Cofactor mobility determines reaction outcome in the IMPDH and GMPR ( 2- ±) 8 barrel enzymes

Nature Chemical Biology

Volumn 7, Issue 12, 2011, Pages 950-958

  Patton, Gregory C ^a   Stenmark, Päl ^b,c   Gollapalli, Deviprasad R ^a   Sevastik, Robin ^d   Kursula, Petri ^b,g   Flodin, Susanne ^b   Schuler, Herwig ^b   Swales, Colin T ^a   Eklund, Hans ^e   Himo, Fahmi ^d   Nordlund, Par ^b,f   Hedstrom, Lizbeth ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c STOCKHOLM UNIVERSITY   (Sweden)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^f NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^g UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; GUANOSINE PHOSPHATE; GUANOSINE PHOSPHATE REDUCTASE; GUANOSINE PHOSPHATE REDUCTASE 2; INOSINATE DEHYDROGENASE; INOSINE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; WATER;

ARTICLE; BINDING SITE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME CONFORMATION; ENZYME STRUCTURE; MUTAGENESIS; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PROTEIN CONFORMATION; REACTION ANALYSIS;

EID: 81355146320     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.693     Document Type: Article

References (50)

1. Glasner, M.E., Gerlt, J.A. & Babbitt, P.C. Evolution of enzyme superfamilies. Curr. Opin. Chem. Biol. 10, 492-497 (2006). (Pubitemid 44375064)
2. Soskine, M. & Tawfik, D.S. Mutational effects and the evolution of new protein functions. Nat. Rev. Genet. 11, 572-582 (2010).
3. Zalatan, J.G. & Herschlag, D. The far reaches of enzymology. Nat. Chem. Biol. 5, 516-520 (2009).
4. Nagano, N., Orengo, C.A. & Thornton, J.M. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 321, 741-765 (2002).
5. Gerlt, J.A. & Raushel, F.M. Evolution of function in (?/?)8-barrel enzymes. Curr. Opin. Chem. Biol. 7, 252-264 (2003).
6. Wise, E.L. & Rayment, I. Understanding the importance of protein structure to nature's routes for divergent evolution in TIM barrel enzymes. Acc. Chem. Res. 37, 149-158 (2004).
7. Lo Conte, L., Brenner, S.E., Hubbard, T.J., Chothia, C. & Murzin, A.G. SCOP database in 2002: refinements accommodate structural genomics. Nucleic Acids Res. 30, 264-267 (2002). (Pubitemid 34679560)
8. Orengo, C.A. et al. CATH-a hierarchic classification of protein domain structures. Structure 5, 1093-1108 (1997). (Pubitemid 27393093)
9. Anantharaman, V., Aravind, L. & Koonin, E.V. Emergence of diverse Biochemical activities in evolutionarily conserved structural scaffolds of proteins. Curr. Opin. Chem. Biol. 7, 12-20 (2003). (Pubitemid 36126487)
10. Taylor, J.S. & Raes, J. Duplication and divergence: the evolution of new genes and old ideas. Annu. Rev. Genet. 38, 615-643 (2004). (Pubitemid 40017189)
11. Bergthorsson, U., Andersson, D.I. & Roth, J.R. Ohno's dilemma: evolution of new genes under continuous selection. Proc. Natl. Acad. Sci. USA 104, 17004-17009 (2007). (Pubitemid 350210980)
12. Conant, G.C. & Wolfe, K.H. Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 9, 938-950 (2008). (Pubitemid 352719432)
13. Innan, H. & Kondrashov, F. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11, 97-108 (2010).
14. Khersonsky, O. & Tawfik, D.S. Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu. Rev. Biochem. 79, 471-505 (2010).
15. Hedstrom, L. IMP dehydrogenase: structure, mechanism and inhibition. Chem. Rev. 109, 2903-2928 (2009).
16. Weber, G., Nakamura, H., Natsumeda, Y., Szekeres, T. & Nagai, M. Regulation of GTP biosynthesis. Adv. Enzyme Regul. 32, 57-69 (1992).
17. Gan, L., Petsko, G.A. & Hedstrom, L. Crystal structure of a ternary complex of Tritrichomonas foetus inosine 5?-monophosphate dehydrogenase: NAD+ orients the active site loop for catalysis. Biochemistry 41, 13309-13317 (2002). (Pubitemid 35244721)
18. Prosise, G.L. & Luecke, H. Crystal structures of Tritrichomonas foetus inosine monophosphate dehydrogenase in complex with substrate, cofactor and analogs: a structural basis for the random-in ordered-out kinetic mechanism. J. Mol. Biol. 326, 517-527 (2003). (Pubitemid 36279345)
19. Colby, T.D., Vanderveen, K., Strickler, M.D., Markham, G.D. & Goldstein, B.M. Crystal structure of human type II inosine monophosphate dehydrogenase: implications for ligand binding and drug design. Proc. Natl. Acad. Sci. USA 96, 3531-3536 (1999). (Pubitemid 29168943)
20. Riera, T.V., Wang, W., Josephine, H.R. & Hedstrom, L. A kinetic alignment of orthologous inosine-5?-monophosphate dehydrogenases. Biochemistry 47, 8689-8696 (2008).
21. Gan, L. et al. The immunosuppressive agent mizoribine monophosphate forms a transition state analog complex with IMP dehydrogenase. Biochemistry 42, 857-863 (2003). (Pubitemid 36159515)
