Comparative hydrogen-deuterium exchange for a mesophilic vs thermophilic dihydrofolate reductase at 25 °c: Identification of a single active site region with enhanced flexibility in the mesophilic protein

Biochemistry

Volumn 50, Issue 38, 2011, Pages 8251-8260

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

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c E11 SSH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3-DIMENSIONAL STRUCTURES; ACTIVE SITE; AMIDE HYDROGENS; COFACTORS; DIHYDROFOLATE REDUCTASE; E. COLI; ENTHALPIC BARRIERS; HYDRIDE TRANSFERS; HYDROGEN-DEUTERIUM EXCHANGE; INCREASED FLEXIBILITY; INTRINSIC RATE CONSTANT; MESOPHILIC; ORTHOLOGOUS PROTEINS; ORTHOLOGS; PRIMARY STRUCTURES; PROTEIN SURFACE; SEQUENCE IDENTITY; SPATIAL RESOLUTION; STEAROTHERMOPHILUS; SUBSTRATE-BINDING SITES; SURROUNDING REGIONS;

AMIDES; BINDING SITES; DEUTERIUM; MASS SPECTROMETRY; PEPTIDES; RATE CONSTANTS;

HYDROGEN;

DIHYDROFOLATE REDUCTASE; HYDROGEN; PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL ANALYSIS; COMPARATIVE STUDY; DEUTERIUM HYDROGEN EXCHANGE; ENTHALPY; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; GEOBACILLUS STEAROTHERMOPHILUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FLEXIBILITY; PROTEIN FUNCTION; TEMPERATURE MEASUREMENT;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CATALYTIC DOMAIN; DEUTERIUM EXCHANGE MEASUREMENT; ENZYME STABILITY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GEOBACILLUS STEAROTHERMOPHILUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; STRUCTURAL HOMOLOGY, PROTEIN; TETRAHYDROFOLATE DEHYDROGENASE; THERMODYNAMICS;

EID: 80053000013     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200640s     Document Type: Article

References (37)

