Measurement of histidine pKa values and tautomer populations in invisible protein states

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

Volumn 111, Issue 17, 2014, Pages

  Hansen, Alexandar L ^a   Kay, Lewis E ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

CEST; Chemical exchange; Conformationally excited protein states; Im7 protein folding intermediate; PH stability

Indexed keywords

HISTIDINE; IMIDAZOLE; IMIDAZOLE DERIVATIVE; PROTEIN;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CATALYSIS; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HYDROGEN BOND; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PKA; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTON NUCLEAR MAGNETIC RESONANCE; STATIC ELECTRICITY; TAUTOMER; TAUTOMERIZATION; CEST; CHEMICAL EXCHANGE; CHEMISTRY; CONFORMATIONALLY EXCITED PROTEIN STATES; IM7 PROTEIN-FOLDING INTERMEDIATE; PH; PH STABILITY; PROTEIN DATABASE; REPRODUCIBILITY; STEREOISOMERISM;

CEST; CHEMICAL EXCHANGE; CONFORMATIONALLY EXCITED PROTEIN STATES; IM7 PROTEIN-FOLDING INTERMEDIATE; PH STABILITY;

DATABASES, PROTEIN; HISTIDINE; HYDROGEN-ION CONCENTRATION; IMIDAZOLES; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEINS; REPRODUCIBILITY OF RESULTS; STEREOISOMERISM;

EID: 84899622622     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400577111     Document Type: Article

References (84)

