Redox-dependent stability, protonation, and reactivity of cysteine-bound heme proteins

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 3, 2014, Pages

  Zhong, Fangfang ^a   Lisi, George P ^a   Collins, Daniel P ^b   Dawson, John H ^b   Pletneva, Ekaterina V ^a  

^a Lamont Doherty Earth Observatory   (United States)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Electron transfer; Folding; Metalloenzyme

Indexed keywords

CYSTEINE; CYTOCHROME C; HEMOPROTEIN; PEROXIDASE; THIOL;

ARTICLE; ENTROPY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PH; PRIORITY JOURNAL; PROTEIN STABILITY; PROTON TRANSPORT; THERMODYNAMICS;

ELECTRON TRANSFER; FOLDING; METALLOENZYME;

ANIMALS; CYSTEINE; CYTOCHROMES C; ELECTRON TRANSPORT; FUNGAL PROTEINS; HEME; HEMEPROTEINS; HORSES; HYDROGEN-ION CONCENTRATION; IRON; KINETICS; LIGANDS; MODELS, MOLECULAR; MUTATION; MYOCARDIUM; OXIDATION-REDUCTION; PEROXIDASES; SPECTROPHOTOMETRY; SULFHYDRYL COMPOUNDS; THERMODYNAMICS;

EID: 84892935332     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1317173111     Document Type: Article

References (69)

