HIV-1 protease catalytic efficiency effects caused by random single amino acid substitutions

Molecular Biology and Evolution

Volumn 24, Issue 2, 2007, Pages 382-387

  Parera, Mariona ^a   Fernàndez, Guerau ^a   Clotet, Bonaventura ^a   Martínez, Miguel Angel ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Epistasis; Protein evolution; Robustness

Indexed keywords

AMINO ACID; PROTEINASE; VIRUS ENZYME;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; EPISTAXIS; HUMAN IMMUNODEFICIENCY VIRUS 1; LETHAL MUTANT; MUTAGENESIS; NONHUMAN; WILD TYPE;

AMINO ACID SUBSTITUTION; CATALYSIS; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; GENE LIBRARY; HIV PROTEASE; HIV-1; MUTATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33846829804     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msl168     Document Type: Article

References (42)

1. Aharoni A, Gaidukov L, Khersonsky O, Gould SM, Roodveldt C, Tawfik DS. 2005. The 'evolvability' of promiscuous protein functions. Nat Genet. 37:73-76.
2. Bloom JD, Drummond DA, Arnold FH, Wilke CO. 2006. Structural determinants of the rate of protein evolution in yeast. Mol Biol Evol. 23:1751-1761.
3. Bloom JD, Labthavikul ST, Otey CR, Arnold FH. 2006. Protein stability promotes evolvability. Proc Natl Acad Sci USA. 103:5869-5874.
4. Bloom JD, Silberg JJ, Wilke CO, Drummond DA, Adami C, Arnold FH. 2005. Thermodynamic prediction of protein neutrality. Proc Natl Acad Sci USA. 102:606-611.
5. Bonhoeffer S, Chappey C, Parkin NT, Whitcomb JM, Petropoulos CJ. 2004. Evidence for positive epistasis in HIV-1. Science. 306:1547-1550.
6. Bridgham JT, Carroll SM, Thornton JW. 2006. Evolution of hormone-receptor complexity by molecular exploitation. Science. 312:97-101.
7. Burch CL, Chao L. 2004. Epistasis and its relationship to canalization in the RNA virus phi 6. Genetics. 167:559-567.
8. Cabana M, Fernandez G, Parera M, Clotet B, Martinez MA. 2002. Catalytic efficiency and phenotype of HIV-1 proteases encoding single critical resistance substitutions. Virology. 300:71-78.
9. Ceccherini-Silberstein F, Erba F, Gago F, et al. (13 co-authors). 2004. Identification of the minimal conserved structure of HIV-1 protease in the presence and absence of drug pressure. Aids. 18:F11-F19.
10. Condra JH, Schleif WA, Blahy OM, et al. (16 co-authors). 1995. In vivo emergence of HIV-1 variants resistant to multiple protease inhibitors. Nature. 374:569-571.
11. Domingo E, Menendez-Arias L, Quinones-Mateu ME, Holguin A, Gutierrez-Rivas M, Martinez MA, Quer J, Novella IS, Holland JJ. 1997. Viral quasispecies and the problem of vaccine-escape and drug-resistant mutants. Prog Drug Res. 48:99-128.
12. Elena SF, Carrasco P, Daros JA, Sanjuan R. 2006. Mechanisms of genetic robustness in RNA viruses. EMBO Rep. 7:168-173.
13. Guo HH, Choe J, Loeb LA. 2004. Protein tolerance to random amino acid change. Proc Natl Acad Sci USA. 101:9205-9210.
14. Ishima R, Ghirlando R, Tozser J, Gronenborn AM, Torchia DA, Louis JM. 2001. Folded monomer of HIV-1 protease. J Biol Chem. 276:49110-49116.
15. Johnson VA, Brun-Vezinet F, Clotet B, Conway B, Kuritzkes DR, Pillay D, Schapiro JM, Telenti A, Richman DD. 2005. Update of the drug resistance mutations in HIV-1: Fall 2005. Top HIV Med. 13:125-131.
16. Lenski RE, Ofria C, Pennock RT, Adami C. 2003. The evolutionary origin of complex features. Nature. 423:139-144.
17. Loeb DD, Swanstrom R, Everitt L, Manchester M, Stamper SE, Hutchison CA 3rd. 1989. Complete mutagenesis of the HIV-1 protease. Nature. 340:397-400.
18. Maisnier-Patin S, Berg OG, Liljas L, Andersson DI. 2002. Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol Microbiol. 46:355-366.
19. Mammano F, Trouplin V, Zennou V, Clavel F. 2000. Retracing the evolutionary pathways of human immunodeficiency virus type1 resistance to protease inhibitors: virus fitness in the absence and in the presence of drug. J Virol. 74:8524-8531.
