Hydrogen/deuterium exchange mass spectrometry reveals specific changes in the local flexibility of plasminogen activator inhibitor 1 upon binding to the somatomedin B domain of vitronectin

Biochemistry

Volumn 51, Issue 41, 2012, Pages 8256-8266

  Trelle, Morten Beck ^a   Hirschberg, Daniel ^a   Jansson, Anna ^a   Ploug, Michael ^b   Roepstorff, Peter ^a   Andreasen, Peter A ^c   Jørgensen, Thomas J D ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b Rigshospitalet   (Denmark)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING INTERFACE; COFACTORS; HYDROGEN/DEUTERIUM EXCHANGE; LOCAL FLEXIBILITY; PLASMINOGEN ACTIVATOR INHIBITOR-1; STRUCTURAL FLEXIBILITIES; VITRONECTIN; WILD TYPES;

MASS SPECTROMETRY;

PEPTIDES;

DEUTERIUM; HYDROGEN; PLASMINOGEN ACTIVATOR INHIBITOR 1; SOMATOMEDIN B; VITRONECTIN;

ARTICLE; BETA SHEET; BINDING SITE; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STABILITY; STRUCTURE ANALYSIS; THERMODYNAMICS; THERMOSTABILITY;

DEUTERIUM; HYDROGEN; MASS SPECTROMETRY; MODELS, MOLECULAR; PLASMINOGEN ACTIVATOR INHIBITOR 1; SOMATOMEDINS; VITRONECTIN;

EID: 84867501635     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3008998     Document Type: Article

References (47)

