The structure of horseradish peroxidase C characterized as a molten globule state after Ca2+ depletion

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1784, Issue 12, 2008, Pages 1965-1974

  Szigeti, Krisztián ^a,b   Smeller, László ^b   Osváth, Szabolcs ^b   Majer, Zsuzsanna ^c   Fidy, Judit ^a,b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Ca2+ depletion; Circular dichroism; Conformational dynamics; FTIR; H D exchange; High pressure; Horseradish peroxidase; pH effect; Secondary structure

Indexed keywords

ASPARTIC ACID; BENZOHYDROXAMIC ACID; CALCIUM; HISTIDINE; HORSERADISH PEROXIDASE; HORSERADISH PEROXIDASE C; UNCLASSIFIED DRUG; WATER;

ALPHA HELIX; ARTICLE; CALCIUM DEPLETION; CIRCULAR DICHROISM; ENZYME ACTIVITY; ENZYME STRUCTURE; HYDROGEN BOND; INFRARED SPECTROSCOPY; PH; PRESSURE; PRIORITY JOURNAL; TEMPERATURE; ULTRAVIOLET SPECTROSCOPY; VISCOSITY;

ARMORACIA; CALCIUM; CIRCULAR DICHROISM; HORSERADISH PEROXIDASE; HYDROGEN-ION CONCENTRATION; PLANT PROTEINS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

ARMORACIA RUSTICANA;

EID: 54549091987     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2008.08.015     Document Type: Article

References (58)

