Sampling the conformational energy landscape of a hyperthermophilic protein by engineering key substitutions

Molecular Biology and Evolution

Volumn 29, Issue 6, 2012, Pages 1683-1694

  Colletier, Jacques Philippe ^a,b   Aleksandrov, Alexey ^a   Coquelle, Nicolas ^a,c   Mraihi, Sonia ^a   Mendoza Barberá, Elena ^a,d   Field, Martin ^a   Madern, Dominique ^a  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^c UNIVERSITY OF ALBERTA   (Canada)

^d BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

Author keywords

Hyperthermophilic; Lactate dehydrogenase; Protein adaptation; Protein conformational energy landscape

Indexed keywords

FRUCTOSE 1,6 BISPHOSPHATE; LACTATE DEHYDROGENASE; LACTIC ACID; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ADAPTATION; ALLOSTERISM; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; ENERGY; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; HIGH TEMPERATURE; HYPERTHERMOPHILIC BACTERIUM; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; OXIDATION; PHENOTYPE; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN STABILITY; SAMPLING; THERMOSTABILITY; THERMUS THERMOPHILUS; WILD TYPE;

ALLOSTERIC REGULATION; AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ENZYME STABILITY; FRUCTOSEDIPHOSPHATES; HOT TEMPERATURE; KINETICS; L-LACTATE DEHYDROGENASE; LACTIC ACID; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PYRUVIC ACID; THERMODYNAMICS; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); THERMUS THERMOPHILUS;

EID: 84861359623     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss015     Document Type: Article

References (56)