22. Guillén Schlippe, Y.V., Riera, T.V., Seyedsayamdost, M.R. & Hedstrom, L. Substitution of the conserved Arg-Tyr dyad selectively disrupts the hydrolysis phase of the IMP dehydrogenase reaction. Biochemistry 43, 4511-4521 (2004). (Pubitemid 38500580)
23. Guillén Schlippe, Y.V. & Hedstrom, L. Is Arg418 the catalytic base required for the hydrolysis step of the IMP dehydrogenase reaction? Biochemistry 44, 11700-11707 (2005). (Pubitemid 41262703)
24. Min, D. et al. An enzymatic atavist revealed in dual pathways for water activation. PLoS Biol. 6, e206 (2008).
25. Li, J. et al. Crystal structure of human guanosine monophosphate reductase 2 (GMPR2) in complex with GMP. J. Mol. Biol. 355, 980-988 (2006). (Pubitemid 43012141)
26. Spector, T., Jones, T.E. & Miller, R.L. Reaction mechanism and specificity of human GMP reductase. Substrates, inhibitors, activators, and inactivators. J. Biol. Chem. 254, 2308-2315 (1979). (Pubitemid 9160046)
27. Deng, Y. et al. NADPH-dependent GMP reductase isoenzyme of human (GMPR2). Expression, purification, and kinetic properties. Int. J. Biochem. Cell Biol. 34, 1035-1050 (2002). (Pubitemid 34495453)
28. Martinelli, L.K. et al. Recombinant Escherichia coli GMP reductase: kinetic, catalytic and chemical mechanisms, and thermodynamics of enzyme-ligand binary complex formation. Mol. Biosyst. 7, 1289-1305 (2011).
29. Bellamacina, C.R. The nicotinamide dinucleotide binding motif: a comparison of nucleotide binding proteins. FASEB J. 10, 1257-1269 (1996). (Pubitemid 26307511)
30. Hughes, R., Magee, E.A. & Bingham, S. Protein degradation in the large intestine: relevance to colorectal cancer. Curr. Issues Intest. Microbiol. 1, 51-58 (2000).
31. Roberts, R.E., Lienhard, C.I., Gaines, C.G., Smith, J.M. & Guest, J.R. Genetic and molecular characterization of the guaC-nadC-aroP region of Escherichia coli K-12. J. Bacteriol. 170, 463-467 (1988).
32. Macpherson, I.S. et al. The structural basis of Cryptosporidium-specific IMP dehydrogenase inhibitor selectivity. J. Am. Chem. Soc. 132, 1230-1231 (2010).
33. Talfournier, F., Pailot, A., Stines-Chaumeil, C. & Branlant, G. Stabilization and conformational isomerization of the cofactor during the catalysis in hydrolytic ALDHs. Chem. Biol. Interact. 178, 79-83 (2009).
34. Minegishi, S. & Mayr, H. How constant are Ritchie?s "constant selectivity relationships"? A general reactivity scale for n-, pi-, and sigma-nucleophiles. J. Am. Chem. Soc. 125, 286-295 (2003). (Pubitemid 36068665)
35. Musa-Aziz, R., Chen, L.M., Pelletier, M.F. & Boron, W.F. Relative CO2/NH3 selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG. Proc. Natl. Acad. Sci. USA 106, 5406-5411 (2009).
36. Ji, R. & Brune, A. Nitrogen mineralization, ammonia accumulation, and emission of gaseous NH3 by soil-feeding termites. Biogeochemistry 78, 267-283 (2006). (Pubitemid 43893884)
37. van Ham, R.C. et al. Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. USA 100, 581-586 (2003). (Pubitemid 36126095)
38. Hansen, A.K. & Moran, N.A. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc. Natl. Acad. Sci. USA 108, 2849-2854 (2011).
39. Zahnle, K., Schaefer, L. & Fegley, B. Earth's earliest atmospheres. Cold Spring Harb. Perspect. Biol. 2, a004895 (2010).
40. Kim, H.S., Mittenthal, J.E. & Caetano-Anolles, G. MANET: tracing evolution of protein architecture in metabolic networks. BMC Bioinformatics 7, 351 (2006).
41. Zhang, R. et al. Differential signatures of bacterial and mammalian IMP dehydrogenase enzymes. Curr. Med. Chem. 6, 537-543 (1999). (Pubitemid 29327999)
42. Leslie, A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 and ESF-EAMCB Newsl. Protein Crystallogr. 26, (1992).
43. Kabsch, W. Evaluation of single-crystal X-ray diffraction data from a position-sensitive detector. J. Appl. Crystallogr. 21, 916-924 (1988).
44. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997). (Pubitemid 27235885)
45. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
46. Chen, V.B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
47. Frisch, M.J. et al. Gaussian 03, Revision C.02. (ed. Gaussian, I.) (2004).
48. Brady, K. & Abeles, R.H. Inhibition of chymotrypsin by peptidyl trifluoromethyl ketones: determinants of slow-binding kinetics. Biochemistry 29, 7608-7617 (1990). (Pubitemid 20279177)
49. Zhang, R. et al. Characteristics and crystal structure of bacterial inosine- 5?-monophosphate dehydrogenase. Biochemistry 38, 4691-4700 (1999).
50. Pettersen, E.F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).