1. Smith A.T., and Veitch N.C. Structural versatility of heme peroxidases for substrate binding and catalysis. Curr. Opin. Chem. Biol. 2 (1998) 269-278
2. Ryan O., Smyth M.R., and Fagain C. Horseradish peroxidase: the analyst's friend. z 28 (1994) 129-146
3. Veitch N.C., and Smith A.T. Horseradish peroxidase. Adv. Inorg. Chem. 51 (2001) 107-162
4. Dunford H.B. Heme Peroxidases (1999), Wiley-VCH, New York
5. Huang Q., Laberge M., Szigeti K., Fidy J., and Schweitzer-Stenner R. Resonance Raman spectroscopy study of change of iron spin state in horseradish peroxidase C induced by removal of calcium. Biopolymers 72 (2003) 241-248
6. La Mar G.N., de Ropp J.S., Smith K.M., and Langry K.C. Proton nuclear magnetic resonance study of the electronic and molecular structure of the heme crevice in horseradish peroxidase. J. Biol. Chem. 255 (1980) 6646-6652
7. Smulevich G., English A.M., Mantini A.R., and Marzocchi M.P. Resonance Raman investigation of ferric iron in horseradish peroxidase and its aromatic donor complexes at room and low temperatures. Biochemistry 30 (1991) 772-779
8. Morishima I., and Ogawa S. Proton nuclear magnetic resonance spectra of compounds I and II of horseradish peroxidase. Biochemistry 17 (1978) 4384-4388
9. Teraoka J., and Kitagawa T. Structural implication of the heme-linked ionization of horseradish peroxidase probed by the Fe-Histidine stretching Raman line. J. Biol. Chem. 256 (1981) 3969-3977
10. Haschke R., and Friedhoff J.M. Calcium-related properties of horseradish peroxidase. Biochem. Biophys. Res. Commun. 80 (1978) 1039-1042
11. Ogawa S., Shiro Y., and Morishima I. Calcium binding by horseradish peroxidase C and the heme environmental structure. Biochem. Biophys. Res. Commun. 90 (1979) 674-678
12. Shiro Y., Kurono M., and Morishima I. Presence of Endogenous calcium ion and its functional and structural regulation in horseradish peroxidase. J. Biol. Chem. 261 (1986) 9382-9390
13. Morishima I., Kurono M., and Shiro Y. Presence of endogenous calcium ion in horseradish peroxidase. J. Biol. Chem. 261 (1986) 9391-9399
14. Gajhede M., Schuller D.J., Henriksen A., Smith A.T., and Poulos T.L. Crystal structure of horseradish peroxidase C at 2.15 A resolution. Nat. Struct. Mol. Biol. 4 (1997) 1032-1038
15. Nagano S., Tanaka M., Ishimori K., Watanabe Y., and Morishima I. Catalytic roles of the distal site asparagine-histidine couple in peroxidases. Biochemistry 35 (1996) 14251-14258
16. Tanaka M., Nagano S., Ishimori K., and Morishima I. Hydrogen bond network in the distal site of peroxidases: spectroscopic properties of Asn70-Asp horseradish peroxidase mutant. Biochemistry 36 (1997) 9791-9798
17. Tanaka M., Morimoto A., Ishimori K., and Morishima I. Structure-activity relation of horseradish peroxidases as studied with mutations at heme distal and proximal sites. Pure Appl. Chem. 70 (1998) 911-916
18. Tanaka M., Ishimori K., Mukai M., Kitagawa T., and Morishima I. Catalytic activities and structural properties of horseradish peroxidase distal His42 → Glu or Gln mutant. Biochemistry 36 (1997) 9889-9898
19. Tanaka M., Ishimori K., and Morishima I. Structural roles of the highly conserved Glu residue in heme distal site of peroxidase. Biochemitry 37 (1998) 2629-2638
20. Smeller L., Meersman F., Fidy J., and Heremans K. High-pressure FTIR Study of the stability of horseradish peroxidase. Effect of heme substitution, ligand binding, Ca removal, and reduction of the disulfide bonds. Biochemistry 42 (2003) 553-561
21. Kaposi A.D., Fidy J., Manas E.S., Vanderkooi J.M., and Wright W.W. Horseradish peroxidase monitored by infrared spectroscopy: effect of temperature, substrate and calcium. Biochim. Biophys. Acta 1435 (1999) 41-50
22. Feis A., Marzocchi M.P., Paoli M., and Smulevich G. Spin state and axial ligand bonding in the hydroxide complexes of metmyoglobin, methemoglobin, and horseradish peroxidase at room and low temperatures. Biochemistry 33 (1994) 4577-4583
23. Howes B.D., Rodrigez-Lopez J.N., Smith A.T., and Smulevich G. Mutation of distal residues of horseradish peroxidase: influence on substrate binding and cavity properties. Biochemistry 36 (1997) 1532-1543
24. Feis A., Howes B.D., Indiani C., and Smulevich G. Resonance Raman and electronic absorption spectra of horseradish peroxidase isozyme A2: evidence for a quantum-mixed spin species. J. Raman Spectrosc. 29 (1998) 933-938
25. Smulevich G., Feis A., Indiani C., Becucci M., and Marzocchi M.P. Peroxidase-benzhydroxamic acid complexes: spectroscopic evidence that a Fe-H2O distance of 2.6 angstrom can correspond to hexa-coordinate high-spin heme. J. Biol. Inorg. Chem. 4 (1999) 39-47
26. Howes B.D., Feiss A., Indiani C., Marzocchi M.P., and Smulevich G. Formation of two type of low-spin heme in horseradish peroxidase isoenzyme A2 at low temperature. J. Biol. Inorg. Chem. 5 (2000) 227-235
27. Indiani C., Feis A., Howes B.D., Marzocchi M.P., and Smulevich G. Benzohydroxamic acid-peroxidase complexes: spectroscopic characterization of a novel heme spin species. JACS 122 (2000) 7368-7376
28. Howes B.D., Feiss A., Raimondi L., Indiani C., and Smulevich G. The critical role of the proximal calcium ion in the structural properties of horseradish peroxidase. J. Biol. Chem. 276 (2001) 40704-40711
29. Heering H.A., Smith A.T., and Smulevich G. Spectroscopic characterization of mutations at the Phe41 position in the distal haem pocket of horseradish peroxidase C: structural and functional consequences. Biochem. J. 363 (2002) 571-579