1. Perutz MF (1978) Electrostatic effects in proteins. Science 201(4362):1187-1191.
2. Warshel A (1981) Electrostatic basis of structure-function correlation in proteins. Acc Chem Res 14(9):284-290.
3. Grimsley GR, Scholtz JM, Pace CN (2009) A summary of the measured pK values of the ionizable groups in folded proteins. Protein Sci 18(1):247-251.
4. Pace CN, Grimsley GR, Scholtz JM (2009) Protein ionizable groups: pK values and their contribution to protein stability and solubility. J Biol Chem 284(20):13285-13289.
5. Hedstrom L (2002) Serine protease mechanism and specificity. Chem Rev 102(12): 4501-4524.
6. Shimba N, et al. (2003) Quantitative identification of the protonation state of histidines in vitro and in vivo. Biochemistry 42(30):9227-9234.
7. Pelton JG, Torchia DA, Meadow ND, Roseman S (1993) Tautomeric states of the activesite histidines of phosphorylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci 2(4):543-558.
8. Puttick J, Baker EN, Delbaere LTJ (2008) Histidine phosphorylation in biological systems. Biochim Biophys Acta 1784(1):100-105.
9. Edgcomb SP, Murphy KP (2002) Variability in the pKa of histidine side-chains correlates with burial within proteins. Proteins 49(1):1-6.
10. Markley JL (1975) Observation of histidine residues in proteins by nuclear magnetic resonance spectroscopy. Acc Chem Res 8(2):70-80.
11. Bachovchin WW (2001) Review: Contributions of NMR spectroscopy to the study of hydrogen bonds in serine protease active sites. Magn Reson Chem 39:S199-S213.
12. Mandel M (1964) The effect of temperature on the proton magnetic resonance spectra of ribonuclease, oxidized ribonuclease, and lysozyme. Proc Natl Acad Sci USA 52(3):736-741.
13. Mandel M (1965) Proton magnetic resonance spectra of some proteins: I. Ribonuclease, oxidized ribonuclease, lysozyme, and cytochrome C. J Biol Chem 240:1586-1592.
14. Meadows DH, Markley JL, Cohen JS, Jardetzky O (1967) Nuclear magnetic resonance studies of the structure and binding sites of enzymes. I. Histidine residues. Proc Natl Acad Sci USA 58(4):1307-1313.
15. Alei M, Morgan LO, Wageman WE, Whaley TW (1980) The pH dependence of nitrogen-15 NMR shifts and coupling constants in aqueous imidazole and 1-methylimidazole. Comments on estimation of tautomeric equilibrium constants for aqueous histidine. J Am Chem Soc 102(9):2881-2887.
16. Farr-Jones S, Wong WYL, Gutheil WG, Bachovchin WW (1993) Direct observation of the tautomeric forms of histidine in nitrogen-15 NMR spectra at low temperatures. Comments on intramolecular hydrogen bonding and on tautomeric equilibrium constants. J Am Chem Soc 115(15):6813-6819.
17. Tan YJ, Oliveberg M, Davis B, Fersht AR (1995) Perturbed pKA-values in the denatured states of proteins. J Mol Biol 254(5):980-992.
18. Tollinger M, Crowhurst KA, Kay LE, Forman-Kay JD (2003) Site-specific contributions to the pH dependence of protein stability. Proc Natl Acad Sci USA 100(8):4545-4550.
19. Brockwell DJ, Radford SE (2007) Intermediates: Ubiquitous species on folding energy landscapes? Curr Opin Struct Biol 17(1):30-37.
20. Roca M, Messer B, Hilvert D, Warshel A (2008) On the relationship between folding and chemical landscapes in enzyme catalysis. Proc Natl Acad Sci USA 105(37): 13877-13882.
21. Vendruscolo M, Dobson CM (2005) Towards complete descriptions of the free-energy landscapes of proteins. Philos Trans A Math Phys Eng Sci 363(1827):433-450, discussion 450-452.
22. Tsytlonok M, Itzhaki LS (2013) The how's and why's of protein folding intermediates. Arch Biochem Biophys 531(1-2):14-23.
23. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366.
24. Tokuriki N, Tawfik DS (2009) Protein dynamism and evolvability. Science 324(5924): 203-207.
25. Haddad KC, Sudmeier JL, Bachovchin DA, Bachovchin WW (2005) alpha-lytic protease can exist in two separately stable conformations with different His57 mobilities and catalytic activities. Proc Natl Acad Sci USA 102(4):1006-1011.
26. Korzhnev DM, Religa TL, Banachewicz W, Fersht AR, Kay LE (2010) A transient and low-populated protein-folding intermediate at atomic resolution. Science 329(5997): 1312-1316.
27. Neudecker P, et al. (2012) Structure of an intermediate state in protein folding and aggregation. Science 336(6079):362-366.
28. Meinhold DW, Wright PE (2011) Measurement of protein unfolding/refolding kinetics and structural characterization of hidden intermediates by NMR relaxation dispersion. Proc Natl Acad Sci USA 108(22):9078-9083.
29. Capaldi AP, Kleanthous C, Radford SE (2002) Im7 folding mechanism: Misfolding on a path to the native state. Nat Struct Biol 9(3):209-216.