1. Adams PD, Afonine PV, Bunkóczi G, et al. (18 co-authors). 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr Sect D Biol Crystallogr. 66:213-221.
2. Aghajari N, Feller G, Gerday C, Haser R. 1998. Structures of the psychrophilic Alteromonas haloplanctis alpha-amylase give insights into cold adaptation at a molecular level. Structure 6:1503-1516. (Pubitemid 29000528)
3. Arai K, Ishimitsu T, Fushinobu S, Uchikoba H, Matsuzawa H, Taguchi H. 2010. Active and inactive state structures of unliganded Lactobacillus casei allosteric L-lactate dehydrogenase. Proteins 78:681-694.
4. Arnold FH, Wintrode PL, Miyazaki K, Gershenson A. 2001. How enzymes adapt: lessons from directed evolution. Trends Biochem Sci. 26:100-106. (Pubitemid 32144744)
5. Bae E, Phillips GN Jr. 2006. Roles of static and dynamic domains in stability and catalysis of adenylate kinase. Proc Natl Acad Sci USA. 103:2132-2137. (Pubitemid 43271635)
6. Bershtein S, Goldin K, Tawfik DS. 2008. Intense neutral drifts yield robust and evolvable consensus proteins. J Mol Biol. 379:1029-1044.
7. Bloom JD, Arnold FH. 2009. In the light of directed evolution: pathways of adaptive protein evolution. Proc Natl Acad Sci USA. 106:9995-10000.
8. Brooks BR, Brooks CL 3rd, Mackerell AD Jr, et al. (35 co-authors). 2009. CHARMM: the biomolecular simulation program. J Comput Chem. 30:1545-1614.
9. Cameron AD, Roper DI, Moreton KM, Muirhead H, Holbrook JJ, Wigley DB. 1994. Allosteric activation in Bacillus stearothermophilus lactate dehydrogenase investigated by an X-ray crystallographic analysis of a mutant designed to prevent tetramerization of the enzyme. J Mol Biol. 238:615-625. (Pubitemid 24160286)
10. Carroll MJ, Gromova AV, Miller KR, Tang H, Wang XS, Tripathy A, Singleton SF, Collins EJ, Lee AL. 2011. Direct detection of structurally resolved dynamics in a multiconformation receptorligand complex. J Am Chem Soc. 133:6422-6428.
11. Coquelle N, Fioravanti E, Weik M, Vellieux F, Madern D. 2007. Activity, stability and structural studies of lactate dehydrogenases adapted to extreme thermal environments. J Mol Biol. 374:547-562. (Pubitemid 350007659)
12. Crehuet R, Field MJ. 2003. A temperature-dependent nudgedelastic-band algorithm. J Chem Phys. 118:9563-9571.
13. Crehuet R, Thomas A, Field MJ. 2005. An implementation of the nudged elastic band algorithm and application to the reaction mechanism of HGXPRTase from Plasmodium falciparum. J Mol Graph Model. 24:102-110. (Pubitemid 41377110)
14. Delano W. 2002. The PyMOL molecular graphics system. San Carlos (CA): DeLano Scientific.
15. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr Sect D Biol Crystallogr. 60:2126-2132. (Pubitemid 41742764)
16. Eventoff W, Rossmann MG, Taylor SS, Torff HJ, Meyer H, Keil W, Kiltz HH. 1977. Structural adaptations of lactate dehydrogenase isozymes. Proc Natl Acad Sci USA. 74:2677-2681. (Pubitemid 8150798)
17. Feller G, Gerday C. 2003. Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol. 1:200-208.
18. Ferrer S, Silla E, Tunon I, Oliva M, Moliner V, Williams I. 2005. Dependence of enzyme reaction mechanism on protonation state of titratable residues and QM level description: lactate dehydrogenase. Chem Commun. 47:5873-5875. (Pubitemid 43021902)
19. Ferrer S, Tunon I, Marti SV, Garcia-Viloca M, Gonzalez-Lafont A, Lluch J. 2006. A theoretical analysis of rate constants and kinetic isotope effects corresponding to different reactant valleys in lactate dehydrogenase. J Am Chem Soc. 128:16851-16863. (Pubitemid 46032761)
20. Field MJ. 2007. A practical introduction to the simulation of molecular systems. New York: Cambridge University Press.
21. Field MJ. 2008. The pDynamo program for molecular simulations using hybrid quantum chemical and molecular mechanical potentials. J Chem Theory Comput. 4:1151-1161.
22. Fields PA, Houseman DE. 2004. Decreases in activation energy and substrate affinity in cold-adapted A4-lactate dehydrogenase: evidence from the Antarctic notothenioid fish Chaenocephalus aceratus. Mol Biol Evol. 21:2246-2255. (Pubitemid 39488895)
23. Fields PA, Somero GN. 1998. Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes. Proc Natl Acad Sci USA. 95:11476-11481. (Pubitemid 28450154)
24. Fraser JS, Clarkson MW, Degnan SC, Erion R, Kern D, Alber T. 2009. Hidden alternative structures of proline isomerase essential for catalysis. Nature 462:669-673.
25. Frauenfelder H, Chen G, Berendzen J, Fenimore PW, Jansson H, McMahon BH, Stroe IR, Swenson J, Young RD. 2009. A unified model of protein dynamics. Proc Natl Acad Sci USA. 106:5129-5134.
26. Galvan I, Field MJ. 2008. Improving the efficiency of the NEB reaction path finding algorithm. J Comput Chem. 29:139-143.
27. Gershenson A, Schauerte JA, Giver L, Arnold FH. 2000. Tryptophan phosphorescence study of enzyme flexibility and unfolding in laboratory-evolved thermostable esterases. Biochemistry 39: 4658-4665. (Pubitemid 30225329)
