Enzymatic turnover of macromolecules generates long-lasting protein-water-coupled motions beyond reaction steady state

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

Volumn 111, Issue 50, 2014, Pages 17857-17862

  Dielmann Gessner, Jessica ^a   Grossman, Moran ^a   Nibali, Valeria Conti ^a   Born, Benjamin ^b   Solomonov, Inna ^b   Fields, Gregg B ^c   Havenith, Martina ^a   Sagi, Irit ^b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

Author keywords

Enzyme catalysis; Metalloenzymes; Solvation dynamics

Indexed keywords

COLLAGEN; GELATIN; MATRIX METALLOPROTEINASE 14; WATER; MMP14 PROTEIN, HUMAN; SOLVENT;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME DEGRADATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SUBSTRATE; HUMAN; HYDRATION; HYDROGEN BOND; MACROMOLECULE; MOLECULAR DYNAMICS; PHASE TRANSITION; PROTEIN STRUCTURE; ROENTGEN SPECTROSCOPY; SOLVATION; STEADY STATE; TERAHERTZ SPECTROSCOPY; CHEMICAL MODEL; FLUORESCENCE; KINETICS; METABOLISM; PROTEIN DEGRADATION; X RAY ABSORPTION SPECTROSCOPY;

COLLAGEN; FLUORESCENCE; HUMANS; KINETICS; MATRIX METALLOPROTEINASE 14; MODELS, CHEMICAL; MOLECULAR DYNAMICS SIMULATION; PROTEOLYSIS; SOLVENTS; TERAHERTZ SPECTROSCOPY; WATER; X-RAY ABSORPTION SPECTROSCOPY;

EID: 84919363043     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1410144111     Document Type: Article

References (38)

