ADP-binding and ATP-binding sites in native and proteinase-K-digested creative kinase, probed by reaction-induced difference infrared spectroscopy

European Journal of Biochemistry

Volumn 247, Issue 3, 1997, Pages 1197-1208

  Raimbault, Cyrille ^a   Clottes, Eric ^a   Leydier, Chantal ^a   Vial, Christian ^a   Buchet, René ^a  

^a UNIVERSITÉ LYON 1   (France)

Author keywords

Caged nucleotide; Caged phosphate; Creatine kinase; Fourier transform infrared spectroscopy; Protein conformation

Indexed keywords

CREATINE KINASE;

ARTICLE; BINDING SITE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME BINDING; INFRARED SPECTROSCOPY; PHOTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; RABBIT;

ORYCTOLAGUS CUNICULUS;

EID: 0030789742     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.01197.x     Document Type: Article

References (96)

1. Babbitt, P. C., Kenyon, G. L., Kuntz, I. D., Cohen, F. E., Baxter, J. D., Benfield, P. A., Buskin, J. D., Gilbert, W. A., Hauschka, S. D., Hossle, J. P., Ordahl, C. H., Pearson, M. L., Perriard, J. C., Pickering, L. A., Putney, S. D., West, B. L. & Ziven, R. A. (1986) Comparisons of creatine kinase primary structures, J. Protein Chem. 5, 1-14.
2. Balny, C., Travers, F., Barman, T. & Douzou, P. (1985) Cryobaroenzymic studies as a tool for investigating activated complexes: creatine kinase · ADP · Mg · nitrate · creatine as a model, Proc. Natl Acad. Sci. USA 82, 7495-7499.
3. Bandekar, J. (1992) Amide modes and protein conformation, Biochim. Biophys. Acta 1120, 123-143.
4. Barth, A., Kreutz, W. & Mantele W. (1990) Molecular changes in the sarcoplasmic reticulum calcium ATPase during catalytic activity, FEBS Lett. 277, 147-150.
5. Barth, A., Mäntele, W. & Kreutz, W. (1991) Infrared spectroscopic signals arising from ligand binding and conformational changes in the catalytic cycle of sarcoplasmic reticulum calcium ATPase, Biochim. Biophys. Acta 1057, 115-123.
6. 2+-ATPase: investigation of nucleotide-binding, phosphorylation and phosphoenzyme conversion by FTIR difference spectroscopy, Biochim. Biophys. Acta 1194, 75-91.
7. Bensadoun, A. & Weinstein, D. (1976) Assay of protein in the presence of interfering materials, Anal. Biochem. 70, 241-256.
8. Bessman, S. P. & Carpenter, C. L. (1985) The creatine-creatine phosphate energy shuttle, Annu. Rev. Biochem. 54, 831-862.
9. Borders, C. L. & Riordan, J. F. (1975) An essential arginyl residue at the nucleotide-binding site of creatine kinase, Biochemistry 14, 4699-4704.
10. 2+ alters the FTIR spectrum of sarcoplasmic reticulum, Biochim. Biophys. Acta 1069, 209-217.
11. 2+, Biochim. Biophys. Acta 1104, 207-214.
12. Buechter, D. D., Medzihradszky, K. F., Burlingame, A. L. & Kenyon, G. L. (1992) The active site of creatine kinase, J. Biol. Chem. 267, 2173-2178.
13. Byler, M. D. & Susi, H. (1986) Examination of the secondary structure of proteins by deconvolved FTIR spectra, Biopolymers 25, 469-487.
14. Chirgadze, Y. N., Fedorov, O. V. & Trushina, N. P. (1975) Estimation of amino acid residue side-chain absorption in the infrared spectra of protein solutions in heavy water, Biopolymers 14, 679-694.
15. Clottes, E., Leydier, C., Couthon, F., Marcillat, O. & Vial, C. (1997) Denaturation by guanidinium hydrochloride of dimeric MM-creatine kinase and its proteinase K nicked form: evidence for a multiple step-process, Biochim. Biophys. Acta 1338, 37-47.
16. 2+-ATPase by a nonionic detergent, J. Biol. Chem. 252, 3551-3553.
