Adaptive protein evolution grants organismal fitness by improving catalysis and flexibility

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

Volumn 105, Issue 52, 2008, Pages 20605-20610

  Tomatis, Pablo E ^a   Fabiane, Stella M ^b   Simona, Fabio ^c   Carloni, Paolo ^c   Sutton, Brian J ^b   Vila, Alejandro J ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c SISSA   (Italy)

Author keywords

Antibiotic resistance; Enzyme; Epistasis; Fitness landscape; Metalloproteins

Indexed keywords

METAL ION; METALLO BETA LACTAMASE;

ANTIBIOTIC RESISTANCE; ARTICLE; CATALYSIS; CONTROLLED STUDY; EPISTASIS; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY;

BACILLUS CEREUS; BACTERIAL PROTEINS; BETA-LACTAMASES; CATALYSIS; DIRECTED MOLECULAR EVOLUTION; DRUG RESISTANCE, BACTERIAL; ENZYME STABILITY; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; METALLOPROTEINS; MUTATION; PROTEIN STRUCTURE, TERTIARY;

EID: 58549106768     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0807989106     Document Type: Article

References (45)

1. Poelwijk FJ, Kiviet DJ, Weinreich DM, Tans SJ (2007) Empirical fitness landscapes reveal accessible evolutionary paths. Nature 445:383-386.
2. Depristo MA, Weinreich DM, Hartl DL (2005) Missense meanderings in sequence space: A biophysical view of protein evolution. Nat Rev Genet 6:678-687.
3. Bershtein S, Segal M, Bekerman R, Tokuriki N, Tawfik DS (2006) Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444:929-932.
4. Weinreich DM, Delaney NF, Depristo MA, Hartl DL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111-114.
5. Orencia MC, Yoon JS, Ness JE, Stemmer WP, Stevens RC (2001) Predicting the emergence of antibiotic resistance by directed evolution and structural analysis. Nat Struct Biol 8:238-242.
6. Benkovic SJ, Hammes-Schiffer S (2003) A perspective on enzyme catalysis. Science 301:1196-1202.
7. Lunzer M, Miller SP, Felsheim R, Dean AM (2005) The biochemical architecture of an ancient adaptive landscape. Science 310:499-501.
8. Zhu G, Golding GB, Dean AM (2005) The selective cause of an ancient adaptation. Science 307:1279-1282.
9. Hammes-Schiffer S, Benkovic SJ (2006) Relating protein motion to catalysis. Annu Rev Biochem 75:519-541.
10. Miller SP, Lunzer M, Dean AM (2006) Direct demonstration of an adaptive constraint. Science 314:458-461.
11. Dean AM, Thornton JW (2007) Mechanistic approaches to the study of evolution: The functional synthesis. Nat Rev Genet 8:675-688.
12. Ortlund EA, Bridgham JT, Redinbo MR, Thornton JW (2007) Crystal structure of an ancient protein: Evolution by conformational epistasis. Science 317:1544-1548.
13. Tomatis PE, Rasia RM, Segovia L, Vila AJ (2005) Mimicking natural evolution in metallo-beta-lactamases through second-shell ligand mutations. Proc Natl Acad Sci USA 102:13761-13766.
14. Fisher JF, Meroueh SO, Mobashery S (2005) Bacterial resistance to beta-lactam antibiotics: Compelling opportunism, compelling opportunity. Chem Rev 105:395-424.
15. Beadle BM, Shoichet BK (2002) Structural bases of stability-function tradeoffs in enzymes. J Mol Biol 321:285-296.
16. Sideraki V, Huang W, Palzkill T, Gilbert HF (2001) A secondary drug resistance mutation of TEM-1 beta-lactamase that suppresses misfolding and aggregation. Proc Natl Acad Sci USA 98:283-288.
17. Crowder MW, Spencer J, Vila AJ (2006) Metallo-beta-lactamases: Novel weaponry for antibiotic resistance in bacteria. Acc Chem Res 39:721-728.
18. Walsh TR, Toleman MA, Poirel L, Nordmann P (2005) Metallo-beta- lactamases: The quiet before the storm? Clin Microbiol Rev 18:306-325.
19. Rasia RM, Vila AJ (2002) Exploring the role and the binding affinity of a second zinc equivalent in B. cereus metallo-beta-lactamase. Biochemistry 41:1853-1860.
20. Fabiane SM, et al. (1998) Crystal structure of the zinc-dependent beta lactamase from Bacillus cereus at 1.9 A resolution: Binuclear active site with features of amononuclear enzime. Biochemistry 37:12404-12411.