1. Sono M, Roach MP, Coulter ED, Dawson JH (1996) Heme-containing oxygenases. Chem Rev 96(7):2841-2888.
2. Julsing MK, Cornelissen S, Bühler B, Schmid A (2008) Heme-iron oxygenases: Powerful industrial biocatalysts? Curr Opin Chem Biol 12(2):177-186.
3. Sevrioukova IF, Poulos TL (2013) Understanding the mechanism of cytochrome P450 3A4: Recent advances and remaining problems. Dalton Trans 42(9):3116-3126.
4. Hannibal L, Somasundaram R, Tejero J, Wilson A, Stuehr DJ (2011) Influence of hemethiolate in shaping the catalytic properties of a bacterial nitric-oxide synthase. J Biol Chem 286(45):39224-39235.
5. Groves JT, Wang CC-Y (2000) Nitric oxide synthase: Models and mechanisms. Curr Opin Chem Biol 4(6):687-695.
6. Su Y, et al. (2013) Comparative study of enzyme activity and heme reactivity in Drosophila melanogaster and Homo sapiens cystathionine β-synthases. Biochemistry 52(4):741-751.
7. Hofrichter M, Ullrich R (2006) Heme-thiolate haloperoxidases: Versatile biocatalysts with biotechnological and environmental significance. Appl Microbiol Biotechnol 71(3):276-288.
8. Cheesman MR, Little PJ, Berks BC (2001) Novel heme ligation in a c-type cytochrome involved in thiosulfate oxidation: EPR and MCD of SoxAX from Rhodovulum sulfidophilum. Biochemistry 40(35):10562-10569.
9. Shelver D, et al. (1999) Identification of two important heme site residues (cysteine 75 and histidine 77) in CooA, the CO-sensing transcription factor of Rhodospirillum rubrum. Biochemistry 38(9):2669-2678.
10. Dioum EM, et al. (2002) NPAS2: A gas-responsive transcription factor. Science 298(5602):2385-2387.
11. Sabat J, Stuehr DJ, Yeh SR, Rousseau DL (2009) Characterization of the proximal ligand in the P420 form of inducible nitric oxide synthase. J Am Chem Soc 131(34):12186-12192.
12. Perera R, et al. (2003) Neutral thiol as a proximal ligand to ferrous heme iron: Implications for heme proteins that lose cysteine thiolate ligation on reduction. Proc Natl Acad Sci USA 100(7):3641-3646.
13. Smulevich G, Bjerrum MJ, Gray HB, Spiro TG (1994) Resonance raman spectra and the active site structure of semisynthetic Met80Cys horse heart cytochrome c. Inorg Chem 33(21):4629-4634.
14. Collman JP, Sorrell TN, Hodgson KO, Kulshrestha AK, Strouse CE (1977) Molecular dynamics in the solid state. A dynamic model of the low-spin iron (III) to high-spin iron (III) transformation in P450 enzymes. J Am Chem Soc 99(15):5180-5181.
15. Sono M, Andersson LA, Dawson JH (1982) Sulfur donor ligand binding to ferric cytochrome P-450-CAM and myoglobin. Ultraviolet-visible absorption, magnetic circular dichroism, and electron paramagnetic resonance spectroscopic investigation of the complexes. J Biol Chem 257(14):8308-8320.
16. Sono M, Dawson JH, Hager LP (1984) The generation of a hyperporphyrin spectrum upon thiol binding to ferric chloroperoxidase. Further evidence of endogenous thiolate ligation to the ferric enzyme. J Biol Chem 259(21):13209-13216.
17. McGuire DG, Khan MA, Ashby MT (2002) Discontinuum between a thiolate and a thiol ligand. Inorg Chem 41(8):2202-2208.
18. Bayer E, Hill H A O, Roder A, Williams R J P (1969) The interaction between haem-iron and thiols. J Chem Soc D 3:109.
19. Sadeque A J M, Shimizu T, Hatano M (1987) Thiol-coordinated heme octapeptides of cytochrome c; model compounds of cytochrome P-450. Inorg Chim Acta 135(2):109-113.
20. Dawson JH, et al. (1978) Magnetic circular dichroism of purified forms of rabbit liver cytochromes P-450 and P-420. Biochemistry 17(1):33-42.
21. Raphael AL, Gray HB (1991) Semisynthesis of axial-ligand (position 80) mutants of cytochrome c. J Am Chem Soc 113(3):1038-1040.
22. Pollock W B R, Rosell FI, Twitchett MB, Dumont ME, Mauk AG (1998) Bacterial expression of a mitochondrial cytochrome c. Trimethylation of Lys72 in yeast iso-1 cytochrome c and the alkaline conformational transition. Biochemistry 37(17):6124-6131.
23. McKnight J, Cheesman MR, Thomson AJ, Miles JS, Munro AW (1993) Identification of charge-transfer transitions in the optical spectrum of low-spin ferric cytochrome P-450 Bacillus megaterium. Eur J Biochem 213(2):683-687.
