Photo-induced unfolding and inactivation of bovine carbonic anhydrase in the presence of a photoresponsive surfactant

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 1, 2010, Pages 106-114

  Mirarefi, Panteha ^a   Lee Jr , C Ted ^a  

^a University of Southern California ^*  (United States)

Author keywords

Carbonic anhydrase; Enzyme activity; Photoresponsive surfactant; Protein aggregation; Protein unfolding; Small angle neutron scattering

Indexed keywords

CARBONATE DEHYDRATASE; SURFACTANT;

ADDITION REACTION; ARTICLE; CIS ISOMER; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COW; ENZYME ACTIVITY; ENZYME INACTIVATION; FLUORESCENCE SPECTROSCOPY; HYDROPHILICITY; HYDROPHOBICITY; ILLUMINATION; INFRARED SPECTROSCOPY; ISOMERIZATION; LIGHT; LIGHT SCATTERING; MOLECULAR INTERACTION; NEUTRON SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; TRANS ISOMER; ULTRAVIOLET RADIATION;

ANIMALS; CARBONIC ANHYDRASES; CATTLE; NEUTRON DIFFRACTION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; QUATERNARY AMMONIUM COMPOUNDS; SCATTERING, RADIATION; SCATTERING, SMALL ANGLE; SURFACE-ACTIVE AGENTS;

BOVINAE;

EID: 71649115177     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2009.09.007     Document Type: Article

References (75)

