Correlated Electrostatic Mutations Provide a Reservoir of Stability in HIV Protease

PLoS Computational Biology

Volumn 8, Issue 9, 2012, Pages

  Haq, Omar ^a   Andrec, Michael ^a,b   Morozov, Alexandre V ^a,b   Levy, Ronald M ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COARSE-GRAINED MODELING; DISEASES; ELECTROSTATICS; ENZYMES; SAMPLING; VIRUSES;

ASPARTYL PROTEASE; COARSE-GRAINED; DEVELOPMENT PROGRAMMES; DRUG DEVELOPMENT; DRUG-RESISTANCE; ENERGY MODEL; HIV-PROTEASE; LOSS OF STABILITY; PROTEASE INHIBITOR; STATISTICAL INFERENCE;

STABILITY;

PROTEINASE;

ANTIVIRAL RESISTANCE; ARTICLE; BIOPHYSICS; CORRELATION ANALYSIS; ENZYME STABILITY; HUMAN IMMUNODEFICIENCY VIRUS; MOLECULAR MODEL; PREDICTION; PROTEIN INTERACTION; SAMPLE SIZE; STATIC ELECTRICITY; STATISTICAL ANALYSIS; STATISTICAL PARAMETERS; STATISTICAL SIGNIFICANCE; VIRUS MUTANT; VIRUS MUTATION;

EID: 84866913347     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002675     Document Type: Article

References (67)

