Biocatalyst activity in nonaqueous environments correlates with centisecond-range protein motions

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

Volumn 105, Issue 41, 2008, Pages 15672-15677

  Eppler, Ross K ^a   Hudson, Elton P ^a   Chase, Shannon D ^a   Dordick, Jonathan S ^b   Reimer, Jeffrey A ^a   Clark, Douglas S ^a,c  

^a University of California   (United States)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Enzyme activation; Enzyme dynamics; NMR spectroscopy; Organic solvents; Subtilisin Carlsberg

Indexed keywords

FLUORIDE; FLUOROBENZENE; INORGANIC SALT; ORGANIC SOLVENT; PROTEIN; SUBTILISIN;

ARTICLE; BIOCATALYST; CHEMICAL ANALYSIS; CHEMICAL ENVIRONMENT; COMPETITIVE INHIBITION; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME METABOLISM; FLUORINE NUCLEAR MAGNETIC RESONANCE; MAGNETISM; MOLECULAR DYNAMICS; MOTION; NONAQUEOUS PHASE LIQUID; PHASE TRANSITION; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTON NUCLEAR MAGNETIC RESONANCE; SUSPENDED PARTICULATE MATTER; TEMPERATURE MEASUREMENT; TIME;

CATALYSIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME ACTIVATION; ENZYMES; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MOTION; PROTEINS; SOLVENTS; TIME FACTORS;

EID: 57349109904     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0804566105     Document Type: Article

References (48)