1. Gettins, P. G. (2002) Serpin structure, mechanism, and function Chem. Rev. 102, 4751-4804
2. Dupont, D. M., Madsen, J. B., Kristensen, T., Bodker, J. S., Blouse, G. E., Wind, T., and Andreasen, P. A. (2009) Biochemical properties of plasminogen activator inhibitor-1 Front. Biosci. 14, 1337-1361
3. Wind, T., Hansen, M., Jensen, J. K., and Andreasen, P. A. (2002) The molecular basis for anti-proteolytic and non-proteolytic functions of plasminogen activator inhibitor type-1: Roles of the reactive centre loop, the shutter region, the flexible joint region and the small serpin fragment Biol. Chem. 383, 21-36 (Pubitemid 34224025)
4. Kaslik, G., Kardos, J., Szabo, E., Szilagyi, L., Zavodszky, P., Westler, W. M., Markley, J. L., and Graf, L. (1997) Effects of serpin binding on the target proteinase: global stabilization, localized increased structural flexibility, and conserved hydrogen bonding at the active site Biochemistry 36, 5455-5464 (Pubitemid 27200042)
5. Takehara, S., Onda, M., Zhang, J., Nishiyama, M., Yang, X., Mikami, B., and Lomas, D. A. (2009) The 2.1-Å crystal structure of native neuroserpin reveals unique structural elements that contribute to conformational instability J. Mol. Biol. 388, 11-20
6. Stein, P. and Chothia, C. (1991) Serpin tertiary structure transformation J. Mol. Biol. 221, 615-621 (Pubitemid 121003403)
7. 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
8. Beauchamp, N. J., Pike, R. N., Daly, M., Butler, L., Makris, M., Dafforn, T. R., Zhou, A., Fitton, H. L., Preston, F. E., Peake, I. R., and Carrell, R. W. (1998) Antithrombins Wibble and Wobble (T85M/K): Archetypal conformational diseases with in vivo latent-transition, thrombosis, and heparin activation Blood 92, 2696-2706 (Pubitemid 28469081)
9. Im, H., Woo, M. S., Hwang, K. Y., and Yu, M. H. (2002) Interactions causing the kinetic trap in serpin protein folding J. Biol. Chem. 277, 46347-46354 (Pubitemid 35417629)
10. Lindahl, T. L., Sigurdardottir, O., and Wiman, B. (1989) Stability of plasminogen activator inhibitor 1 (PAI-1) Thromb. Haemostasis 62, 748-751 (Pubitemid 19267430)
11. Sancho, E., Tonge, D. W., Hockney, R. C., and Booth, N. A. (1994) Purification and characterization of active and stable recombinant plasminogen-activator inhibitor accumulated at high levels in Escherichia coli Eur. J. Biochem. 224, 125-134 (Pubitemid 24267113)
12. Declerck, P. J., De Mol, M., Alessi, M. C., Baudner, S., Paques, E. P., Preissner, K. T., Muller-Berghaus, G., and Collen, D. (1988) Purification and characterization of a plasminogen activator inhibitor 1 binding protein from human plasma. Identification as a multimeric form of S protein (vitronectin) J. Biol. Chem. 263, 15454-15461
13. Bodker, J. S., Wind, T., Jensen, J. K., Hansen, M., Pedersen, K. E., and Andreasen, P. A. (2003) Mapping of the epitope of a monoclonal antibody protecting plasminogen activator inhibitor-1 against inactivating agents Eur. J. Biochem. 270, 1672-1679 (Pubitemid 36532526)
14. Hansen, M., Busse, M. N., and Andreasen, P. A. (2001) Importance of the amino-acid composition of the shutter region of plasminogen activator inhibitor-1 for its transitions to latent and substrate forms Eur. J. Biochem. 268, 6274-6283 (Pubitemid 33132049)
15. Berkenpas, M. B., Lawrence, D. A., and Ginsburg, D. (1995) Molecular evolution of plasminogen activator inhibitor-1 functional stability EMBO J. 14, 2969-2977
16. Jensen, J. K., Thompson, L. C., Bucci, J. C., Nissen, P., Gettins, P. G., Peterson, C. B., Andreasen, P. A., and Morth, J. P. (2011) Crystal structure of plasminogen activator inhibitor-1 in an active conformation with normal thermodynamic stability J. Biol. Chem. 286, 29709-29717
17. Zhou, A., Huntington, J. A., Pannu, N. S., Carrell, R. W., and Read, R. J. (2003) How vitronectin binds PAI-1 to modulate fibrinolysis and cell migration Nat. Struct. Biol. 10, 541-544 (Pubitemid 36792905)