1. Depristo MA, Weinreich DM, Hartl DL, (2005) Missense meanderings in sequence space: A bio-physical view of protein evolution. Nature 6: 678-687.
2. Pace CN, (1975) The stability of globular proteins. CRC Crit Rev Biochem 3: 1-43.
3. Pain R, (1987) Temperature and macromolecular structure and function. Symp Soc Exp Biol 41: 21-33.
4. Shoichet BK, Baase WA, Kuroki R, Matthews BW, (1995) A relationship between protein stability and protein function. Proc Natl Acad Sci U S A 92: 452-456.
5. Bloom JD, Labthavikul ST, Otey CR, Arnold FH, (2006) Protein Stability promotes Evolvability. Proc Natl Acad Sci U S A 103: 5869-5874.
6. Tokuriki N, Tawfik DS, (2009) Stability effects of mutations and protein evolvability. Curr Opin Struct Biol 19: 596-604.
7. Chang MW, Torbett BE, (2011) Accessory mutations maintain stability in drug-resistant HIV-1 protease. J Mol Bio 410: 756-760.
8. Lindquist S, (2009) Protein folding sculpting evolutionary change. Cold Spring Harb Symp Quant Biol 74: 103-108.
9. Zeldovich KB, Chen P, Shakhnovich EI, (2007) Protein stability imposes limits on organism com-plexity and speed of molecular evolution. Proc Natl Acad Sci U S A 104: 16152-16157.
10. Tokuriki N, Stricher F, Serrano L, Tawfik DS, (2008) How protein stability and new functions trade off. PLoS Comput Biol 4: e1000002.
11. Bloom JD, Gong LI, Baltimore D, (2010) Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328: 1272-1275.
12. Gobel U, Sander C, Schneider R, Valencia A, (1994) Correlated mutations and residue contacts in proteins. Proteins 18: 309-317.
13. Codoner FM, Fares MA, (2008) Why should we care about molecular coevolution. Evol Bioinform Online 4: 29-38.
14. Chen L, Lee C, (2006) Distinguishing HIV-1 drug resistance, accessory, and viral fitness mutations using conditional selection pressure analysis of treated versus untreated patient samples. Biol Direct 1: 14.
15. Rhee SY, Liu TF, Holms SP, Shafer RW, (2007) HIV-1 subtype B protease and reverse transcriptase amino acid covariation. PLoS Comput Biol 3: 0836-0843.
16. Liu Y, Eyal E, Bahar I, (2008) Analysis of correlated mutations in HIV-1 protease using spectral clustering. Bioinformatics 24: 1243-1250.
17. Haq O, Levy RM, Morozov AV, Andrec M, (2009) Pairwise and higher-order correlations among drug-resistance mutations in HIV-1 subtype B protease. BMC Bioinformatics 10: S10.
18. 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.
19. Zhang J, Hou T, Wang W, Liua JS, (2010) Detecting and understanding combinatorial mutation patterns responsible for hiv drug resistance. Proc Natl Acad Sci USA.
20. Lockless SW, Ranganathan R, (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286: 295-299.
21. Chi CN, Elfstrom L, Shi Y, Snall T, Engstrom A, et al. (2008) Reassessing a sparse energetic network within a single protein domain. Proc Natl Acad Sci U S A 105: 4679-4684.
22. Fodor AA, Aldrich RW, (2004) Influence of conservation on calculations of amino acid covariance in multiple sequence alignments. Proteins 56: 211-221.
23. Liu Z, Chen K, Thirumalai D, (2009) On the accuracy of inferring energetic coupling between distant sites in protein families from evolutionary imprints: Illustrations using lattice model. Proteins 77: 823-831.
24. Atchley WR, Wollenberg KR, Fitch WM, Terhalle W, Dress AW, (2000) Correlations among amino acid sites in bhlh protein domains: An information theoretic analysis. Mol Biol Evol 17: 164-178.
25. Olmea O, Rost B, Valencia A, (1999) Effective use of sequence correlation and conservation in fold recognition. J Mol Biol 295: 1221-1239.
26. Rost B, Sander C, (1994) Structure prediction of proteins- where are we now? Curr Biol 5: 372-380.
27. Potapov V, Cohen M, Schreiber G, (2009) Assessing computational methods for predicting protein stability upon mutation: good on average but not in the details. Protein Eng Des Sel 22: 553-560.
28. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG, (1995) Funnels, pathways, and the energy landscape of protein folding: A synthesis. Proteins 21: 167-195.
29. Onuchic JN, Wolynes PG, (2004) Theory of protein folding. Curr Opin Struct Biol 14: 70-75.
30. Chen L, Perlina A, Lee C, (2004) Positive selection detection in 40,000 human immunodeficiency virus (HIV) type 1 sequences automatically identifies drug resistance and positive fitness mutations in HIV protease and reverse transcriptase. J Virol 78: 3722-3732.
31. Rhee SY, Gonzales MJ, Kantor R, Betts BJ, Ravela J, et al. (2003) Human immunodeficiency virus reverse transcriptase and protease sequence database. Nucl Acids Res 31: 298-303.
32. Mahalingam B, Boross P, Wang YF, Louis JM, Fischer CC, et al. (2002) Combining mutations in HIV-1 protease to understand mechanisms of resistance. Protein 48: 107-116.