1. Michaelis L, Menten ML (1913) Die Kinetik der Invertinwirkung. Biochem Z 49:333-362.
2. Johnson KA (2013) A century of enzyme kinetic analysis, 1913 to 2013. FEBS Lett 587(17):2753-2766.
3. Segel IH (1993) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme System (Wiley, New York).
4. Cleland WW (1989) Enzyme kinetics revisited: A commentary on 'The Kinetics of Enzyme-Catalyzed Reactions With Two or More Substrates or Products.' Biochim Biophys Acta 1000:209-212.
5. Min W, Xie XS, Bagchi B (2009) Role of conformational dynamics in kinetics of an enzymatic cycle in a nonequilibrium steady state. J Chem Phys 131(6):065104.
6. Min W, et al. (2006) When does the Michaelis-Menten equation hold for fluctuating enzymes? J Phys Chem B 110(41):20093-20097.
7. Schnell S (2014) Validity of the Michaelis-Menten equation-steady-state or reactant stationary assumption: That is the question. FEBS J 281(2):464-472.
8. Kou SC, Cherayil BJ, Min W, English BP, Xie XS (2005) Single-molecule Michaelis-Menten equations. J Phys Chem B 109(41):19068-19081.
9. Kolomeisky AB (2011) Michaelis-Menten relations for complex enzymatic networks. J Chem Phys 134(15):155101.
10. Dhar A, et al. (2010) Structure, function, and folding of phosphoglycerate kinase are strongly perturbed by macromolecular crowding. Proc Natl Acad Sci USA 107(41):17586-17591.
11. Grossman M, et al. (2011) Correlated structural kinetics and retarded solvent dynamics at the metalloprotease active site. Nat Struct Mol Biol 18(10):1102-1108.
12. Zaccai G (2004) The effect of water on protein dynamics. Philos Trans R Soc Lond B Biol Sci 359(1448):1269-1275.
13. Bagchi B (2005) Water dynamics in the hydration layer around proteins and micelles. Chem Rev 105(9):3197-3219.
14. Fenimore PW, Frauenfelder H, McMahon BH, Young RD (2004) Bulk-solvent and hydration-shell fluctuations, similar to alpha- and beta-fluctuations in glasses, control protein motions and functions. Proc Natl Acad Sci USA 101(40):14408-14413.
15. Frauenfelder H, et al. (2009) A unified model of protein dynamics. Proc Natl Acad Sci USA 106(13):5129-5134.
16. Frauenfelder H, Fenimore PW, Chen G, McMahon BH (2006) Protein folding is slaved to solvent motions. Proc Natl Acad Sci USA 103(42):15469-15472.
17. Frauenfelder H, Fenimore PW, McMahon BH (2002) Hydration, slaving and protein function. Biophys Chem 98(1-2):35-48.
18. Pal SK, Peon J, Zewail AH (2002) Biological water at the protein surface: Dynamical solvation probed directly with femtosecond resolution. Proc Natl Acad Sci USA 99(4):1763-1768.
19. Pal SK, Zewail AH (2004) Dynamics of water in biological recognition. Chem Rev 104(4):2099-2123.
20. Levy Y, Onuchic JN (2006) Water mediation in protein folding and molecular recognition. Annu Rev Biophys Biomol Struct 35:389-415.
21. Ahmad M, Gu W, Geyer T, Helms V (2011) Adhesive water networks facilitate binding of protein interfaces. Nat Commun 2:261.
22. Lockett MR, et al. (2013) The binding of benzoarylsulfonamide ligands to human carbonic anhydrase is insensitive to formal fluorination of the ligand. Angew Chem Int Ed Engl 52(30):7714-7717.
23. Grover CN, Cameron RE, Best SM (2012) Investigating the morphological, mechanical and degradation properties of scaffolds comprising collagen, gelatin and elastin for use in soft tissue engineering. J Mech Behav Biomed Mater 10:62-74.
24. Bertini I, et al. (2012) Structural basis for matrix metalloproteinase 1-catalyzed collagenolysis. J Am Chem Soc 134(4):2100-2110.
25. Manka SW, et al. (2012) Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc Natl Acad Sci USA 109(31):12461-12466.
26. Minond D, Lauer-Fields JL, Nagase H, Fields GB (2004) Matrix metalloproteinase triplehelical peptidase activities are differentially regulated by substrate stability. Biochemistry 43(36):11474-11481.
27. Lauer-Fields JL, et al. (2001) Kinetic analysis of matrix metalloproteinase activity using fluorogenic triple-helical substrates. Biochemistry 40(19):5795-5803.
28. Bhaskaran R, Palmier MO, Lauer-Fields JL, Fields GB, Van Doren SR (2008) MMP-12 catalytic domain recognizes triple helical peptide models of collagen V with exosites and high activity. J Biol Chem 283(31):21779-21788.
29. Grossman M, et al. (2010) The intrinsic protein flexibility of endogenous protease inhibitor TIMP-1 controls its binding interface and affects its function. Biochemistry 49(29):6184-6192.
30. Chung L, et al. (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 23(15):3020-3030.
31. Solomon A, Akabayov B, Frenkel A, Milla ME, Sagi I (2007) Key feature of the catalytic cycle of TNF-alpha converting enzyme involves communication between distal protein sites and the enzyme catalytic core. Proc Natl Acad Sci USA 104(12):4931-4936.
32. Heyden M, Havenith M (2010) Combining THz spectroscopy and MD simulations to study protein-hydration coupling. Methods 52(1):74-83.
33. Bergner A, et al. (2005) New p-Ge THz laser spectrometer for the study of solutions: THz absorption spectroscopy of water. Rev Sci Instrum 76(6):063110-063115.
34. Conti Nibali V, Havenith M (2014) New insights into the role of water in biological function: Studying solvated biomolecules using terahertz absorption spectroscopy in conjunction with molecular dynamics simulations. J Am Chem Soc 136(37):12800-12807.
35. Ball P (2011) Biophysics: More than a bystander. Nature 478(7370):467-468.
36. Van Der Spoel D, et al. (2005) GROMACS: Fast, flexible, and free. J Comput Chem 26(16):1701-1718.
37. Mackerell AD, Jr, Feig M, Brooks CL, 3rd (2004) Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25(11):1400-1415.
38. Fields GB (2013) Interstitial collagen catabolism. J Biol Chem 288(13):8785-8793.