28. Giver L, Gershenson A, Freskgard PO, Arnold FH. 1998. Directed evolution of a thermostable esterase. Proc Natl Acad Sci USA. 95:12809-12813. (Pubitemid 28509479)
29. Henzler-Wildman KA, Lei M, Thai V, Kerns SJ, Karplus M, Kern D. 2007. A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450:913-916. (Pubitemid 350231333)
30. Hochachka PW, Somero GN. 2002. Biochemical adaptation: mechanism and process in physiological evolution. Oxford (UK): Oxford University Press.
31. Iwata S, Kamata K, Yoshida S, Minowa T, Ohta T. 1994. T and R states in the crystals of bacterial L-lactate dehydrogenase reveal the mechanism for allosteric control. Nat Struct Biol. 1:176-185. (Pubitemid 24974834)
32. Iwata S, Ohta T. 1993. Molecular basis of allosteric activation of bacterial L-lactate dehydrogenase. J Mol Biol. 230:21-27. (Pubitemid 23093544)
33. Jackson CJ, Foo JL, Tokuriki N, Afriat L, Carr PD, Kim HK, Schenk G, Tawfik DS, Ollis DL. 2009. Conformational sampling, catalysis, and evolution of the bacterial phosphotriesterase. Proc Natl Acad Sci USA. 106:21631-21636.
34. Jeon J, Nam H-J, Choi YS, Yang J-S, Hwang J, Kim S. 2011. Molecular evolution of protein conformational changes revealed by a network of evolutionary coupled residues. Mol Biol Evol. 28:2675-2685.
35. Jorgensen W, Chandrasekar J, Madura J, Impey R, Klein M. 1983. Comparison of simple potential functions for simulating liquid water. J Chem Phys. 79:926-935.
36. Kabsch W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst. 26:795-800.
37. Lam SY, Yeung RC, Yu TH, Sze KH, Wong KB. 2011. A rigidifying saltbridge favors the activity of thermophilic enzyme at high temperatures at the expense of low-temperature activity. PLoS Biol. 9:e1001027.
38. Li H, Robertson AD, Jensen JH. 2005. Very fast empirical prediction and rationalization of protein pKa values. Proteins 61:704-721. (Pubitemid 41753142)
39. MacKerell A, Bashford D, Bellott M, et al. (29 co-authors). 1998. An all-atom empirical potential for molecular modelling and dynamics study of proteins. J Phys Chem B. 102:3586-3616. (Pubitemid 128576688)
40. Madern D. 2002. Molecular evolution within the L-malate and L-lactate dehydrogenase super-family. J Mol Evol. 54:825-840. (Pubitemid 34553648)
41. Mingardon F, Bagert JD, Maisonnier C, Trudeau DL, Arnold FH. 2011. Comparison of family 9 cellulases from mesophilic and thermophilic bacteria. Appl Environ Microbiol. 77:1436-1442.
42. Monod J, Wyman J, Changeux JP. 1965. On the nature of allosteric transitions: a plausible model. J Mol Biol. 12:88-118.
43. Neese F. 2008. ORCA-an ab initio, density functional and semiempirical program package, version 2.6. Bonn (Germany): University of Bonn.
44. Patthy L. 2008. Protein evolution. 2nd ed. Oxford (UK): Blackwell Publishing.
45. Phillips J, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel R, Kale L, Schulten K. 2005. Scalable molecular dynamics with NAMD. J Comput Chem. 26:1781-1802. (Pubitemid 43078511)
46. Ramanathan A, Savol AJ, Langmead CJ, Agarwal PK, Chennubhotla CS. 2011. Discovering conformational sub-states relevant to protein function. PLoS One 6:e15827.
47. Ranganathan S, Gready J. 1997. Hybrid quantum and molecular mechanical (QM/MM) studies on the pyruvate to l-lactate interconversion in l-lactate dehydrogenase. J Phys Chem B. 101: 5614-5618. (Pubitemid 127607135)
48. Read RJ. 2001. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr Sect D Biol Crystallogr. 57:1373-1382. (Pubitemid 36117185)
49. Salverda ML, Dellus E, Gorter FA, Debets AJ, van der Oost J, Hoekstra RF, Tawfik DS, de Visser JA. 2011. Initial mutations direct alternative pathways of protein evolution. PLoS Genet. 7(3):e1001321.
50. Sanson B, Colletier JP, Xu Y, Lang PT, Jiang H, Silman I, Sussman JL, Weik M. 2011. Backdoor opening mechanism in acetylcholinesterase based on X-ray crystallography and molecular dynamics simulations. Protein Sci. 20:1114-1118.
51. Schrank TP, Bolen DW, Hilser VJ. 2009. Rational modulation of conformational fluctuations in adenylate kinase reveals a local unfolding mechanism for allostery and functional adaptation in proteins. Proc Natl Acad Sci USA. 106:16984-16989.
52. Siddiqui KS, Cavicchioli R. 2006. Cold adapted enzymes. Annu Rev Biochem. 75:403-433.
53. Soskine M, Tawfik DS. 2010. Mutational effects and the evolution of new protein functions. Nat Rev Genet. 11:572-582.
54. Thomas AS, Elcock AH. 2006. Direct observation of salt effects on molecular interactions through explicit-solvent molecular dynamics simulations: differential effects on electrostatic and hydrophobic interactions and comparisons to Poisson-Boltzmann theory. J Am Chem Soc. 128:7796-7806. (Pubitemid 43945722)
55. Tokuriki N, Tawfik DS. 2009. Protein dynamism and evolvability. Science 324:203-207.
56. Wilks HM, Hart KW, Feeney R, Dunn CR, Muirhead H, Chia WN, Barstow DA, Atkinson T, Clarke AR, Holbrook JJ. 1988. A specific, highly active malate dehydrogenase by redesign of a lactate dehydrogenase framework. Science 242:1541-1544. (Pubitemid 19023696)