17. Fattoum, A., Kassab, R. & Pradel, L. A. (1975) The tyrosyl residues in creatine kinase modification by iodine, Biochim. Biophys. Acta 405, 324-339.
18. Font, B., Vial, C., Goldschmidt, D., Eichenberger, D. & Gautheron, D. (1981) Heart mitochondrial creatine kinase solubilisation effects of mitochondrial swelling and SH group reagents, Arch. Biochem. Biophys. 212, 195-203.
19. Fringeli, U. P. (1992) In situ infrared attenuated total reflection (IR ATR) spectroscopy: a complementary analytical tool for drug design and drug delivery, Chimia 46, 200-214.
20. Fritz-Wolf, K., Schnyder, T., Wallimann, T. & Kabsch, W. (1996) Structure of mitochondrial creatine kinase, Nature 381, 341-345.
21. Furter, R., Furter-Graves, E. M. & Wallimann, T. (1993) Creatine kinase: the reactive cysteine is required for synergism but is nonessential for catalysis, Biochemistry 32, 7022-7029.
22. Gabriel, J. L. & Davis, R. C. (1977) Circular dichroism of colbatous complexes of creatine kinase, Biochemistry 16, 5364-5367.
23. 2+ binding studied by simultaneous measurements of infrared absorbance changes and changes of intrinsic fluorescence, Biochim. Biophys. Acta 1188, 139-150.
24. Glasoe, P. K. & Long, F. A. (1960) Use of glass electrodes to measure acidities in deuterium oxide, J. Phys. Chem. 64, 188-190.
25. Goormaghtigh, E., Cabiaux, V. & Ruysschaert, J. M. (1994) Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy 1. Assignments and model compounds in subcellular biochemistry, in Physical methods in the study of biomembranes (Hilderson, H. J. & Ralston, G. B., eds) vol. 23, pp. 329-362, Plenum Press, New York.
26. Görne-Tschelnokow, U., Hucho, F., Naumann, D., Barth, A. & Mäntele, W. (1992) Fourier transform infrared (FTIR) spectroscopic investigation of the nicotinic acetylcholine receptor (nAChR), FEBS Lett. 309, 213-217.
27. Gross, M. & Wallimann, T. (1995) Dimer-dimer interactions in octameric mitochondrial creatine kinase, Biochemistry 34, 6660-6667.
28. Grossman, S. H. (1991) Conformational heterogeneity of creatine kinase determined from phase resolved fluorometry, Biophys. J. 59, 590-597.
29. Grossman, S. H., France, R. M. & Mattheis, J. R. (1992) Heterogeneous flexibilities of the active site domains of homodimeric creatine kinase: effect of substrate, Biochim. Biophys. Acta 1159, 29-36.
30. Hammes, G. G. & Hurst, J. K. (1969) Relaxation spectra of adenosine triphosphate-creatine phosphotransferase, Biochemistry 8, 1083-1094.
31. Hansen, D. E. & Knowles, J. R. (1981) The stereochemical course of the reaction catalyzed by creatine kinase, J. Biol. Chem. 256, 5967-5969.
32. Jackson, M. & Mantsch, H. H. (1995) The use and misuse of FTIR spectroscopy in the determination of protein structure, Crit. Rev. Biochem. Mol. Biol. 30, 95-120.
33. James, P., Wyss, M., Lutsenko, S., Wallimann, T. & Carafoli, E. (1990) ATP binding site of mitochondrial creatine kinase, FEBS Lett. 273, 139-143.
34. 31P NMR measurements using Mn (II) and Co(II), Biochemistry 24, 3487-3494.
35. Kaplan, J. H., Forbusch, B. III & Hoffman, J. F. (1978) Rapid photolytic release of adenosine 5′-triphosphate from a protected analogue: utilization by the Na: K pump of human red blood cell ghosts, Biochemistry 17, 1929-1935.
36. Kassab, R., Pradel, A., Der Terrosian, E. & Thoai, N. V. (1967) Comparaison des groupes SH réactifs des ATP: guanidines phosphotransferases, Biochim. Biophys. Acta 132, 347-360.
37. 2 lysine essentiels avec le 1-diméthylaminonaphtaléne-5-sulfochlorure, Biochim. Biophys. Acta 167, 308-316.