1. Wang S.C., and Lee Jr. C.T. Enhanced enzymatic activity through photoreversible conformational changes. Biochemistry 46 (2007) 14557-14566
2. Lima C.F., Nome F., and Zanette D. First evidence of poly(ethyleneoxide)-mixed sodium dodecyl sulfate/sodium decyl phosphate complexes. J. Colloid Interface Sci. 189 (1997) 174-176 (3)
3. Lee Jr. C.T., Smith K.A., and Hatton T.A. Photocontrol of protein folding: the interaction of photosensitive surfactant with bovine serum albumin. Biochemistry 44 (2005) 524-536
4. Hamill A.C., Wang S.C., and Lee Jr. C.T. Probing lysozyme conformation with light reveals a new folding intermediate. Biochemistry 44 (2005) 15139-15149
5. Hamill A.C., Wang S.C., and Lee Jr. C.T. Solution structure of an amyloid-forming during photo-initiated hexamer-dodecamer transitions revealed through small-angle neutron scattering. Biochemistry 46 (2007) 7694-7705
6. Wang S.C., and Lee Jr. C.T. Protein secondary structure controlled with light and photoresponsive surfactants. J. Phys. Chem., B 110 (2006) 16117-16123
7. Lee Jr. C.T., Smith K.A., and Hatton T.A. Photoreversible viscosity changes and gelation in mixtures of hydrophobically modified polyelectrolytes and photosensitive surfactants. Macromolecules 37 (2004) 5397-5405
8. Verpoorte J.A., Mehta S., and Edsall J.T. Esterase activities of human carbonic anhydrase B and C. J. Biol. Chem. 242 (1967) 4221-4229
9. Thorslund A., and Lindskog S. Studies of the esterase activity and the anion inhibition of Bovine zinc and cobalt carbonic anhydrase. Eur. J. Biochem. 3 (1967) 117-123
10. Ohta S., Alam M.T., Arakawa H., and Ikai A. Origin of mechanical strength of bovine carbonic anhydrase studied by molecular dynamics simulation. Biophys. J. 87 (2004) 4007-4020
11. Stams T., and Christianson D.W. X-ray crystallographic studies of mammalian carbonic anhydrase isozymes. In: Chegwidden W.R., Carter N.D., and Edwards Y.H. (Eds). The Carbonic Anhydrases, New Horizons (2000), Birkhauser 159-174
12. Hakansson K., Carlsson M., Svensson L.A., and Liljas A. Structure of native and apo carbonic anhydrase II and structure of some of its anion-ligand complexes. J. Mol. Biol. 227 (1992) 1192-1204
13. Eriksson A.E., and Liljas A. X-ray crystallographic studies of mammalian carbonic snhydrase isozymes I, II, and III. In: Dodgson S.J., Tashian R.E., Gros G., and Carter N.D. (Eds). The Carbonic Anhydrase, Cellular Physiology and Molecular Genetics (1991), Plenum Press, New York 33-48
14. Kanna K.K., Notstrand B., Fridborg K., Lovegren S., Ohlsson A., and Petef M. Crystal structure of human erythrocyte carbonic anhydrase B. Three-dimensional structure at a nominal 2.2-Å resolution. Proc. Nat. Acad. Sci. 72 (1975) 51-55
15. Aronsson G., Martensson L.G., Carlsson U., and Jonsson B.H. Folding and stability of the N-terminus of human carbonic anhydrase II. Biochemistry 34 (1995) 2153-2162
16. Eriksson A.E., Jones T.A., and Liljas A. A refined structure of human carbonic anhydrase II at 2.0 Å resolution. Proteins: Struct. Func. Genet. 4 (1988) 274-282
17. Alam M.T., Yamada T., Carlsson U., and Ikai A. The importance of being knotted: effects of C-terminal knot structure on enzymatic and mechanical properties of bovine carbonic anhydrase II. FEBS Lett. 519 (2002) 35-42
18. Clenland J.F., and Wang D.I.C. Refolding and aggregation of bovine carbonic anhydrase B: quasi-elastic light scattering analysis. Biochemistry 29 (1990) 11072-11078
19. Clenland J.L., and Wang D.I.C. Equilibrium association of a molten globule intermediate in the refolding of bovine carbonic anhydrase. In: Georgiou G., and Bernardez-Clark E.D. (Eds). Protein Refolding (1991), American Chemical Society, Washington, D. C 169-179
20. Silverman D.N., and Lindskog S. The catalytic mechanism of carbonic anhydrase: implications of a rate-limiting proteolysis of water. Acc. Chem. Res. 21 (1988) 30-36
21. An H., Tu C., Duda D., Montanez-Clemente I., Math K., Laipis P.J., McKenna R., and Silverman D.N. Chemical rescue in catalysis by human carbonic anhydrase II and III. Biochemistry 41 (2002) 3235-3242
22. Eriksson A.E., and Liljas A. X-ray crystallographic studies of mammalian carbonic anhydrase isozymes I, II, and III. In: Dodgson S.J., Tashian R.E., Gros G., and Carter N.D. (Eds). The Carbonic Anhydrase, Cellular Physiology and Molecular Genetics (1991), Plenum Press, New York 42-48
23. Lindskog S., and Silverman D.N. The catalytic mechanism of mammalian carbonic anhydrases. In: Chegwidden W.R., Carter N.D., and Edwards Y.H. (Eds). The Carbonic Anhydrase, New Horizons (2000), Birkhauser 175-195