30. Laberge M., Huang Q., Schweitzer-Stenner R., and Fidy J. The endogenous calcium ions of horseradish peroxidase C are required to maintain the functional nonplanarity of the heme. Biophys. J. 84 (2003) 2542-2552
31. Laberge M., Szigeti K., and Fidy J. The charge transfer band in horseradish peroxidase correlates with heme in-plane distortions induced by calcium removal. Biopolymers 74 (2004) 41-45
32. Laberge M., Kovesi I., Yonetani T., and Fidy J. Normal mode analysis of the horseradish peroxidase collective motions: correlation with spectroscopicalliy observed heme distortions. Biopolymers 82 (2006) 425-429
33. Huang Q., Szigeti K., Fidy J., and Schweitzer-Stenner R. Structural disorder of native horseradish peroxidase C probed by resonance Raman and low-temperature optical absorption spectroscopy. J. Phys. Chem., B 107 (2003) 2822-2830
34. Prange A., Boddeker H., and Michaelis W. Multielement determination of trace elements in whole blood and blood serum by TXRF. Fresenius Z. Anal. Chem. 335 (1989) 914-918
35. Hvidt A., and Wallevik K. Conformational changes in human serum albumin as revealed by hydrogen-deuterium exchange studies. J. Biol. Chem. 247 (1971) 1530-1535
36. Zavodszky P., Johansen J.T., and Hvidt A. Hydrogen-exchange study of the conformational stability of human carbonic anhydrase B and its metallocomplexes. Eur. J. Biochem. 56 (1975) 67-72
37. Mukai M., Nagano S., Tanaka M., Ishimori K., Morishima I., Ogura T., Watanabe Y., and Kitagawa T. Effects of concerted hydrogen bonding of distal histidine on active site structures of horseradish peroxidase. Resonance Raman studies with Asn70 Mutants. J. Am. Chem. Soc. 119 (1997) 1758-1766
38. Frauenfelder H., Fenimore P.W., and McMahon B.H. Hydration, slaving and protein function. Biophys. Chem. 98 (2002) 35-48
39. Laird B.B., and Skinner J. Microscopic theory of reversible pressure broadening in hole-burning spectra of impurities in glasses. Chem. Phys. 90 (1989) 3274-3281
40. Smeller L., Meersman F., Fidy J., and Heremans K. High-pressure FTIR Study of the stability of horseradish peroxidase. Effect of heme substitution, ligand binding, Ca removal, and reduction of the disulfide bonds. Biochemistry 42 (2003) 553-561
41. Kaposi A.D., Wright W.W., Fidy J., Stavrov S.S., Vanderkooi J.M., and Rasnik I. Carbonmonoxy horseradish peroxidase as a function of pH and substrate: influence of local electric fields on the optical and infrared spectra. Biochemistry 40 (2001) 3483-3491
42. Zelent B., Kaposi A.D., Nucci N.V., Sharp K.A., Dalosto S.D., Wright W.W., and Vanderkooi J.M. Water channel of horseradish peroxidase studied by the charge-transfer absorption band of Ferric heme. J. Phys. Chem., B 108 (2004) 10317-10324
43. Ohgushi M., and Wada A. "Molten-globule state": a compact form of globular proteins with mobile side-chains. FEBS. Lett. 164 (1983) 14-21
44. Stryer L. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of non-polar binding sites. J. Mol. Biol. 13 (1965) 482-495
45. Ptitsyn O.B., Pain R.H., Semisotnov G.V., Zerovnik E., and Razgulyaev O.I. Evidence for a molten globule state as a general intermediate in protein folding. FEBS Lett. 262 (1990) 20-24
46. Sutherland G.R.J., Zapanta L.S., Tien M., and Aust S.D. Role of calcium in maintaining the heme environment of manganese peroxidase. Biochemistry 36 (1997) 3654-3662
47. Nie G., and Aust S.D. Spectal changes of lignin peroxidase during reversible inactivation. Biochemistry 36 (1997) 5113-5119
48. 2+ depletion. Biophys. Chem. 121 (2006) 163-170
49. 2+myosin. J. Biol. Chem. 280 (2005) 41458-41464
50. Schlichter J., Friedrich J., Herenyi L., and Fidy J. Trehalose effect on low temperature protein dynamics: fluctuation and relaxation phenomena. Biophys. J. 80 (2001) 2011-2017
51. Frauenfelder H., Fenimore P.W., and McMahon B.H. Hydration, slaving and protein function. Biophys. Chem. 98 (2002) 35-48
52. Galley W.C., and Purkey R.M. Role of heterogeneity of the solvation site in electronic spectra in solution. Proc. Natl. Acad. Sci. 67 (1970) 1116-1121
53. Bersuker I.B., and Stavrov S.S. Structure and properties of metalloporphyrins and hemoproteins: the vibronic approach. Coord. Chem. Rev. 88 (1988) 1-68
54. Henriksen A., Schuller D.J., Meno K., Welinder K.G., Smith A.T., and Gajhede M. Structural interactions between horseradish peroxidase C and the substrate benzhydroxamic acid determined by X-ray crystallography. Biochemistry 37 (1998) 8054-8060
55. Balog E., Kis-Petik K., Fidy J., Köhler M., and Friedrich J. Interpretation of multiple Q(0,0) bands in the absorption spectrum of Mg-mesoporphyrin embedded in horseradish peroxidase. Biophys. J. 73 (1997) 397-405
56. G. Smulevich, A. Feis, C. Indiani, M. Becucci, M.P. Marzocchi. Peroxidase-benzhydroxamic acid complexes: spectroscopic evidence that a Fe-H2O distance of 2.6 angstrom can correspond to hexa-coordinate high-spin heme. J. Biol. Inorg. Chem. 4 (99) (1999) 39-47.
57. Fidy J., Paul K.G., and Vanderkooi J.M. Differences in the binding of aromatic substrates to horseradish peroxidase revealed by fluorescence line narrowing. Biochemistry 28 (1989) 531-7541
58. Banci L., Carloni P., Diaz A., and Savellini G.G. Molecular dynamics calculation on peroxidases: the effect of calcium ions on protein structure. J. Biol. Inorg. Chem. 1 (1996) 264-272