38. Keighren, M. A. & Price, N. C. (1978) A study of the role of the reactive thiol group of rabbit muscle creatine kinase with a chromophoric reporter group, Biochem. J. 171, 269-272.
39. Krimm, S. & Bandekar, J. (1986) Vibrational spectroscopy and conformation of peptides, polypeptides and proteins, Adv. Protein Chem. 38, 181-386.
40. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
41. Lebherz, H. G., Burke, T., Shackelford, J. E., Strickler, J. E. & Wilson, K. J. (1986) Specific proteolytic modification of creatine kinase isoenzymes. Implication of C terminal involvement in enzymic activity but not in subunit recognition, Biochem. J. 233, 51-56.
42. Leydier, C., Andersen, J. S., Couthon, F., Forest, E., Marcillat, O., Denoroy, L., Vial, C. & Clottes, E. (1997) Proteinase K processing of rabbit muscle creatine kinase, J. Protein Chem. 16, 67-74.
43. Leyh, T. S., Goodhart, P. J., Nguyen, A. C., Kenyon, G. L. & Reed, G. H. (1985) Structures of manganese (II) complexes with ATP, ADP, and Phosphocreatine in the reactive central complexes with creatine kinase: Electron Paramagnetic Resonance studies with oxygen-17-labeled ligands, Biochemistry 24, 308-316.
44. Lough, J., Wrenn, D. S., Miziorko, H. M. & Auer, H. E. (1985) Differential sensitivity of chicken MM-creatine kinase to trypsin and proteinase-K, Int. J. Biochem. 17, 309-318.
45. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951) Protein measurement with the folin phenol reagent, J. Biol. Chem. 193, 265-275.
46. Mahowald, T. A., Noltmann, E. A. & Kuby, S. A. (1962) Studies on adenosine triphosphate transphophosrylases inhibition reaction, J. Biol. Chem. 237, 1535-1548.
47. Marcillat, O., Goldschmidt, D., Eichenberger, D. & Vial, C. (1987) Only one of the two interconvertible forms of creatine kinase binds to heart mitoplasts, Biochim. Biophys. Acta 890, 233-241.
48. 3S-blocked creatine kinase with altered catalytic activity, J. Biol. Chem. 252, 1202-1207.
49. Mäntele, W. (1993) Reaction-induced infrared difference spectroscopy for the study of protein function and reaction mechanisms, Trends Biochem. Sci. 18, 197-202.
50. Messmer, C. H. & Kägi, H. R. (1985) Tryptophan residues of creatine kinase: a fluorescence study, Biochemistry 24, 7172-7178.
51. Milner-White, E. J. & Watts, D. C. (1971) Inhibition of adenosine 5′-triphosphate-creatine phosphotransferase by substrate-anion complexes, Biochem. J. 122, 727-740.
52. Morris, G. E., Frost, L. C. & Head, L. P. (1985) Monoclonal-antibody studies of creatine kinase, Biochem. J. 228, 375-381.
53. Mühlebach, S. M., Gross, M., Wirz, T., Wallimann, T., Perriard, J.-C. & Wyss, M. (1994) IV-2 sequence homology and structure predictions of the creatine kinase isoenzymes, Mol. Cell. Biochem. 133/134, 245-262.
54. Murali, N., Jarori, G. K., Landy, S. B. & Nageswara Rao, B. D. (1993) Two-dimensional transferred nuclear Overhauser effect spectroscopy (TRNOESY) studies of nucleotide conformations in creatine kinase complexes: effects due to weak nonspecific binding, Biochemistry 32, 12941-12948.
55. 31P NMR of enzyme-bound substrates of rabbit muscle creatine kinase equilibrium constants, interconversion rates and NMR parameters of enzyme-bound complexes, J. Biol. Chem. 256, 1716-1721.
56. Olcott, M. C., Bradley, M. L. & Haley, B. E. (1994) Photoaffinity labelling of creatine kinase with 2-azido- and 8-azidoadenosine triphosphate: identification of two peptides from the ATP-binding domain, Biochemistry 33, 11 935-11 941.
