Temperature dependence of protein motions in a thermophilic dihydrofolate reductase and its relationship to catalytic efficiency

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

Volumn 107, Issue 22, 2010, Pages 10074-10079

  Oyeyemi, Olayinka A ^a,b   Sours, Kevin M ^b   Lee, Thomas ^b   Resing, Katheryn A ^b   Ahn, Natalie G ^b   Klinman, Judith P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Dihydrofolate reductase; Hydrogen deuterium exchange; Hydrogen tunneling; Protein dynamics; Thermophilic protein

Indexed keywords

DIHYDROFOLATE REDUCTASE; HYDROGEN;

ARTICLE; CATALYSIS; CIRCULAR DICHROISM; DEUTERIUM HYDROGEN EXCHANGE; GEOBACILLUS STEAROTHERMOPHILUS; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DEUTERIUM; ENZYME STABILITY; GEOBACILLUS STEAROTHERMOPHILUS; HYDROGEN; KINETICS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MOTION; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; TEMPERATURE; TETRAHYDROFOLATE DEHYDROGENASE; THERMODYNAMICS;

GEOBACILLUS STEAROTHERMOPHILUS;

EID: 77953386194     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1003678107     Document Type: Article

References (46)

1. Blakley R (1984) Folates and Pterins, eds RA Blakley and SJ Benkovic (Wiley, New York), pp 191-253.
2. Peppard WJ, Schuenke CD (2008) Iclaprim, a diaminopyrimidine dihydrofolate reductase inhibitor for the potential treatment of antibiotic-resistant staphylococcal infections. Curr Opin Invest Dr 9:210-225.
3. Gangjee A, Kurup S, Namjoshi O (2007) Dihydrofolate reductase as a target for chemotherapy in parasites. Curr Pharm Design 13:609-639. (Pubitemid 46477747)
4. Soeiro MNC, de Castro SL (2009) Trypanosoma cruzi targets for new chemotherapeutic approaches. Expert Opin Ther Tar 13:105-121.
5. Sikorski RS, et al. (2004) Tunneling and coupled motion in the E. coli dihydrofolate reductase catalysis. J Am Chem Soc 126:4778-4779.
6. Wang L, Goodey NM, Benkovic SJ, Kohen A (2006) Coordinated effects of distal mutations on environmentally coupled tunneling in dihydrofolate reductase. Proc Natl Acad Sci USA 103:15753-15758. (Pubitemid 44657539)
7. Osborne MJ, Schnell J, Benkovic SJ, Dyson HJ, Wright PE (2001) Backbone dynamics in dihydrofolate reductase complexes: Role of loop flexibility in the catalytic mechanism. Biochemistry 40:9846-9859. (Pubitemid 32769533)
8. Venkitakrishnan RP, et al. (2004) Conformational changes in the active site loops of dihydrofolate reductase during the catalytic cycle. Biochemistry 43:16046-16055.
9. Boehr DD, Dyson HJ, Wright PE (2008) Conformational relaxation following hydride transfer plays a limiting role in dihydrofolate reductase catalysis. Biochemistry 35:9227-9233.
10. Zhang ZQ, Rajagopalan PTR, Selzer T, Benkovic SJ, Hammes GG (2004) Single-molecule and transient kinetics investigation of the interaction of dihydrofolate reductase with NADPH and dihydrofolate. Proc Natl Acad Sci USA 101:2764-2769. (Pubitemid 38327685)
11. Antikainen NM, Smiley RD, Benkovic SJ, Hammes GG (2005) Conformation coupled enzyme catalysis: Single-molecule and transient kinetics investigation of dihydrofolate reductase. Biochemistry 44:16835-16843.
12. Falzone CJ, Wright PE, Benkovic SJ (1994) Dynamics of a flexible loop in dihydrofolate reductase from E. coli and its implication for catalysis. Biochemistry 33:439-442.
13. Boehr DD, McElheny D, Dyson HJ, Wright PE (2006) The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313:1638-1642. (Pubitemid 44414038)
14. Kim HS, Damo SM, Lee SY, Wemmer D, Klinman JP (2005) Structure and hydride transfer mechanism of a moderate thermophilic dihydrofolate reductase from B. stearothermophilus and comparison to its mesophilic and hyperthermophilic homologues. Biochemistry 44:11428-11439. (Pubitemid 41209078)
15. Fierke CA, Kuchta RD, Johnson KA, Benkovic SJ (1987) Implications for enzymic catalysis from free-energy reaction coordinate profiles. Cold Spring Harb Sym 52:631-638.
16. Wintrode PL, Zhang DQ, Vaidehi N, Arnold FH, Goddard WA (2003) Protein dynamics in a family of laboratory evolved thermophilic enzymes. J Mol Biol 327:745-757. (Pubitemid 36299076)
17. Wallon G, et al. (1997) Crystal structures of E. coli and Salmonella typhimurium 3-isopropylmalate dehydrogenase and comparison with their thermophilic counterpart from Thermus thermophilus. J Mol Biol 266:1016-1031. (Pubitemid 27122606)
18. Britton KL, et al. (1999) Structure determination of the glutamate dehydrogenase from the hyperthermophile Thermococcus litoralis and its comparison with that from Pyrococcus furiosus. J Mol Biol 293:1121-1132.