30. Rumbley J, Hoang L, Mayne L, Englander SW (2001) An amino acid code for protein folding. Proc Natl Acad Sci USA 98(1):105-112.
31. Carr H, Purcell E (1954) Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys Rev 94(3):630-638.
32. Meiboom S, Gill D (1958) Modified spin-echo method for measuring nuclear relaxation times. Rev Sci Instrum 29(8):688.
33. Allerhand A, Gutowsky HS (1964) Spin-echo NMR studies of chemical exchange. I. Some general aspects. J Chem Phys 41(7):2115.
34. Forsén S, Hoffman RA (1963) Study of moderately rapid chemical exchange reactions by means of nuclear magnetic double resonance. J Chem Phys 39(11):2892.
35. Ward KM, Aletras AH, Balaban RS (2000) A new class of contrast agents for MRI based on proton chemical exchange dependent saturation transfer (CEST). J Magn Reson 143(1):79-87.
36. Hansen DF, Vallurupalli P, Kay LE (2008) Using relaxation dispersion NMR spectroscopy to determine structures of excited, invisible protein states. J Biomol NMR 41(3): 113-120.
37. Palmer AG, 3rd, Kroenke CD, Loria JP (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol 339(1997):204-238.
38. Ishima R, Torchia DA (2000) Protein dynamics from NMR. Nat Struct Biol 7(9):740-743.
39. Shen Y, et al. (2008) Consistent blind protein structure generation from NMR chemical shift data. Proc Natl Acad Sci USA 105(12):4685-4690.
40. Kohlhoff KJ, Robustelli P, Cavalli A, Salvatella X, Vendruscolo M (2009) Fast and accurate predictions of protein NMR chemical shifts from interatomic distances. J Am Chem Soc 131(39):13894-13895.
41. Shen Y, Bax A (2010) SPARTA+: A modest improvement in empirical NMR chemical shift prediction by means of an artificial neural network. J Biomol NMR 48(1):13-22.
42. Han B, Liu Y, Ginzinger SW, Wishart DS (2011) SHIFTX2: Significantly improved protein chemical shift prediction. J Biomol NMR 50(1):43-57.
43. Camilloni C, Robustelli P, De Simone A, Cavalli A, Vendruscolo M (2012) Characterization of the conformational equilibrium between the two major substates of RNase A using NMR chemical shifts. J Am Chem Soc 134(9):3968-3971.
44. Bouvignies G, Vallurupalli P, Kay LE (2014) Visualizing side chains of invisible protein conformers by solution NMR. J Mol Biol 426(3):763-774.
45. Capaldi AP, Shastry MC, Kleanthous C, Roder H, Radford SE (2001) Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nat Struct Biol 8(1): 68-72.
46. Papadakos G, Wojdyla JA, Kleanthous C (2012) Nuclease colicins and their immunity proteins. Q Rev Biophys 45(1):57-103.
47. Friel CT, Capaldi AP, Radford SE (2003) Structural analysis of the rate-limiting transition states in the folding of Im7 and Im9: Similarities and differences in the folding of homologous proteins. J Mol Biol 326(1):293-305.
48. Gorski SA, et al. (2004) Equilibrium hydrogen exchange reveals extensive hydrogen bonded secondary structure in the on-pathway intermediate of Im7. J Mol Biol 337(1): 183-193.
49. Bartlett AI, Radford SE (2010) Desolvation and development of specific hydrophobic core packing during Im7 folding. J Mol Biol 396(5):1329-1345.
50. Gorski SA, Capaldi AP, Kleanthous C, Radford SE (2001) Acidic conditions stabilise intermediates populated during the folding of Im7 and Im9. J Mol Biol 312(4):849-863.
51. Hass MAS, Hansen DF, Christensen HEM, Led JJ, Kay LE (2008) Characterization of conformational exchange of a histidine side chain: Protonation, rotamerization, and tautomerization of His61 in plastocyanin from Anabaena variabilis. J Am Chem Soc 130(26):8460-8470.
52. Reynolds WF, Peat IR, Freedman MH, Lyerla JR, Jr. (1973) Determination of the tautomeric form of the imidazole ring of L-histidine in basic solution by carbon-13 magnetic resonance spectroscopy. J Am Chem Soc 95(2):328-331.
53. Blomberg F, Maurer W, Rüterjans H (1977) Nuclear magnetic resonance investigation of 15N-labeled histidine in aqueous solution. J Am Chem Soc 99(25):8149-8159.
54. Shimahara H, et al. (2007) Tautomerism of histidine 64 associated with proton transfer in catalysis of carbonic anhydrase. J Biol Chem 282(13):9646-9656.
55. Singer AU, Forman-Kay JD (1997) pH titration studies of an SH2 domain-phosphopeptide complex: Unusual histidine and phosphate pKa values. Protein Sci 6(9): 1910-1919.
56. Cheng F, Sun H, Zhang Y, Mukkamala D, Oldfield E (2005) A solid state 13C NMR, crystallographic, and quantum chemical investigation of chemical shifts and hydrogen bonding in histidine dipeptides. J Am Chem Soc 127(36):12544-12554.
57. Li S, Hong M (2011) Protonation, tautomerization, and rotameric structure of histidine: A comprehensive study by magic-angle-spinning solid-state NMR. J Am Chem Soc 133(5):1534-1544.