24. Tripp B.C., Smith K., and Ferry J.G. Carbonic anhydrase: new insight for an ancient enzyme. J. Biol. Chem. 276 (2001) 48615-48618
25. Tu C.K., Silverman D.N., Forsman C., Jonsson B.H., and Lindskog S. Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant. Biochemistry 28 (1989) 7913-7918
26. Steiner H., Jansson B.H., and Lindskog S. The catalytic mechanism of carbonic anhydrase hydrogen-isotope effects on the kinetic parameters of the human C isoenzyme. Eur. J. Biochem. 59 (1975) 253-259
27. Taoka S., Tu C., Kistler K.A., and Silverman D.N. Comparison of intra- and intermolecular proton transfer in human carbonic anhydrase II. J. Biol. Chem. 269 (1994) 17988-17992
28. Silverman D.N., and Vincent S.H. Proton transfer in the catalytic mechanism of carbonic anhydrase. CRC Crit. Rev. Biochem. 14 (1983) 207-255
29. Shang T., Smith K.A., and Hatton T.A. Photoresponsive surfactants exhibiting unusually large, reversible surface tension changes under varying illumination conditions. Langmuir 19 (2003) 10764-10773
30. Hayashita T., Kurosawas T., Miyata T., Tanaka K., and Igawa M. Effect of structural variation within cationic azo-surfactant upon photoresponsive function in aqueous solution. Colloid Polym. Sci. 272 (1994) 1611-1619
31. Wilbur K., and Anderson N. Electrometric and colorimetric determination of carbonic anhydrase. J. Biol. Chem. 176 (1948) 147-154
32. Nyman P.O., and Lindskog S. Acid composition of various forms of bovine and human Erythrocyte carbonic anhydrase. Biochem. Biophys. Acta 85 (1964) 141-151
33. Harned H.S., and Davis R. The ionization constant of carbonic acid in water and the solubility of carbon dioxide in water and aqueous salt solutions from 0 to 50 °C. Chem. Soc. 65 (1943) 2030-2037
34. Glinka C.J., Barker J.G., Hammouda B., Krueger S., Moyer J.J., and Ort W.J. The 30 m small-angle neutron scattering instrument at the National Institute of Standards and Technology. Appl. Crystallogr. 31 (1998) 430-445
35. Svergun D.I., Petoukhov M.V., and Koch M.H.J. Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80 (2001) 2946-2953
36. Durchschlag H., Fochler C., Feser B., Hausmann S., Seroneit T., Swientek M., Swoboda E., Winklmair A., Wlcek C., and Zipper P. Effects of X- and UV-irradiation on proteins. Radiat. Phys. Chem. 47 (1996) 501-505
37. Shugar D. Measurement of lysozyme activity and the ultraviolet inactivation of lysozyme. Biochim. Biophys. Acta 8 (1952) 302-309
38. Durchschlag H., Hefferle T., and Zipper P. Comparative investigations of the effects of X- and UV-irradiation on lysozyme in the absence or presence of additives. Radiat. Phys. Chem. 67 (2003) 479-486
39. Zhou H.M., Zhang X.H., Yin Y., and Tsou C.L. Conformational changes at the active site of creatine kinase at low concentrations of guanidinium chloride. Biochem. J. 291 (1993) 103-107
40. Wei X., Ding S., Jiang Y., Zeng X.G., and Zhou H.M. Conformational changes and inactivation of bovine carbonic anhydrase II in 2,2,2-trifluoroethanol solutions. Biochemistry (Moscow) 71 (2006) S77-S82
41. Safarian S., Saffarzadeh M., Zargar S.J., and Moosavi-Movahedi A.A. Molten globule-like state of bovine carbonic anhydrase in the presence of acetonitrile. J. Biochem. 139 (2006) 1025-1033
42. Qian M., Tu C., Earnhardt N., Laipis P.J., and Silverman D.N. Glutamate and aspartate as proton shuttles in mutants of carbonic anhydrase. Biochemistry 36 (1997) 15758-15764
43. Silverman D.N., and Mckenna R. Solvent-mediated proton transfer in catalysis by carbonic anhydrase. Acc. Chem. Res. 40 (2007) 669-675
44. Lee H.W., Yang W., Ye Y., Liu Z.R., Glushka J., and Yang J.J. Isolated EF-loop III of calmodulin in a scaffold protein remains unpaired in solution using pulsed-field-gradient NMR spectroscopy. Biochim. Biophys. Acta 1598 (2002) 80-87
45. Uversky V.N., and Fink A.L. The chicken-egg scenario of protein folding revisited. FEBS Lett. 515 (2002) 79-83
46. Jennings P.A., and Wright P.E. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 262 (1993) 892-896
47. Jacob M.D., and Fox R.O. Staphylococcal nuclease folding intermediate characterized by hydrogen exchange and NMR spectroscopy. Proc. Nat. Acad. Sci. U. S. A. 91 (1994) 449-453
48. Eliezer D., Yao J., Dyson H.J., and Wright P.E. Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding. Nat. Struct. Biol. 5 (1998) 148-155
49. Bergasa-Caceres F., and Rabitz H.A. Two-state folding kinetics of small proteins in the sequential collapse model: dependence of the folding rate on contact order and temperature. J. Phys. Chem., B 107 (2003) 12874-12877
50. Kuwajima K., Nitta K., Yoneyama M., and Sugai S. Three-state denaturation of a-lactalbumin by guanidine hydrochloride. J. Mol. Biol. 106 (1976) 359-373