19. Wang L, Goodey NM, Benkovic SJ, Kohen A (2006) The role of enzyme dynamics and tunnelling in catalysing hydride transfer: Studies of distal mutants of dihydrofolate reductase. Philos T R Soc B 361:1307-1315. (Pubitemid 44338491)
20. Bai Y, Milne JS, Mayne L, Englander SW (1993) Primary structure effects on peptide group hydrogen exchange. Proteins 17:75-86. (Pubitemid 23261059)
21. Englander SW, Downer NW, Teitelba H (1997) Hydrogen exchange: The modern legacy of Linderstrom-Lang. Protein Sci 6:1101-1109.
22. Bai Y, Sosnick TR, Mayne L, Englander SW (1995) Protein folding intermediates: Native-state hydrogen exchange. Science 269:192-196.
23. Chamberlain AK, Handel TM, Marqusee S (1996) Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH. Nat Struct Biol 3:782-787.
24. Hoofnagle AN, Resing KA, Ahn NG (2003) Protein analysis by hydrogen exchange mass spectrometry. Annu Rev Bioph Biom 32:1-25. (Pubitemid 37056219)
25. Klinman JP (2009) An integrated model for enzyme catalysis emerges from studies of hydrogen tunneling. Chem Phys Lett 471:179-193.
26. Nagel ZD, Klinman JP (2009) A 21st century revisionist's view at a turning point in enzymology. Nat Chem Biol 5:543-551.
27. Swanwick RS, Daines AM, Tey LH, Flitsch SL, Allemann RK (2005) Increased thermal stability of site-selectivity glycosylated dihydrofolate reductase. Chem Biochem 6:1338-1340.
28. Yamamoto T, Izumi S, Gekko K (2004) Mass spectrometry of hydrogen/deuterium exchange of E. coli dihydrofolate reductase: effects of loop mutations. J Biochem-Tokyo 135:487-94. (Pubitemid 38660935)
29. Sawaya MR, Kraut J (1997) Loop and subdomain movements in the mechanism of E. coli dihydrofolate reductase: Crystallographic evidence. Biochemistry 36:586-603.
30. Danell AS, Parks JH (2003) Fraying and electron autodetachment dynamics of trapped gas phase oligonucleotides. J Am Soc Mass Spectr 14:1330-1339.
31. Milev S, et al. (2003) Energetics of sequence-specific protein-DNA association: Conformational stability of the DNA-binding domain of integrase Tn916 and its cognate DNA duplex. Biochemistry 42:3492-3502. (Pubitemid 36368643)
32. Lam SL, Ip LN (2002) Low temperature solution structures and base pair stacking of double helical d(CGTACG)(2). J Biomol Struct Dyn 19:907-917.
33. Hochstrasser RA, Carver TE, Sowers LC, Millar DP (1994) Melting of a DNA helix terminus within the active-site of a DNA-polymerase. Biochemistry 33:11971-11979.
34. Luo J, Iwakura M, Matthews CR (1995) Detection of a stable intermediate in the thermal unfolding of a cysteine-free form of dihydrofolate reductase from Escherichia coli. Biochemistry 34:10669-10675.
35. Knapp MJ, Klinman JP (2002) Environmentally coupled hydrogen tunneling: Linking catalysis to dynamics. Eur J Biochem 269:3113-3121.
36. Kuznetsov AM, Ulstrup J (1999) Proton and hydrogen atom tunneling in hydrolytic and redox enzyme catalysis. Can J Chem 77:1085-1096.
37. Hammes-Schiffer S (2002) Comparison of hydride, hydrogen atom, and proton-coupled electron transfer reactions. Chemphyschem 3:33-42.
38. Liang ZX (2004) Thermal-activated protein mobility and its correlation with catalysis in thermophilic alcohol dehydrogenase. Proc Natl Acad Sci USA 101:9556-9561.
39. Nagel ZD, Klinman JP (2006) Tunneling and dynamics in enzymatic hydride transfer. Chem Rev 106:3095-3118.
40. Eisenmesser EZ, et al. (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438:117-121. (Pubitemid 41599831)
41. Hanson JA, et al. (2007) Illuminating the mechanistic roles of enzyme conformational dynamics. Proc Natl Acad Sci USA 104:18055-18060.
42. Liu Y-H, De La Rosa M (2006) Enzyme conformational dynamics during catalysis and in the "resting" state monitored by hydrogen/deuterium exchange mass spectrometry. FEBS Lett 580:5137-5142.
43. Agarwal PK, Billeter SR, Rajagopalan PT, Benkovic SJ, Hammes-Schiffer S (2002) Network of coupled promoting motions in enzyme catalysis. Proc Natl Acad Sci USA 99:2794-2799.
44. Wong KF, Selzer T, Benkovic SJ, Hammes-Schiffer S (2005) Impact of distal mutations on the network of coupled motions correlated to hydride transfer in dihydrofolate reductase. Proc Natl Acad Sci USA 102:6807-6812. (Pubitemid 40675397)
45. Arora K, Brooks CL (2009) Functionally important conformations of the Met20 Loop in dihydrofolate reductase are populated by rapid thermal fluctuations. J Am Chem Soc 131:5642-5647.
46. Resing KA, Hoofnagle AN, Ahn NG (1999) Modeling deuterium exchange behavior of ERK2 using pepsin mapping to probe secondary struture. J Am Soc Mass Spectr 10:685-702.