Folding transitions in calpain activator peptides studied by solution NMR spectroscopy

Journal of Peptide Science

Volumn 15, Issue 6, 2009, Pages 404-410

  Toke, Orsolya ^a   Bánóczi, Zoltán ^b   Tárkányi, Gábor ^a   Friedrich, Péter ^c   Hudecz, Ferenc ^b,d  

^a CHEMICAL RESEARCH CENTER   (Hungary)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Calcium binding; Calpain; Calpastatin; Conformational change; Folding; Inhibitor; Intrinsically unstructured proteins; NMR spectroscopy; Order disorder transition

Indexed keywords

CALCIUM ION; CALPAIN; CALPASTATIN; HELICASE; METHANOL; PROTEIN CALPA; PROTEIN CALPC; UNCLASSIFIED DRUG; WATER; CALCIUM; CALCIUM BINDING PROTEIN; PEPTIDE;

ARTICLE; CALCIUM BINDING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVATION; HYDROPHOBICITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; STRUCTURE ANALYSIS; CHEMISTRY; DRUG EFFECT; METABOLISM; METHODOLOGY;

EUKARYOTA;

CALCIUM; CALCIUM-BINDING PROTEINS; CALPAIN; ENZYME ACTIVATION; MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 67649743774     PISSN: 10752617     EISSN: 10991387     Source Type: Journal    
DOI: 10.1002/psc.1131     Document Type: Article

References (38)