18. Salonen, E. M., Vaheri, A., Pollanen, J., Stephens, R., Andreasen, P., Mayer, M., Dano, K., Gailit, J., and Ruoslahti, E. (1989) Interaction of plasminogen activator inhibitor (PAI-1) with vitronectin J. Biol. Chem. 264, 6339-6343 (Pubitemid 19106712)
19. Seiffert, D. and Loskutoff, D. J. (1991) Kinetic analysis of the interaction between type 1 plasminogen activator inhibitor and vitronectin and evidence that the bovine inhibitor binds to a thrombin-derived amino-terminal fragment of bovine vitronectin Biochim. Biophys. Acta 1078, 23-30
20. Lawrence, D. A., Palaniappan, S., Stefansson, S., Olson, S. T., Francis-Chmura, A. M., Shore, J. D., and Ginsburg, D. (1997) Characterization of the binding of different conformational forms of plasminogen activator inhibitor-1 to vitronectin. Implications for the regulation of pericellular proteolysis J. Biol. Chem. 272, 7676-7680 (Pubitemid 27137317)
21. Schar, C. R., Jensen, J. K., Christensen, A., Blouse, G. E., Andreasen, P. A., and Peterson, C. B. (2008) Characterization of a site on PAI-1 that binds to vitronectin outside of the somatomedin B domain J. Biol. Chem. 283, 28487-28496
22. Schar, C. R., Blouse, G. E., Minor, K. H., and Peterson, C. B. (2008) A deletion mutant of vitronectin lacking the somatomedin B domain exhibits residual plasminogen activator inhibitor-1-binding activity J. Biol. Chem. 283, 10297-10309
23. Jensen, J. K., Wind, T., and Andreasen, P. A. (2002) The vitronectin binding area of plasminogen activator inhibitor-1, mapped by mutagenesis and protection against an inactivating organochemical ligand FEBS Lett. 521, 91-94 (Pubitemid 34628465)
24. Seiffert, D., Ciambrone, G., Wagner, N. V., Binder, B. R., and Loskutoff, D. J. (1994) The somatomedin B domain of vitronectin. Structural requirements for the binding and stabilization of active type 1 plasminogen activator inhibitor J. Biol. Chem. 269, 2659-2666
25. Kjaergaard, M., Gardsvoll, H., Hirschberg, D., Nielbo, S., Mayasundari, A., Peterson, C. B., Jansson, A., Jorgensen, T. J., Poulsen, F. M., and Ploug, M. (2007) Solution structure of recombinant somatomedin B domain from vitronectin produced in Pichia pastoris Protein Sci. 16, 1934-1945 (Pubitemid 47367116)
26. Mathiasen, L., Dupont, D. M., Christensen, A., Blouse, G. E., Jensen, J. K., Gils, A., Declerck, P. J., Wind, T., and Andreasen, P. A. (2008) A peptide accelerating the conversion of plasminogen activator inhibitor-1 to an inactive latent state Mol. Pharmacol. 74, 641-653
27. Rist, W., Mayer, M. P., Andersen, J. S., Roepstorff, P., and Jorgensen, T. J. (2005) Rapid desalting of protein samples for on-line microflow electrospray ionization mass spectrometry Anal. Biochem. 342, 160-162 (Pubitemid 40805640)
28. Stout, T. J., Graham, H., Buckley, D. I., and Matthews, D. J. (2000) Structures of active and latent PAI-1: A possible stabilizing role for chloride ions Biochemistry 39, 8460-8469 (Pubitemid 30489942)
29. Tsutsui, Y., Liu, L., Gershenson, A., and Wintrode, P. L. (2006) The conformational dynamics of a metastable serpin studied by hydrogen exchange and mass spectrometry Biochemistry 45, 6561-6569 (Pubitemid 43825356)
30. Sengupta, T., Tsutsui, Y., and Wintrode, P. L. (2009) Local and global effects of a cavity filling mutation in a metastable serpin Biochemistry 48, 8233-8240
31. Sarkar, A., Zhou, C., Meklemburg, R., and Wintrode, P. L. (2011) Local conformational flexibility provides a basis for facile polymer formation in human neuroserpin Biophys. J. 101, 1758-1765
32. Nukuna, B. N., Penn, M. S., Anderson, V. E., and Hazen, S. L. (2004) Latency and substrate binding globally reduce solvent accessibility of plasminogen activator inhibitor type 1 (PAI-1). An adaptation of PAI-1 conformer crystal structures by hydrogen-deuterium exchange J. Biol. Chem. 279, 50132-50141 (Pubitemid 39577825)
33. Egelund, R., Schousboe, S. L., Sottrup-Jensen, L., Rodenburg, K. W., and Andreasen, P. A. (1997) Type-1 plasminogen-activator inhibitor: Conformational differences between latent, active, reactive-centre-cleaved and plasminogen-activator-complexed forms, as probed by proteolytic susceptibility Eur. J. Biochem. 248, 775-785 (Pubitemid 27400032)