57. Pradel, L. A. & Kassab, R. (1968) Site actif des ATP: guanidine phosphotransférases. II. Mise en évidence de résidus histidine essentiels au moyen du pyrocarbonate d'élhyle, Biophys. Biochim. Acta 167, 317-325.
58. Price, N. C., Murray, S. & Milner-White, E. J. (1981) The effect of limited proteolysis on rabbit muscle creatine kinase, Biochem. J. 199, 239-244.
59. Quémeneur, E., Eichenberger, D., Goldschmidt, D., Vial, C., Beauregard, G. & Potier, M. (1988) The radiation inactivation method provides evidence that membrane-bound mitochondrial creatine kinase is an oligomer, Biochem. Biophys. Res. Commun. 153, 1310-1314.
60. Raimbault, C., Couthon, F., Vial, C. & Buchet, R. (1995) Effects of pH and KCl on the conformations of creatine kinase from rabbit muscle: infrared, circular dichroic and fluorescence studies, Eur. J. Biochem. 234, 570-578.
61. Raimbault, C., Buchet, R. & Vial, C. (1996) Changes of creatine kinase secondary structure induced by the release of nucleotides from caged compounds. An infrared difference-spectroscopy study, Eur. J. Biochem. 240, 134-142.
62. Raimbault, C., Besson, F. & Buchet, R. (1997) Conformational changes of arginine kinase induced by photochemical release of nucleotides from caged nucleotides. An infrared difference-spectroscopy investigation, Eur. J. Biochem. 244, 343-351.
63. 13C)-ADP, Biochemistry 35, 7239-7246.
64. Reed, G. H. & Cohn, M. (1972) Structural changes induced by substrates and anions at the active site of creatine kinase, J. Biol. Chem. 247, 3073-3081.
65. Reed, G. H., Barlow, C. H. & Burns, R. A. Jr (1978) Investigations of anion binding sites in transition state analog complexes of creatine kinase by infrared spectroscopy, J. Biol. Chem. 253, 4153-4158.
66. Rosevear, P. R., Desmeules, P., Kenyon, G. L. & Mildvan, A. S. (1981) Nuclear magnetic resonance studies of the role of histidine residues at the active site of rabbit muscle creatine kinase, Biochemistry 20, 6155-6164.
67. Rotschild, K. J. (1992) FTIR difference spectroscopy of bacteriorhodopsin: toward a molecular model, J. Bioenerg. Biomembr. 24, 147-167.
68. Roustan, C., Kassab, R., Pradel, L. A. & Van Thoai, N. (1968) Interactions des ATP: guanidine phosphotransférases avec leurs substrats, étudiée par spectrométrie différentielle, Biochim. Biophys. Acta 167, 326-338.
69. Roustan, C., Brevet, A. & Pradel, L. A. (1973) Structural properties of the creatine kinase active site studied by chromophoric reagent labelling. Eur. J. Biochem. 39, 371-379.
70. Saks, V. A., Rosenshtraukh, L. V., Smirnov, V. N. & Chazov, E. I. (1978) Role of creatine phosphokinase in cellular function and metabolism, Can. J. Physiol. Pharmacol. 56, 691-706.
71. Schägger, H. & von Jagow, G. (1987) Tricine sodium dodecylsulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa, Anal. Biochem. 166, 368-379.
72. Schimerlik, M. I. & Cleland, W. W. (1973) Inhibition of creatine kinase by chromium nucleotides, J. Biol. Chem. 248, 8418-8423.
73. Schlegel, J., Wyss, M., Schürch, U., Schnyder, T., Quest, A., Wegmann, G., Eppenberger, H. M. & Wallimann, T. (1988) Mitochondrial creatine kinase from cardiac muscle and brain are two distinct isoenzymes but form octameric molecules, J. Biol. Chem. 263, 16963-16969.
74. Shimanouchi, T., Tsuboi, M. & Kyogoku, Y. (1964) Infrared spectra of nucleic acids and related compounds, Adv. Chem. Phys. 7, 435-496.
75. Siebert, F. (1995) Infrared spectroscopy applied to biochemical and biological problems, Methods Enzymol. 246, 501-526.