24. Blanke SR, et al. (1996) Probing the heme iron coordination structure of alkaline chloroperoxidase. Biochemistry 35(46):14537-14543.
25. Reynolds MF, et al. (1998) EPR and electronic absorption spectroscopies of the CO-sensing CooA protein reveal a cysteine-ligated low-spin ferric heme. J Am Chem Soc 120(35):9080-9081.
26. Dawson JH, Andersson LA, Sono M (1983) The diverse spectroscopic properties of ferrous cytochrome P-450-CAM ligand complexes. J Biol Chem 258(22):13637-13645.
27. Cohen DS, Pielak GJ (1995) Entropic stabilization of cytochrome c upon reduction. J Am Chem Soc 117(6):1675-1677.
28. Liggins JR, Lo TP, Brayer GD, Nall BT (1999) Thermal stability of hydrophobic heme pocket variants of oxidized cytochrome c. Protein Sci 8(12):2645-2654.
29. Betz SF, Pielak GJ (1992) Introduction of a disulfide bond into cytochrome c stabilizes a compact denatured state. Biochemistry 31(49):12337-12344.
30. Herrmann LM, Bowler BE (1997) Thermal denaturation of iso-1-cytochrome c variants: Comparison with solvent denaturation. Protein Sci 6(3):657-665.
31. Godbole S, Hammack B, Bowler BE (2000) Measuring denatured state energetics: Deviations from random coil behavior and implications for the folding of iso-1-cytochrome c. J Mol Biol 296(1):217-228.
32. Dunford AJ, et al. (2007) Rapid P450 heme iron reduction by laser photoexcitation of Mycobacterium tuberculosis CYP121 and CYP51B1. Analysis of CO complexation reactions and reversibility of the P450/P420 equilibrium. J Biol Chem 282(34):24816-24824.
33. Rosell FI, Ferrer JC, Mauk AG (1998) Proton-linked protein conformational switching: Definition of the alkaline conformational transition of yeast Iso-1-ferricytochrome c. J Am Chem Soc 120(44):11234-11245.
34. Cherney MM, Bowler BE (2011) Protein dynamics and function: Making new strides with an old warhorse, the alkaline conformational transition of cytochrome c. Coord Chem Rev 255(7-8):664-677.
35. Silkstone G, Stanway G, Brzezinski P, Wilson MT (2002) Production and characterisation of Met80X mutants of yeast iso-1-cytochrome c: Spectral, photochemical and binding studies on the ferrous derivatives. Biophys Chem 98(1-2):65-77.
36. Wilson MT, Brunori M, Rotilio GC, Antonini E (1973) Properties of modified cytochromes. II. Ligand binding to reduced carboxymethyl cytochrome c. J Biol Chem 248(23):8162-8169.
37. Tezcan FA, Winkler JR, Gray HB (1998) Effects of ligation and folding on reduction potentials of heme proteins. J Am Chem Soc 120(51):13383-13388.
38. Wang JS, Tsai AL, Heldt J, Palmer G, Van Wart HE (1992) Temperature- and pH-dependent changes in the coordination sphere of the heme c group in the model peroxidase N alpha-acetyl microperoxidase-8. J Biol Chem 267(22):15310-15318.
39. Marques HM, Rousseau A (1996) Reactions of ferric porphyrins and thiols. The reaction of the haem octapeptide, N-acetylmicroperoxidase-8, with cysteine. Inorg Chim Acta 248(1):115-119.
40. Lu Y, Casimiro DR, Bren KL, Richards JH, Gray HB (1993) Structurally engineered cytochromes with novel ligand-binding properties. Expression of S. cerevisiae Met80Ala iso-1-cytochrome c. Proc Natl Acad Sci USA 90(24):11456-11459.
41. Danehy JP, Parameswaran KN (1968) Acidic dissociation constants of thiols. J Chem Engineer Data 13(3):386-389.
42. Matsubara T, Ford PC (1976) Some applications of cyclic voltammetry to the reactions and properties of ruthenium ammine complexes. Reduction potentials and rate studies. Inorg Chem 15(5):1107-1110.
43. Taniguchi VT, Sailasuta-Scott N, Anson FC, Gray HB (1980) Thermodynamics of metalloprotein electron transfer reactions. Pure Appl Chem 52(10):2275-2281.
44. Moore GR, Pettigrew GW (1990) Cytochromes c: Evolutionary, Structural, and Physicochemical Aspects (Springer, New York).
45. Silkstone GG, Cooper CE, Svistunenko D, Wilson MT (2005) EPR and optical spectroscopic studies of Met80X mutants of yeast ferricytochrome c. Models for intermediates in the alkaline transition. J Am Chem Soc 127(1):92-99.
46. Latimer WM (1952) The Oxidation States of the Elements and Their Potentials in Aqueous Solution (Prentice-Hall, New York).