34. Fa, M., Karolin, J., Aleshkov, S., Strandberg, L., Johansson, L. B., and Ny, T. (1995) Time-resolved polarized fluorescence spectroscopy studies of plasminogen activator inhibitor type 1: Conformational changes of the reactive center upon interactions with target proteases, vitronectin and heparin Biochemistry 34, 13833-13840
35. Gibson, A., Baburaj, K., Day, D. E., Verhamme, I., Shore, J. D., and Peterson, C. B. (1997) The use of fluorescent probes to characterize conformational changes in the interaction between vitronectin and plasminogen activator inhibitor-1 J. Biol. Chem. 272, 5112-5121 (Pubitemid 27090067)
36. Keijer, J., Ehrlich, H. J., Linders, M., Preissner, K. T., and Pannekoek, H. (1991) Vitronectin governs the interaction between plasminogen activator inhibitor 1 and tissue-type plasminogen activator J. Biol. Chem. 266, 10700-10707 (Pubitemid 21906858)
37. Egelund, R., Einholm, A. P., Pedersen, K. E., Nielsen, R. W., Christensen, A., Deinum, J., and Andreasen, P. A. (2001) A regulatory hydrophobic area in the flexible joint region of plasminogen activator inhibitor-1, defined with fluorescent activity-neutralizing ligands. Ligand-induced serpin polymerization J. Biol. Chem. 276, 13077-13086
38. Kjoller, L., Martensen, P. M., Sottrup-Jensen, L., Justesen, J., Rodenburg, K. W., and Andreasen, P. A. (1996) Conformational changes of the reactive-centre loop and β-strand 5A accompany temperature-dependent inhibitor-substrate transition of plasminogen-activator inhibitor 1 Eur. J. Biochem. 241, 38-46 (Pubitemid 26342969)
39. Harrop, S. J., Jankova, L., Coles, M., Jardine, D., Whittaker, J. S., Gould, A. R., Meister, A., King, G. C., Mabbutt, B. C., and Curmi, P. M. (1999) The crystal structure of plasminogen activator inhibitor 2 at 2.0 Å resolution: Implications for serpin function Structure 7, 43-54 (Pubitemid 29159181)
40. Lawrence, D. A., Olson, S. T., Palaniappan, S., and Ginsburg, D. (1994) Serpin reactive center loop mobility is required for inhibitor function but not for enzyme recognition J. Biol. Chem. 269, 27657-27662 (Pubitemid 24346602)
41. Belorgey, D., Crowther, D. C., Mahadeva, R., and Lomas, D. A. (2002) Mutant neuroserpin (S49P) that causes familial encephalopathy with neuroserpin inclusion bodies is a poor proteinase inhibitor and readily forms polymers in vitro J. Biol. Chem. 277, 17367-17373 (Pubitemid 34967773)
42. Onda, M., Belorgey, D., Sharp, L. K., and Lomas, D. A. (2005) Latent S49P neuroserpin forms polymers in the dementia familial encephalopathy with neuroserpin inclusion bodies J. Biol. Chem. 280, 13735-13741 (Pubitemid 40517269)
43. Tsutsui, Y. and Wintrode, P. L. (2007) Cooperative unfolding of a metastable serpin to a molten globule suggests a link between functional and folding energy landscapes J. Mol. Biol. 371, 245-255 (Pubitemid 47030465)
44. Seo, E. J., Lee, C., and Yu, M. H. (2002) Concerted regulation of inhibitory activity of α1-antitrypsin by the native strain distributed throughout the molecule J. Biol. Chem. 277, 14216-14220 (Pubitemid 34968035)
45. Podor, T. J., Campbell, S., Chindemi, P., Foulon, D. M., Farrell, D. H., Walton, P. D., Weitz, J. I., and Peterson, C. B. (2002) Incorporation of vitronectin into fibrin clots. Evidence for a binding interaction between vitronectin and γA/γ' fibrinogen J. Biol. Chem. 277, 7520-7528 (Pubitemid 34953150)
46. Pollanen, J., Saksela, O., Salonen, E. M., Andreasen, P., Nielsen, L., Dano, K., and Vaheri, A. (1987) Distinct localizations of urokinase-type plasminogen activator and its type 1 inhibitor under cultured human fibroblasts and sarcoma cells J. Cell Biol. 104, 1085-1096 (Pubitemid 17068679)
47. Li, S. H., Gorlatova, N. V., Lawrence, D. A., and Schwartz, B. S. (2008) Structural differences between active forms of plasminogen activator inhibitor type 1 revealed by conformationally sensitive ligands J. Biol. Chem. 283, 18147-18157