76. Strong, S. J. & Ellington, W. R. (1995) Isolation and sequence analysis of the gene for arginine kinase from the chelicerate arthropod, Limulus polyphemus: insights into catalytically important residue, Biochim. Biophys. Acta 1246, 197-200.
77. Surewicz, W. K. & Mantsch, H. H. (1988) New insight into protein secondary structure from resolution-enhanced infrared spectra, Biochim. Biophys. Acta 952, 115-130.
78. Surewicz, W. K., Manisch, H. H. & Chapman, D. (1993) Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment, Biochemistry 32, 389-394.
79. Susi, H. (1972) Infrared spectroscopy-conformations, Methods Enzymol. 26, 455-472.
80. Suzuki, T. & Furukohori, T. (1994) Evolution of phosphagen kinase. Primary structure of glycocyamine kinase and arginine kinase from invertebrates, J. Mol. Biol. 237, 353-357.
81. Travers, F. & Barman, T. E. (1980) Cryoenzymic studies on the transition-state analog complex creatine kinase · ADPMg · nitrate · creatine, Eur. J. Biochem. 110, 405-412.
82. Trouiller, A., Gerwert, K. & Dupont, Y. (1996) A time-resolved Fourier Transformed infrared difference spectroscopy study of the sarcoplasmic reticulum Ca2+ ATPase: kinetics of the high-affinity calcium binding at low temperature, Biophys. J. 71, 2970-2983.
83. Tsou, C. E. (1986) Locations of the active sites of some enzymes in limited and flexible molecular regions, Trends Biochem. Sci. 11, 427-429.
84. Tsou, C. L. (1995) Inactivation precedes overall molecular conformational changes during enzyme denaturation, Biochem. Biophys. Acta 1253, 151-162.
85. Uversky, V. N. (1993) Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule, Biochemistry 32, 13 288-13 298.
86. Vandest, P., Labbe, J.-P. & Kassab, R. (1980) Photoaffinity labeling of arginine kinase and creatine kinase with a γ-P-substituted arylazido analogue of ATP, Eur. J. Biochem. 104, 433-442.
87. 2O) solutions. I. Spectral parameters of amino acid residue absorption band, Biopolymers 30, 1243-1257.
88. Walker, J. W., Reid, G. P., McGray, J. A. & Trentham, D. R. (1988) Photolabile 1-(2-nitrophenyl)ethyl phosphate esters of adenine nucleotide analogues. Synthesis and mechanism of photolysis, J. Am. Chem. Soc. 110, 7170-7177.
89. Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K. & Eppenberger, H. M. (1992) Intracellular compartimentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the phosphocreatine circuit for cellular energy homeostasis, Biochem. J. 281, 21-40
90. Watts, D. C. (1973) Creatine kinase (adenosine 5′-triphosphate-creatine phosphotransferase), Enzymes 3, 383-455.
91. Williamson, J., Greene, J., Cherif, S. & Milner-White, E. J. (1977) Heterogeneity of rabbit muscle creatine kinase and limited proteolysis by proteinase K, Biochem. J. 167, 731-737.
92. Wong, P. T. T. & Armstrong, D. W. (1992) FTIR spectroscopic kinetic-analysis of alkaline phosphatase under hyperbaric manipulation, Biochim. Biophys. Acta 1159, 237-242.
93. Wyss, M., James, P., Schlegel, J. & Wallimann, T. (1993) Limited proleolysis of creatine kinase. Implications for three-dimensional structure and for conformational substates, Biochemistry 32, 10727-10735.
94. Zhou, H.-M. & Tsou, C.-L. (1985) An essential tryptophan residue for rabbit muscle creatine kinase, Biochim. Biophys. Acta 830, 59-63.
95. Zhou, H.-M. & Tsou, C.-L. (1987) The presence of reactive SH groups in the enzymatically active dicyano derivative of creatine kinase, Biochim. Biophys. Acta 911, 136-143.
96. Zhou, H.-M., Zhang, X.-H., Yin, Y. & Tsou, C.-L. (1993) Conformational changes at the active site of creatine kinase at low concentrations of guanidinium chloride, Biochem. J. 291, 103-107.