20. Markiewicz P, Kleina LG, Cruz C, Ehret S, Miller JH. 1994. Genetic studies of the lac repressor. XIV. Analysis of 4000 altered Escherichia coli lac repressors reveals essential and non-essential residues, as well as "spacers" which do not require a specific sequence. J Mol Biol. 240:421-433.
21. Martinez MA, Cabana M, Parera M, Gutierrez A, Este JA, Clotet B. 2000. A bacteriophage lambda-based genetic screen for characterization of the activity and phenotype of the human immunodeficiency virus type 1 protease. Antimicrob Agents Chemother. 44:1132-1139.
22. Martinez MA, Clotet B. 2003. Genetic screen for monitoring hepatitis C virus NS3 serine protease activity. Antimicrob Agents Chemother. 47:1760-1765.
23. Martinez MA, Pezo V, Marliere P, Wain-Hobson S. 1996. Exploring the functional robustness of an enzyme by in vitro evolution. EMBO J. 15:1203-1210.
24. Martinez-Picado J, Savara AV, Sutton L, D'Aquila RT. 1999. Replicative fitness of protease inhibitor-resistant mutants of human immunodeficiency virus type 1. J Virol. 73:3744-3752.
25. Nijhuis M, Schuurman R, de Jong D, Erickson J, Gustchina E, Albert J, Schipper P, Gulnik S, Boucher CA. 1999. Increased fitness of drug resistant HIV-1 protease as a result of acquisition of compensatory mutations during suboptimal therapy. Aids. 13:2349-2359.
26. Pal C, Papp B, Lercher MJ. 2006. An integrated view of protein evolution. Nat Rev Genet. 7:337-348.
27. Parera M, Clotet B, Martinez MA. 2004. Genetic screen for monitoring severe acute respiratory syndrome coronavirus 3C-like protease. J Virol. 78:14057-14061.
28. Patick AK, Duran M, Cao Y, Shugarts D, Keller MR, Mazabel E, Knowles M, Chapman S, Kuritzkes DR, Markowitz M. 1998. Genotypic and phenotypic characterization of human immunodeficiency virus type 1 variants isolated from patients treated with the protease inhibitor nelfinavir. Antimicrob Agents Chemother. 42:2637-2644.
29. Phillips P, Otto S, Whitlock M. 2000. Beyond the average: the evolutionary importance of gene interactions and variability of epistatic effects. In: Wolf J, Brodie E, Wade M, editors. Epistasis and the evolutionary process. Oxford: Oxford University Press. p. 20-38.
30. Rao JK, Erickson JW, Wlodawer A. 1991. Structural and evolutionary relationships between retroviral and eucaryotic aspartic proteinases. Biochemistry. 30:4663-4671.
31. Rennell D, Bouvier SE, Hardy LW, Poteete AR. 1991. Systematic mutation of bacteriophage T4 lysozyme. J Mol Biol. 222:67-88.
32. Sanjuan R, Elena SF. 2006. Epistasis correlates to genomic complexity. Proc Natl Acad Sci USA. 103:14402-14405.
33. Sanjuan R, Moya A, Elena SF. 2004. The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci USA. 101:15376-15379.
34. Sices HJ, Kristie TM. 1998. A genetic screen for the isolation and characterization of site-specific proteases. Proc Natl Acad Sci USA. 95:2828-2833.
35. Smith JM. 1970. Natural selection and the concept of a protein space. Nature. 225:563-564.
36. Taverna DM, Goldstein RA. 2002. Why are proteins so robust to site mutations? J Mol Biol. 315:479-484.
37. Vartanian JP, Henry M, Wain-Hobson S. 1996. Hypermutagenic PCR involving all four transitions and a sizeable proportion of transversions. Nucleic Acids Res. 24:2627-2631.
38. Wagner A. 2005. Robustness, evolvability, and neutrality. Febs Lett. 579:1772-1778.
39. Wilke CO, Adami C. 2003. Evolution of mutational robustness. Mutat Res. 522:3-11.
40. Wilke CO, Bloom JD, Drummond DA, Raval A. 2005. Predicting the tolerance of proteins to random amino acid substitution. Biophys J. 89:3714-3720.
41. Wilke CO, Lenski RE, Adami C. 2003. Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol Biol. 3:3.
42. Wu TD, Schiffer CA, Gonzales MJ, Taylor J, Kantor R, Chou S, Israelski D, Zolopa AR, Fessel WJ, Shafer RW. 2003. Mutation patterns and structural correlates in human immunodeficiency virus type 1 protease following different protease inhibitor treatments. J Virol. 77:4836-4847.