.C., Bledsoe, G., Juliano, L. and Chao, J. (2001) Identification of a major heparin-binding site in kallistatin. J. Biol. Chem. 276, 1276-1284 CrossRef PubMed
40. Huntington, J.A. and Gettins, P.G. (1998) Conformational conversion of antithrombin to a fully activated substrate of factor Xa without need for heparin. Biochemistry 37, 3272-3277 CrossRef PubMed
41. Irving, J.A., Haq, I., Dickens, J.A., Faull, S.V. and Lomas, D.A. (2014) Altered native stability is the dominant basis for susceptibility of α1-antitrypsin mutants to polymerization. Biochem. J. 460, 103-115 CrossRef PubMed
42. Irving, J.A., Cabrita, L.D., Rossjohn, J., Pike, R.N., Bottomley, S.P. and Whisstock, J.C. (2003) The 1.5 Å crystal structure of a prokaryote serpin: controlling conformational change in a heated environment. Structure 11, 387-397 CrossRef PubMed
43. Bruce, D., Perry, D.J., Borg, J.Y., Carrell, R.W. and Wardell, M.R. (1994) Thromboembolic disease due to thermolabile conformational changes of antithrombin Rouen-VI (187 Asn→Asp). J. Clin. Invest. 94, 2265-2274 CrossRef PubMed
44. Mottonen, J., Strand, A., Symersky, J., Sweet, R.M., Danley, D.E., Geoghegan, K.F., Gerard, R.D. and Goldsmith, E.J. (1992) Structural basis of latency in plasminogen activator inhibitor-1. Nature 355, 270-273 CrossRef PubMed
45. Carrell, R.W., Stein, P.E., Fermi, G. and Wardell, M.R. (1994) Biological implications of a 3 Å structure of dimeric antithrombin. Structure 2, 257-270 CrossRef PubMed
46. Yamasaki, M., Sendall, T.J., Pearce, M.C., Whisstock, J.C. and Huntington, J.A. (2011) Molecular basis of α1-antitrypsin deficiency revealed by the structure of a domain-swapped trimer. EMBO Rep. 12, 1011-1017 CrossRef PubMed
47. Lomas, D.A., Evans, D.L., Finch, J.T. and Carrell, R.W. (1992) The mechanism of Z α1-antitrypsin accumulation in the liver. Nature 357, 605-607 CrossRef PubMed
48. Patston, P.A., Hauert, J., Michaud, M. and Schapira, M. (1995) Formation and properties of C1-inhibitor polymers. FEBS Lett. 368, 401-404 CrossRef PubMed
49. Jeong, E., Youn, B.S., Kim, D.W., Kim, E.H., Park, J.W., Namkoong, C., Jeong, J.Y., Yoon, S.Y., Park, J.Y., Lee, K.U. and Kim, M.S. (2010) Circadian rhythm of serum vaspin in healthy male volunteers: relation to meals. J. Clin. Endocrinol. Metab. 95, 1869-1875 CrossRef PubMed
50. Kovacs, P., Miehle, K., Sandner, B., Stumvoll, M. and Blüher, M. (2013) Insulin administration acutely decreases vaspin serum concentrations in humans. Obes. Facts 6, 86-88 CrossRef PubMed