51. Spolar R.S., Ha J.H., and Record Jr. M.T. Hydrophobic effect in protein folding and other noncovalent processes involving proteins. Proc. Nat. Acad. Sci. U. S. A. 86 (1989) 8382-8385
52. Privalov P.L., and Makhatadze G.I. Heat capacity of proteins: II. Partial molar heat capacity of the unfolding polypeptide chain of proteins: protein unfolding effects. J. Mol. Biol. 213 (1990) 385-391
53. Damaschun G., Gernat C., Damaschun H., Bychkova V.E., and Ptitsyn O.B. Comparison of intramolecular packing of a protein in native and molten globule states. Int. J. Biol. Macromol. 8 (1986) 226-230
54. Baum J., Dobson C.M., Evans P.A., and Hanley C. Characterization of a partly folded protein by NMR methods: studies on the molten globule state of guinea pig a-lactalbumin. Biochemistry 28 (1989) 7-13
55. Bu Z., Neumann D.A., Lee S.H., Brown C.M., Engelman D.M., and Han C.C. A View of dynamics changes in the molten globule-native folding step by quasielastic neutron scattering. J. Mol. Biol. 301 (2000) 525-536
56. Receveur V., Calmettes P., Smith J.C., Desmadril M., Coddens G., and Durand D. Picosecond dynamical changes on denaturation of yeast phosphoglycerate kinase revealed by quasielastic neutron scattering. Proteins Struct. Funct. Genet. 28 (1997) 380-387
57. 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
58. Rodionova N.A., Semisotnov G.V., Kutyshenko V.P., Uversky V.N., Bolotina I.A., Bychkova V.E., and Ptitsyn O.B. Two-stage equilibrium unfolding of carbonic anhydrase B by strong denaturants. Mol. Biol. (Mosk.) 23 (1989) 683-692
59. Uversky V.N., and Ptitsyn O.B. Further evidence on the equilibrium "pre-molten globule state": four-state guanidinium chloride-induced unfolding of carbonic anhydrase B at low temperature. J. Mol. Biol. 255 (1996) 215-228
60. Wong K.P., and Tanford C. Denaturation of bovine carbonic anhydrase B by guanidine hydrochloride. Process involving separable sequential conformational transitions. J. Biol. Chem. 248 (1973) 8518-8523
61. Greenspan P., and Fowler S.D. Spectrofluorometric studies of the lipid probe, Nile red. J. Lipid Res. 26 (1985) 781-789
62. Bushmarina N.A., Kuznetsova I.M., Biktashev A.G., Turoverov K.K., and Uversky V.N. Partially folded conformations in the folding pathway of bovine carbonic anhydrase II: a fluorescence spectroscopic analysis. ChemBioChem 2 (2001) 813-821
63. Gudiksen K.L., Gitlin I., Yang J., Urbach A.R., Moustakas D.T., and Whitesides G.M. Eliminating positively charged lysine epsilon-NH3+ groups on the surface of carbonic anhydrase has no significant influence on its folding from sodium dodecyl sulfate. J. Am. Chem. Soc. 127 (2005) 4707-4714
64. Fujisawa T., Ueka Y., and Kataoka M. X-ray scattering from a troponin C solution and its interpretation with a dumbbell-shaped-molecule model. J. Appl. Crystallogr. 20 (1987) 349-355
65. Tranier S., Mortier-Barriere I., Ilbert M., Birck C., Iobbi-Nivol C., Mejean V., and Samama J.P. Characterization and multiple molecular forms of TorD from Shewanella massila, the putative chaperon of the molybdoenzyme TorA. Protein Sci. 11 (2002) 2148-2157
66. Achter E.K., and Swan L.D.A. Conformation of lysozyme and a-lactalbumin in solution. Biochemistry 10 (1971) 2976-2978
67. Guinier A., and Fournet G. Small-Angle Scattering of X-rays (1995), John Willey & Sons, Inc., New York
68. Semisotnov G.V., Kihara H., Kotova N.V., Kimura K., Amemiya Y., Wakabayashi K., Serdyuk I.N., Timchenko A.A., Chiba K., Nikaido K., Ikura T., and Kuwajima K. Protein globularization during folding. A study by synchrotron small-angle X-ray scattering. J. Mol. Biol. 262 (1996) 559-574
69. Dolgikh D.A., Kolomiets A.P., Bolotina I.A., and Ptitsyn O.B. 'Molten-globule' state accumulates in carbonic anhydrase folding. FEBS Lett. 165 (1984) 88-92
70. Feigin L.A., and Svergun D.I. In: Taylor G.W. (Ed). Structure Analysis by Small-angle X-ray and Neutron Scattering (1987), Plenum Press, New York 1-335
71. Glatter O. A new method for the evaluation of small angle scattering data. J. Appl. Crystallogr. 10 (1977) 415-421
72. Montich G.G. Partly folded states of bovine carbonic anhydrase interact with zwitterionic and anionic lipid membranes. Biochim. Biophys. Acta 1468 (2000) 115-126
73. Barth A. Infrared spectroscopy of proteins. Biochim. Biophys. Acta 1767 (2007) 1073-1101
74. Haris P.I., and Chapman D. The conformational analysis of peptides using fourier transform IR spectroscopy. Biopolymers 37 (1995) 251-263
75. Jackson M., Haris P.I., and Chapman D. Fourier transform infrared spectroscopic studies of calcium-binding proteins. Biochemistry 30 (1991) 9681-9686