1. Henzler-Wildman KA, Kern D (2007) Dynamic personalities of proteins. Nature 450:964-972.
2. Schnell JR, Dyson HJ, Wright PE (2004) Structure, dynamics, and catalytic function of dihydrofolate reductase. Annu Rev Biophys Biomol Struct 33:119-140.
3. Benkovic SJ, Hammes-Schiffer S (2003) A perspective on enzyme catalysis. Science 301:1196-1202.
4. Eisenmesser EZ, et al. (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438:117-121.
5. Henzler-Wildman KA, et al. (2007) Intrinsic motions along an enzymatic reaction trajectory. Nature 450:838-844.
6. McElheny D, Schnell JR, Lansing JC, Dyson HJ, Wright PE (2005) Defining the role of active-site loop fluctuations in dihydrofolate reductase catalysis. Proc Natl Acad Sci USA 102:5032-5037.
7. Kovrigin EL, Loria JP (2006) Characterization of the transition state of function enzyme dynamics. J Am Chem Soc 128:7724-7725.
8. Sola RJ, Griebenow K (2006) Chemical glycosylation: New insights on the interrelation between protein structural mobility, thermodynamic stability, and catalysis. FEBS Lett 580:1685-1690.
9. Castillo B, Solá RJ, Ferrer A, Barletta G, Griebenow K (2008) Effect of PEG modification on subtilisin Carlsberg activity, enantioselectivity, and structural dynamics in 1,4-dioxane. Biotechnol Bioeng 99:9-17.
10. Klibanov AM (2001) Improving enzymes by using them in organic solvents. Nature 409:241-246.
11. Clark DS (2004) Characteristics of nearly dry enzymes in organic solvents: Implications for biocatalysis in the absence of water. Philos Trans R Soc London B 359:1299-1307.
12. Halling PJ (2004) What can we learn by studying enzymes in non-aqueous media? Philos Trans R Soc London B 359:1287-1297.
13. Schmid A, et al. (2001) Industrial biocatalysis today and tomorrow. Nature 409:258-268.
14. Paradkar VM, Dordick JS (1994) Aqueous-like activity of alpha-chymotrypsin dissolved in nearly anhydrous organic solvents. J Am Chem Soc 116:5009-5010.
15. Griebenow K, Vidal M, Baéz C, Santos AM, Barletta G (2001) Native-like enzyme properties are important for optimum activity in neat organic solvents. J Am Chem Soc 123:5380-5381.
16. Griebenow K, et al. (1999) Improved enzyme activity and enantioselectivity in organic solvents by methyl-β-cyclodextrin. J Am Chem Soc 121:8157.
17. Ru MT, et al. (2000) On the salt-induced activation of lyophilized enzymes in organic solvents: Effect of salt kosmotropicity on enzyme activity. J Am Chem Soc 122:1565-1571.
18. Lindsay JP, Clark DS, Dordick JS (2004) Combinatorial formulation of biocatalyst preparations for increased activity in organic solvents: Salt activation of penicillin amidase. Biotechnol Bioeng 85:553-560.
19. Burke PA, Griffin RG, Klibanov AM (1993) Solid-state nuclear magnetic resonance investigation of solvent dependence of tyrosyl ring motion in an enzyme. Biotechnol Bioeng 42:87-94.
20. Affleck R, Haynes CA, Clark DS (1992) Solvent dielectric effects on protein dynamics. Proc Natl Acad Sci USA 89:5167-5170.
21. Broos J, et al. (1995) Flexibility of enzymes suspended in organic solvents probed by time-resolved fluorescence anisotropy. Evidence that enzyme activity and enantioselectivity are directly related to enzyme flexibility. J Am Chem Soc 117:12657-12663.
22. Levitt MH (2008) in Spin Dynamics (Wiley, Hoboken, NJ), pp 509-595.
23. Mehring M (1983) in Principles of High Resolution of NMR in Solids (Springer, New York), pp 260-287.
24. Millet O, Muhandiram DR, Skrynnikov NR, Kay LE (2002) Deuterium spin probes of side-chain dynamics in proteins. 1. Measurement of five relaxation rates per deuteron in (13)C-labeled and fractionally (2)H-enriched proteins in solution. J Am Chem Soc 124:6439-6448.
25. Dabulis K, Klibanov AM (1993) Dramatic enhancement of enzymatic activity in organic solvents by lyoprotectants. Biotechnol Bioeng 41:566-571.
26. Triantafyllou AO, Wehtje E, Adlercreutz P, Mattiasson B (1996) How do additives affect enzyme activity and stability in nonaqueous media? Biotechnol Bioeng 54:67-76.
27. Burke PA, Griffin RG, Klibanov AM (1992) Solid-state NMR assessment of enzyme active center structure under nonaqueous conditions. J Biol Chem 267:20057-20064.
28. Chang BS, Randall CS (1992) Use of sub-ambient thermal analysis to optimize protein lyophilization. Cryobiology 29:632-656.
29. Reif B, et al. (2006) Protein side-chain dynamics observed by solution- and solid-state NMR: Comparative analysis of methyl 2H relaxation data. J Am Chem Soc 128:12354-12355.
30. Hologne M, Faelber K, Diehl A, Reif B (2005) Characterization of dynamics of perdeuterated proteins by MAS solid-state NMR. J Am Chem Soc 127:11208-11209.
31. McDermott A (2004) Structural and dynamic studies of proteins by solid-state NMR spectroscopy: Rapid movement forward. Curr Opin Struct Biol 14:554-561.
32. Lee CS, et al. (1998) Multinuclear NMR study of enzyme hydration in an organic solvent. Bioeng Biotechnol 57:686-693.
33. Eppler RK, et al. (2006) Water dynamics and salt-activation of enzymes in organic media: Mechanistic implications revealed by NMR spectroscopy. Proc Natl Acad Sci USA 103:5706-5710.
34. Fenimore P, Frauenfelder H, McMahon B, Parak F (2002) Slaving: Solvent fluctuations dominate protein dynamics and functions. Proc Natl Acad Sci USA 99:16047-16051.
35. Kamal JKA, Zhao L, Zewail AH (2004) Ultrafast hydration dynamics in protein unfolding: Human serum albumin. Proc Natl Acad Sci USA 101:13411-13416.
36. Frauenfelder H, Fenimore PW, Chen G, McMahon B (2006) Protein folding is slaved to solvent motions. Proc Natl Acad Sci USA 103:15469-15472.
37. Kamal A, et al. (2004) Enzyme functionality and solvation of subtilisin Carlsberg: From hours to femtoseconds. Chem Phys Lett 387:209-215.
38. Pal SK, Peon J, Zewail AH (2002) Ultrafast surface hydration dynamics and expression of protein functionality: α-Chymotrypsin. Proc Natl Acad Sci USA 99:15297-15302.
39. Daniel RM, et al. (1998) Enzyme activity below the dynamical transition at 220 K. Biophys J 75:2504-2507.
40. Dunn RV, et al. (2000) Enzyme activity and dynamics: Xylanase activity in the absence of fast anharmonic dynamics. Biochem J 346:355-358.
41. 19F chemical shielding in fluorobenzenes: Implications for chemical shifts in proteins. J Am Chem Soc 116:7453-7454.
42. Affleck R, et al. (1992) Enzymatic catalysis and dynamics in low-water environments. Proc Natl Acad Sci USA 89:1100-1104.
43. Suzawa VM, et al. (1995) Suspended and immobilized chymotrypsin in organic media: Structure-function relationships revealed by ESR spectroscopy. J Am Chem Soc 117:8435-8440.
44. Carnevale V, Raugei S, Micheletti C, Carloni P (2006) Convergent dynamics in the protease enzymatic superfamily. J Am Chem Soc 128:9766-9772.
45. Moore JW, Pearson RG (1981). Kinetics and Mechanism (Wiley, New York).
46. Gerig JT, Roe DC (1974) Kinetics of Inactivation of alpha-chymotrypsin with substituted benzenesulfonyl fluorides. J Am Chem Soc 96:233-238.
47. Morrisett JD, Broomfield CA (1972) Comparative study of spin-labeled serine enzymes - acetylcholinesterase, trypsin, alpha-chymotrypsin, elastase, and subtilisin. J Biol Chem 247:7224-7231.
48. Stoll S, Schweiger A (2006) EasySpin, a comprehensive software package for spectral simulation and analysis of EPR. J Magn Reson 178:42-55.