47. Vincent KA, et al. (2003) Instantaneous, stoichiometric generation of powerfully reducing states of protein active sites using Eu (II) and polyaminocarboxylate ligands. Chem Commun (Camb) (20): 2590-2591.
48. Creutz C, Sutin N (1973) Reduction of ferricytochrome c by dithionite ion: Electron transfer by parallel adjacent and remote pathways. Proc Natl Acad Sci USA 70(6):1701-1703.
49. De Weerd K, Grigoryants V, Sun Y, Fetrow JS, Scholes CP (2001) EPR-detected folding kinetics of externally located cysteine-directed spin-labeled mutants of iso-1-cytochrome c. Biochemistry 40(51):15846-15855.
50. Wallace CJ, Clark-Lewis I (1992) Functional role of heme ligation in cytochrome c. Effects of replacement of methionine 80 with natural and non-natural residues by semisynthesis. J Biol Chem 267(6):3852-3861.
51. Hanske J, et al. (2012) Conformational properties of cardiolipin-bound cytochrome c. Proc Natl Acad Sci USA 109(1):125-130.
52. Wallace CJ, et al. (1989) Substitutions engineered by chemical synthesis at three conserved sites in mitochondrial cytochrome c. Thermodynamic and functional consequences. J Biol Chem 264(26):15199-15209.
53. Berghuis AM, et al. (1994) The role of a conserved internal water molecule and its associated hydrogen bond network in cytochrome c. J Mol Biol 236(3):786-799.
54. Berghuis AM, Brayer GD (1992) Oxidation state-dependent conformational changes in cytochrome c. J Mol Biol 223(4):959-976.
55. ten Kortenaar PB, Adams PJ, Tesser GI (1985) Semisynthesis of horse heart cytochrome c analogues from two or three fragments. Proc Natl Acad Sci USA 82(24):8279-8283.
56. Bren KL, Gray HB, Banci L, Bertini I, Turano P (1995) Paramagnetic 1H NMR spectroscopy of the cyanide derivative of Met80Ala-iso-1-cytochrome c. J Am Chem Soc 117(31):8067-8073.
57. Assfalg M, et al. (2003) Structural model for an alkaline form of ferricytochrome C. J Am Chem Soc 125(10):2913-2922.
58. Pascher T, Chesick JP, Winkler JR, Gray HB (1996) Protein folding triggered by electron transfer. Science 271(5255):1558-1560.
59. Nakajima H, et al. (2001) Redox properties and coordination structure of the heme in the co-sensing transcriptional activator CooA. J Biol Chem 276(10):7055-7061.
60. Shimizu T (2012) Binding of cysteine thiolate to the Fe (III) heme complex is critical for the function of heme sensor proteins. J Inorg Biochem 108(1):171-177.
61. Pazicni S, et al. (2005) The heme of cystathionine p-synthase likely undergoes a thermally induced redox-mediated ligand switch. Biochemistry 44(51):16785-16795.
62. Galinato MG, Spolitak T, Ballou DP, Lehnert N (2011) Elucidating the role of the proximal cysteine hydrogen-bonding network in ferric cytochrome P450cam and corresponding mutants using magnetic circular dichroism spectroscopy. Biochemistry 50(6):1053-1069.
63. Ying T, et al. (2009) Evolutionary alkaline transition in human cytochrome c. J Bioenerg Biomembr 41(3):251-257.
64. Schejter A, George P (1965) Production of a "cytochrome c" with myoglobin-like properties by alkylating the cyanide complex with bromoacetate. Nature 206(989):1150-1151.
65. Low DW, Winkler JR, Gray HB (1996) Photoinduced oxidation of microperoxidase-8-generation of ferryl and cation-radical porphyrins. J Am Chem Soc 118(1):117-120.
66. Pond AE, Roach MP, Thomas MR, Boxer SG, Dawson JH (2000) The H93G myoglobin cavity mutant as a versatile template for modeling heme proteins: Ferrous, ferric, and ferryl mixed-ligand complexes with imidazole in the cavity. Inorg Chem 39(26):6061-6066.
67. Berry EA, Trumpower BL (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal Biochem 161(1):1-15.
68. Pandurangachar M, et al. (2010) Electrochemical investigations of potassium ferricyanide and dopamine by 1-butyl-4-methylpyridinium tetrafluoro borate modified carbon paste electrode: A cyclic voltammetric study. Int J Electrochem Sci 5(8):1187-1202.
69. Louro RO, Catarino T, Le Gall J, Turner DL, Xavier AV (2001) Cooperativity between electrons and protons in a monomeric cytochrome c (3): The importance of mechanochemical coupling for energy transduction. ChemBioChem 2(11):831-837.