58. Hunkapiller MW, Smallcombe SH, Whitaker DR, Richards JH (1973) Carbon nuclear magnetic resonance studies of the histidine residue in α-lytic protease. Implications for the catalytic mechanism of serine proteases. Biochemistry 12(23):4732-4743.
59. Wasylishen RE, Tomlinson G (1975) pH-dependence of 13C chemical shifts and 13C,H coupling constants in imidazole and L-histidine. Biochem J 147(3):605-607.
60. Pascal SM, et al. (1994) Nuclear magnetic resonance structure of an SH2 domain of phospholipase C-γ 1 complexed with a high affinity binding peptide. Cell 77(3):461-472.
61. Bachovchin WW, Kaiser R, Richards JH, Roberts JD (1981) Catalytic mechanism of serine proteases: Reexamination of the pH dependence of the histidyl 1J13C2-H coupling constant in the catalytic triad of alpha-lytic protease. Proc Natl Acad Sci USA 78(12):7323-7326.
62. Day RM, et al. (2003) Tautomerism, acid-base equilibria, and H-bonding of the six histidines in subtilisin BPN' by NMR. Protein Sci 12(4):794-810.
63. Vila JA, Arnautova YA, Vorobjev Y, Scheraga HA (2011) Assessing the fractions of tautomeric forms of the imidazole ring of histidine in proteins as a function of pH. Proc Natl Acad Sci USA 108(14):5602-5607.
64. Ishima R, Torchia DA (2003) Extending the range of amide proton relaxation dispersion experiments in proteins using a constant-time relaxation-compensated CPMG approach. J Biomol NMR 25(3):243-248.
65. Lundström P, Hansen DF, Kay LE (2008) Measurement of carbonyl chemical shifts of excited protein states by relaxation dispersion NMR spectroscopy: Comparison between uniformly and selectively (13)C labeled samples. J Biomol NMR 42(1):35-47.
66. Vallurupalli P, Bouvignies G, Kay LE (2012) Studying " invisible" excited protein states in slow exchange with a major state conformation. J AmChemSoc 134(19):8148-8161.
67. Fawzi NL, Ying J, Ghirlando R, Torchia DA, Clore GM (2011) Atomic-resolution dynamics on the surface of amyloid-β protofibrils probed by solution NMR. Nature 480(7376):268-272.
68. Whittaker SB-M, Clayden NJ, Moore GR (2011) NMR characterisation of the relationship between frustration and the excited state of Im7. J Mol Biol 414(4):511-529.
69. Hansen AL, Kay LE (2011) Quantifying millisecond time-scale exchange in proteins by CPMG relaxation dispersion NMR spectroscopy of side-chain carbonyl groups. J Biomol NMR 50(4):347-355.
70. Hansen AL, Lundström P, Velyvis A, Kay LE (2012) Quantifying millisecond exchange dynamics in proteins by CPMG relaxation dispersion NMR using side-chain 1H probes. J Am Chem Soc 134(6):3178-3189.
71. Hansen AL, Bouvignies G, Kay LE (2013) Probing slowly exchanging protein systems via 1sCα-CEST: Monitoring folding of the Im7 protein. J Biomol NMR 55(3):279-289.
72. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403-410.
73. Sekhar A, Kay LE (2013) NMR paves the way for atomic level descriptions of sparsely populated, transiently formed biomolecular conformers. Proc Natl Acad Sci USA 110(32): 12867-12874.
74. Karplus M, Kuriyan J (2005) Molecular dynamics and protein function. Proc Natl Acad Sci USA 102(19):6679-6685.
75. Chiti F, Dobson CM (2009) Amyloid formation by globular proteins under native conditions. Nat Chem Biol 5(1):15-22.
76. Bouvignies G, et al. (2011) Solution structure of a minor and transiently formed state of a T4 lysozyme mutant. Nature 477(7362):111-114.
77. Dennis CA, et al. (1998) A structural comparison of the colicin immunity proteins Im7 and Im9 gives new insights into the molecular determinants of immunity-protein specificity. Biochem J 333(Pt 1):183-191.
78. Chak KF, Safo MK, Ku WY, Hsieh SY, Yuan HS (1996) The crystal structure of the immunity protein of colicin E7 suggests a possible colicin-interacting surface. Proc Natl Acad Sci USA 93(13):6437-6442.
79. Shen Y, Bax A (2013) Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. J Biomol NMR 56(3):227-241.
80. Berjanskii MV, Wishart DS (2005) A simple method to predict protein flexibility using secondary chemical shifts. J Am Chem Soc 127(43):14970-14971.
81. Wyman J, Jr. (1964) Linked functions and reciprocal effects in hemoglobin: A second look. Adv Protein Chem 19:223-286.
82. Tollinger M, Kay LE, Forman-Kay JD (2005) Measuring pK(a) values in protein folding transition state ensembles by NMR spectroscopy. J Am Chem Soc 127(25):8904-8905.
83. JaminM, Geierstanger B, Baldwin RL (2001) The pKa of His-24 in the folding transition state of apomyoglobin. Proc Natl Acad Sci USA 98(11):6127-6131.
84. Ottiger M, Delaglio F, Bax A (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J Magn Reson 131(2):373-378.