1. Oyeyemi et al. (2010) Proc. Natl. Acad. Sci. U.S.A. 107, 10074
2. Hammes-Schiffer, S. and Benkovic, S. J. (2006) Relating protein motion to catalysis Annu. Rev. Biochem. 75, 519-541 (Pubitemid 44118042)
3. Henzler-Wildman, K. A., Lei, M., Thai, V., Kerns, S. J., Karplus, M., and Kern, D. (2007) A hierarchy of timescales in protein dynamics is linked to enzyme catalysis Nature 450, 913-916 (Pubitemid 350231333)
4. Nagel, Z. D. and Klinman, J. P. (2009) A 21st century revisionist's view at a turning point in enzymology Nat. Chem. Biol. 5, 543-550
5. Schwartz, S. and Schramm, V. L. (2009) Enzymatic transition states and dynamic motion in barrier crossing Nat. Chem. Biol. 5, 551-558
6. Fields, P. A. (2001) Review: Protein function at thermal extremes: balancing stability and flexibility Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 129, 417-431 (Pubitemid 32553917)
7. Liang, Z.-X., Tsigos, I., Bouriotis, V., and Klinman, J. P. (2004) Impact of protein flexibility on hydride-transfer parameters in thermophilic and psychrophilic alcohol dehydrogenases J. Am. Chem. Soc. 126, 9500-9501 (Pubitemid 39031012)
8. Kim, H. S., Damo, S. M., Lee, S. Y., Wemmer, D., and Klinman, J. P. (2005) Structure and hydride transfer mechanism of a moderate thermophilic dihydrofolate reductase from Bacillus stearothermophilus and comparison to its mesophilic and hyperthermophilic homologues Biochemistry 44, 11428-11439 (Pubitemid 41209078)
9. Bolin, J. T., Filman, D. J., Matthews, D. A., Hamlin, R. C., and Kraut, J. (1982) Crystal structures of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 Å resolution. I. General features and binding of methotrexate J. Biol. Chem. 257, 13650-13662 (Pubitemid 13187127)
10. Filman, D. J., Bolin, J. T., Matthews, D. A., and Kraut, J. (1982) Crystal structures of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 Å resolution. II. Environment of bound NADPH and implications for catalysis J. Biol. Chem. 257, 13663-13672 (Pubitemid 13187128)
11. Bystroff, C. and Kraut, J. (1991) Crystal structure of unliganded Escherichia coli dihydrofolate reductase. Ligand-induced conformational changes and cooperativity in binding Biochemistry 30, 2227-2239
12. Bystroff, C., Oatley, S. J., and Kraut, J. (1990) Crystal structures of Escherichia coli dihydrofolate reductase: the NADP+ holoenzyme and the folate. NADP+ ternary complex. Substrate binding and a model for the transition state Biochemistry 29, 3263-3277 (Pubitemid 20131468)
13. Sikorski, R. S., Wang, L., Markham, K. A., Rajagopalan, P. T. R., Benkovic, S. J., and Kohen, A. (2004) Tuneling and coupled motion in the E. coli dihydrofolate reducatse catalysis J. Am. Chem. Soc. 126, 4778-4779 (Pubitemid 38490135)
14. Knapp, M. J. and Klinman, J. P. (2002) Environmentally coupled hydrogen tunneling-Linking catalysis to dynamics Eur. J. Biochem. 269, 3113-3121 (Pubitemid 34748097)
15. Klinman, J. P. (2009) An integrated model for enzyme catalysis emerges from studies of hydrogen tunneling Chem. Phys. Lett. 471, 179-193
16. Wang, L., Goodey, N. M., Benkovic, S. J., and Kohen, A. (2006) Coordinated effects of distal mutations on environmentally coupled tunneling in dihydrofolate reductase Proc. Natl. Acad. Sci. U.S.A. 103, 15753-15758 (Pubitemid 44657539)
17. Hvidt, A. (1964) A Discussion of the pH dependence of the hydrogen-deuterium exchange of proteins Cr. Trav. Lab. Carlsberg 34, 299-317
18. Swint-Kruse, L. and Robertson, A. D. (1996) Temperature and pH dependences of hydrogen exchange and global stability for ovomucoid third domain Biochemistry 35, 171-180 (Pubitemid 26036420)
19. Oyeyemi, O. A., Sours, K. M., Lee, T., Resing, K. A., Ahn, N. G., and Klinman, J. P. (2010) Temperature dependence of protein motions in a thermophilic dihydrofolate reductase and its relationship to catalytic efficiency Proc. Natl. Acad. Sci. U.S.A. 107, 10074-10079
20. Andreotti, G., Cubellis, M. V., Palo, M. D., Fessas, D., Sannia, G., and Marino, G. (1997) Stability of a thermophilic TIM-barrel enzyme: indole-3-glycerol phosphate synthase from the thermophilic archaeon Sulfolobus solfataricus Biochem. J. 323 (Pt 1) 259-264 (Pubitemid 27153902)
21. Sriprapundh, D. (2003) Directed evolution of Thermotoga neapolitana xylose isomerase: high activity on glucose at low temperature and low pH Protein Eng. 16, 683-690 (Pubitemid 37314396)
22. Wintrode, P. L., Zhang, D. Q., Vaidehi, N., Arnold, F. H., and Goddard, W. A. (2003) Protein dynamics in a family of laboratory evolved thermophilic enzymes J. Mol. Biol. 327, 745-757 (Pubitemid 36299076)
23. Arnold, F. H., Giver, L., Gershenson, A., Zhao, H., and Miyazaki, K. (1999) Directed evolution of mesophilic enzymes into their thermophilic counterparts Ann. N.Y. Acad. Sci. 870, 400-403 (Pubitemid 29349377)
24. Spiller, B., Gershenson, A., Arnold, F. H., and Stevens, R. C. (1999) A structural view of evolutionary divergence Proc. Natl. Acad. Sci. U.S.A. 96, 12305-12310 (Pubitemid 29513497)
25. Giver, L., Gershenson, A., Freskgard, P. O., and Arnold, F. H. (1998) Directed evolution of a thermostable esterase Proc. Natl. Acad. Sci. U.S.A. 95, 12809-12813 (Pubitemid 28509479)
26. Somero, G. N. (1978) Temperature adaptation of enzymes-biological optimization through structure-function compromises Ann. Rev. Ecol. Syst. 9, 1-29
27. Blakley, R. L. (1960) Crystalline dihydropteroylglutamic acid Nature 188, 231-232
28. Sours, K. M., Kwok, S. C., Rachidi, T., Lee, T., Ring, A., Hoofnagle, A. N., Resing, K. A., and Ahn, N. G. (2008) Hydrogen-exchange mass spectrometry reveals activation-induced changes in the conformational mobility of p38 alpha MAP kinase J. Mol. Biol. 379, 1075-1093
29. Resing, K. A., Hoofnagle, A. N., and Ahn, N. G. (1999) Modeling deuterium exchange behavior of ERK2 using pepsin mapping to probe secondary structure J. Am. Soc. Mass. Spectrom. 10, 685-702 (Pubitemid 34498692)
30. Hoofnagle, A. N., Resing, K. A., and Ahn, N. G. (2003) Protein analysis by hydrogen exchange mass spectrometry Annu. Rev. Biophys. Biomol. Struct. 32, 1-25 (Pubitemid 37056219)
31. Bai, Y., Milne, J. S., Mayne, L., and Englander, S. W. (1993) Primary structure effects on peptide group hydrogen exchange Proteins 17, 75-86 (Pubitemid 23261059)
32. Xu, D. and Zhang, Y. (2009) Generating triangulated macromolecular surfaces by Euclidean Distance Transform PLoS One 4, e8140
33. Yamamoto, T., Izumi, S., and Gekko, K. (2004) Mass spectrometry on segment-specific hydrogen exchange of dihydrofolate reductase J. Biochem. (Tokyo) 135, 17-24 (Pubitemid 38405157)
34. Liu, Y. H. and Konermann, L. (2006) Enzyme conformational dynamics during catalysis and in the 'resting state' monitored by hydrogen/deuterium exchange mass spectrometry FEBS Lett. 580, 5137-5142 (Pubitemid 44415783)
35. Schnell, J. R., Dyson, H. J., and Wright, P. E. (2004) Structure, dynamics, and catalytic function of dihydrofolate reductase Annu. Rev. Biophys. Biomol. Struct. 33, 119-140 (Pubitemid 38829954)
36. Bhabha, G., Lee, J., Ekiert, D. C., Gam, J., Wilson, I. A., Dyson, H. J., Benkovic, S. J., and Wright, P. E. (2011) A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis Science 332, 234-238
37. Liang, Z.-X., Tsigos, I., Lee, T., Bouriotis, V., Resing, K. A., Ahn, N. G., and Klinman, J. P. (2004) Evidence for increased local flexibility in psychrophilic alcohol dehydrogenase relative to its thermophilic homologue Biochemistry 43, 14676-14683 (Pubitemid 39524942)