1. Sorimachi H, Ishiura S, Suzuki K. Structure and physiological function of calpains. Biochem. J. 1997; 328: 721-732.
2. Goll DE, Thompson V, Li FH, Wei W, Cong J. The calpain system. Physiol. Rev. 2003; 83: 731-801.
3. Wells A, Huttenlocher A, Lauffenburger DA. Calpain proteases in cell adhesion and motility. Int. Rev. Cytol. 2005; 245: 1-16.
4. Sato K, Kawashima S. Calpain function in the modulation of signal transduction molecules. Biol. Chem. 2001; 382: 743-751.
5. Schollmeyer JE. Calpain II involvement inmitosis. Science 1988; 240: 911-913.
6. Lu T, Xu Y, Mericle MT, Mellgren RL. Participation of the conventional calpains in apoptosis. Biochim. Biophys. Acta 2002; 1590: 16-26.
7. Sato K, Saito Y, Kawashima S. Identification and characterization of membrane-bound calpains in clathrin-coated vesicles from bovine brain. Eur. J. Biochem. 1995; 230: 25-31.
8. Hirai S, Kawasaki H, Yaniv M, Suzuki K. Degradation of transcription factors, c-Jun and c-Fos, by calpains. FEBS Lett. 1991; 287: 57-61.
9. Hong SC, Goto Y, Lanzino G, Soleau S, Kassell NF, Lee KS. Neuroprotectionwith a calpain inhibitor in a model of focal cerebral ischemia. Stroke 1994; 25: 663-669.
10. Jordan J, Galindo MF, Miller RJ. Role of calpain- and interleukin-1 beta converting enzyme-like proteases in the beta-amyloid-induced death of rat hippocampal neurons in culture. J Neurochem. 1997; 68: 1612-1621.
11. Huang Y, Wang KKW. The calpain family and human disease. Trends Mol. Med. 2001; 7: 355-362.
12. Wendt A, Thompson VF, Goll DE. Interaction of calpastatin with calpain: a review. Biol. Chem. 2004; 385: 465-472.
13. Konno T, Tanaka N, Kataoka M, Takano E, Maki M. A circular dichroism study of preferential hydration and alcohol effects on a denaturated protein, pig calpastatin domain I. Biochim. Biophys. Acta 1997; 1342: 73-82.
14. Emori Y, Kawasaki H, Imajoh S, Minami Y, Suzuki K. All 4 repeating domains of the endogeneous inhibitor for calcium-dependent protease independently retain inhibitory activity: expression of the cDNA fragments in Escherichia coli. J. Biol. Chem. 1988; 263: 2364-2370.
15. Maki M, Bagci H, Hamaguchi K, Ueda M, Murachi T, Hatanaka M. Inhibition of calpain by a synthetic oligopeptide corresponding to an exon of the human calpastatin gene. J. Biol. Chem. 1989; 264: 18866-18869.
16. Moldoveanu T, Gehring KK, Green DR. Concerted multi-prolonged attack by calpastatin to occlude the catalytic cleft of heterodimeric calpains. Nature 2008; 456: 404-408.
17. Hanna RA, Campbell RL, Davies PL. Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature 2008; 456: 409-412.
18. Dyson HJ, Wright PE. Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 2002; 12: 54-60.
19. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z. Intrinsic disorder and protein function. Biochemistry 2002; 41: 6573-6582.
20. Tompa P. Intrinsically unstructured proteins. Trends Biochem. Sci. 2002; 27: 527-533.
21. Tompa P, Mucsi Z, Orosz G, Friedrich P. Calpastatin subdomains A and C are activators of calpain. J. Biol. Chem. 2002; 277: 9022-9026.
22. Wüthrich K. NMR of Proteins and Nucleic Acids. Wiley: New York, 1986.
23. Hwang TL, Shaka AJ. Water suppression that works. Excitation sculpting using arbitrary waveforms and pulsed field gradients. J. Magn. Reson., Ser. A 1995; 112: 275-279.
24. Linge JP, O'Donoghue SI, Nilges M. Automated assignment of ambiguous nuclear overhauser effects with ARIA. Methods Enzymol. 2001; 339: 71-90.
25. Habeck M, RiepingW, Linge JP, Nilges M. In NOE Assignment with ARIA 2.0, Methods in Molecular Biology, Volume 278: Protein NMR Techniques, Downing AK (ed). Humana Press: Totowa, 2004.
26. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 1993; 26: 283-291.
27. Laskowski RA, Rullmann JA, MacArthur MW, Kaptein R, Thornton JM. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 1996; 8: 477-486.
28. Todd B, Moore D, Deivanayagam CCS, Lin GD, Chattopadhyay D, Maki M, Wang KKW, Narayana SVL. A structural model for the inhibition of calpain by calpastatin: crystal structures of the native domain VI of calpain and its complexeswith calpastatin peptide and a small molecule inhibitor. J. Mol. Biol. 2003; 328: 131-146.
29. Ishima R, Tamura A, Akasaka K, Hamaguchi K, Makino K, Murachi T, Hatanaka M, Maki M. Structure of the active 27-residue fragment of human calpastatin. FEBS Lett. 1991; 294: 64-66.
30. Kiss R, Kovacs D, Tompa P, Perczel A. Local structural preferences of calpastatin, the intrinsically unstructures protein inhibitor of calpain. Biochemistry 2008; 47: 6936-6945.
31. Daughdrill GW, Hanely LJ, Dahlquist FW. The C-terminal half of the anti-s factor FlgM contains a dynamic equilibrium solution structure favoring helical conformations. Biochemistry 1998; 37: 1076-1082.
32. Bienkiewicz EA, Adkins JN, Lumb KJ. Functional consequences of preorganized helical structure in the intrinsically disordered cell-cycle inhibitor p27(Kip1). Biochemistry 2002; 41: 752-759.
33. Hua QX, Jia WH, Bullock BP, Habener JF, Weiss MA. Transcriptional activator-coactivator recognition: nascent folding of a kinaseinducible transactivation domain predicts its structure on coactivator binding. Biochemistry 1998; 37: 5858-5866.
34. Lee H, Mok KH, Muhandiram R, Park KH, Suk JE, Kim DH, Chung J, Sung YC, Choi KY, Han KH. Local structural elements in the mostly unstructured transcriptional activation domain of human p53. J. Biol. Chem. 2000; 275: 29426-29432.
35. Mucsi Z, Hudecz F, Hollósi M, Tompa P, Friedrich P. Binding-induced folding transitions in calpastatin subdomains A and C. Protein Sci. 2003; 12: 2327-2336.
36. Pidcock E, Moore GR. Structural characteristics of protein binding sites for calcium and lanthanide ions. J. Biol. Inorg. Chem. 2001; 6: 479-489.
37. Kiss R, Bozoky Z, Kovacs D, Rona G, Friedrich P, Dvortsak P, Weisemann R, Tompa P, Perczel A. Calcium-induced tripartite binding of intrinsicaly disordered calpastatin to its cognate enzyme, calpain. FEBS Lett. 2008; 582: 2149-2154.
38. Hackel M, Konno T, Hinz H. A new alternative method to quantify residual structure in 'unfolded' proteins. Biochim. Biophys. Acta 2000; 1479: 155-165.