21. Carfi A, et al. (1995) The 3-D structure of a zinc metallo-beta-lactamase from Bacillus cereus reveals a new type of protein fold. EMBO J 14:4914-4921.
22. Orellano EG, Girardini JE, Cricco JA, Ceccarelli EA, Vila AJ (1998) Spectroscopic characterization of a binuclear metal site in Bacillus cereus beta-lactamase II. Biochemistry 37:10173-10180.
23. Wang Z, Fast W, Benkovic SJ (1998) Direct observationof an enzime bound intermediate in the catalytic cycle of the metallo-beta-lactamase from Bacteroides fragilis. J Am Chem Soc 120:10788-10789.
24. Llarrull LI, et al. (2007) Asp-120 locates Zn2 for optimal metallo-beta-lactamase activity. J Biol Chem 282:18276-18285.
25. Gonzalez JM, Medrano Martin FJ, Costello AL, Tierney DL, Vila AJ (2007) The Zn2 position in metallo-beta-lactamases is critical for activity: A study on chimeric metal sites on a conserved protein scaffold. J Mol Biol 373:1141-1156.
26. Spencer J, et al. (2005) Antibiotic recognition by binuclear metallo-beta-lactamases revealed by X-ray crystallography. J Am Chem Soc 127:14439-14444.
27. Moran-Barrio J, et al. (2007) The metallo-beta-lactamase GOB is amono-Zn(II) enzyme with a novel active site. J Biol Chem 282:18286-18293.
28. 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.
29. Bloom JD, Labthavikul ST, Otey CR, Arnold FH (2006) Protein stability promotes evolvability. Proc Natl Acad Sci USA 103:5869-5874.
30. Oelschlaeger P, Mayo SL, Pleiss J (2005) Impact of remote mutations on metallo-beta-lactamase substrate specificity: Implications for the evolution of antibiotic resistance. Protein Sci 14:765-774.
31. Zeldovich KB, Chen P, Shakhnovich EI (2007) Protein stability imposes limits on organism complexity and speed of molecular evolution. Proc Natl Acad Sci USA 104:16152-16157.
32. Oelschlaeger P, Schmid RD, Pleiss J (2003) Modeling domino effects in enzymes: molecular basis of the substrate specificity of the bacterial metallo-beta-lactamases IMP-1 and IMP-6. Biochemistry 42:8945-8956.
33. Llarrull LI, Tioni MF, Vila AJ (2008) Metal content and localization during turnover in B. cereus metallo-β Lactamase. J Am Chem Soc 130:15842-15851.
34. Tioni MF, et al. (2008) Trapping and characterization of a reaction intermediate in carbapenem hydrolysis by B. cereus metallo-β-lactamase. J Am Chem Soc 130:15852-15863.
35. Sambrook J, Fitsch EF, Maniatis T (1989) Molecular Cloning. A Laboratory Manual (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY).
36. Barik S (1996) In Vitro Mutagenesis Protocols, ed Trower MK (Humana Press, Totowa, NJ), pp 203-215.
37. Paul-Soto R, et al. (1999) Mono- and binuclear Zn2+-beta-lactamase. Role of the conserved cysteine in the catalytic mechanism. J Biol Chem 274:13242-13249.
38. Hunt JB, Neece SH, Ginsburg A (1985) The use of 4-(2-pyridylazo) resorcinol in studies of zinc release from Escherichia coli aspartate transcarbamoylase. Anal Biochem 146:150-157.
39. Llarrull LI, Tioni MF, Kowalski J, Bennett B, Vila AJ (2007) Evidence for a dinuclear active site in the metallo-beta-lactamase BcII with substoichiometric Co(II). A new model for metal uptake. J Biol Chem 282:30586-30595.
40. Kuzmic P (1996) Program DYNAFIT for the analysis of enzyme kinetic data: Application to HIV proteinase. Anal Biochem 237:260-273.
41. Dal Peraro M, Vila AJ, Carloni P (2004) Substrate binding to mononuclear metallo-beta-lactamase from Bacillus cereus. Proteins 54:412-423.
42. Case DA, et al. (2002) AMBER 7 (University of California, San Francisco).
43. Jorgensen WL, Chandrasekhar J, Madura J, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926-935.
44. Wang JM, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general amber force field. J Comput Chem 25:1157-1174.
45. Darden T, York D, Pedersen L (1993) Particle mesh Ewald: An N.Log(N) method for Ewald sums in large systems. J Chem Phys 98:10089-10092.