33. Todd MJ, Luque I, Velazquez-Campoy A, Freire E, (2000) Thermodynamic basis of resistance to HIV-1 protease inhibition: Calorimetric analysis of the V82F/I84V active site resistant mutant. Biochem 39: 11876-11883.
34. Wu TD, Schiffer CA, Gonzales MJ, Taylor J, Kantor R, et al. (2003) Mutation patterns and structural correlates in human immunodeficiency virus type 1 protease following different protease inhibitor treatments. J Virol 77: 4836-4847.
35. Frey KM, Georgiev I, Donald BR, Anderson AC, (2010) Predicting resistance mutations using protein design algorithms. Proc Natl Acad Sci U S A 107: 13707-13712.
36. Safi M, Lilien RH, (2012) Efficient a priori identification of drug resistant mutations using dead-end elimination and mm-pbsa. J Chem Inf Model 52: 1529-1541.
37. Pearl J, (1988) Probabilistic Reasoning in Intelligent Systems: Networks of Plausible Inference. Morgan Kaufmann.
38. Yedidia JS, Freeman WT, Weiss Y (2000) Generalized belief propagation. In: NIPS 13. Leen TK, Dietterich TG, Tresp V.
39. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T, (2009) Identification of direct residue contacts in protein-protein interaction by message passing. Proc Natl Acad Sci U S A 106: 67-72.
40. Kamisetty H, Ramanathan A, Bailey-Kellogg C, Langmead CJ, (2011) Accounting for conforma-tional entropy in predicting binding free energies of protein-protein interactions. Proteins 79: 444-462.
41. Procaccini A, Lunt B, Szurmant H, Hwa T, Weigt M, (2011) Dissecting the specificity of protein-protein interaction in bacterial two-component signaling: Orphans and crosstalks. PLoS ONE 6: e19729.
42. Bethe HA, (1935) Statistical Theory of Superlattices. Proc Roy Soc London 150: 552.
43. Nishimori H (1999) Statistical Physics of Spin Glasses and Information Processing. Oxford Science Publications.
44. Murphy KP, Weiss Y, Jordan MI (1999) Loopy belief propagation for approximate inference: An empirical study. In: Proceedings of the Fifteenth Conference on Uncertainty in AI.
45. Yedidia JS, Freeman WT, Weiss Y, (2005) Constructing free energy approximations and generalized belief propagation algorithms. IEEE Trans Inf Theory 51: 2282-2313.
46. Morcos F, Pagnani A, Lunt B, Bertolino A, Marks DS, et al. (2011) Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc Natl Acad Sci U S A 108: E1293-E1301.
47. Hendsch ZS, Tidor B, (1994) Do salt bridges stabilize proteins? a continuum electrostatic analysis. Protein Sci 3: 211-226.
48. Szeltner Z, Polgar L, (1996) Conformational stability and catalytic activity of HIV-1 protease are both enhanced at high salt concentration. J Biol Chem 271: 5458-5463.
49. Dao-Pin S, Sauer U, Nicholson H, Matthews BW, (1991) Contributions of engineered surface salt bridges to the stability of T4 lysozme determined by directed mutagenesis. Biochem 30: 7142-7153.
50. Xiao L, Honig B, (1999) Electrostatic contributions to the stability of hyperthermophilic proteins. J Mol Biol 289: 1435-1444.
51. Hendsch ZS, Jonsson T, Sauer RT, Tidor B, (1996) Protein stabilization by removal of unsatisfied polar groups: computational approaches and experimental tests. Biochem 35: 7621-7625.
52. Honig B, Nicholls A, (1995) Classical electrostatics in biology and chemistry. Science 268: 1144-1149.
53. Elcock AH, (1998) The stability of salt bridges at high temperatures: implications for hyperther-mophilic proteins. J Mol Biol 284: 489-502.
54. Piana S, Carloni P, Rothlisberger U, (2002) Drug resistance in HIV-1 protease: Flexibility-assisted mechanism of compensatory mutations. Protein Sci 11: 2393-2402.
55. Schneider JP, Lear JD, DeGrado WF, (1997) A designed buried salt bridge in a heterodimeric coiled coil. J Am Chem Soc 119: 5742-5743.
56. Sindelar CV, Hendsch ZS, Tidor B, (1998) Effects of salt bridges on protein structure and design. Protein Sci 7: 1898-1914.
57. Dill KA, (1990) Dominant forces in protein folding. Biochem 29: 7133-7155.
58. Matthews BW, (1993) Structural and genetic analysis of protein stability. Annu Rev Biochem 62: 139-160.
59. Roca M, Messer B, Warshel A, (2007) Electrostatic contributions to protein stability and folding energy. FEBS Lett 581: 2065-2071.
60. Kuhlman B, Baker D, (2000) Native protein sequences are close to optimal for their structures. Proc Natl Acad Sci U S A 19: 10383-10388.
61. Onuchic JN, Luthey-Schulten Z, Wolynes PG, (1997) Theory of Protein Folding: The energy land-scape perspective. Annu Rev Phys Chem 48: 545-600.
62. Baker D, (2000) A surprising simplicity to protein folding. Nature 405: 39-42.
63. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG, (2004) Funnels, pathways, and the energy landscape of protein folding: A synthesis. Proteins 21: 167-195.
64. Balakrishnan S, Kamisetty H, Carbonell JG, Lee SI, Langmead CJ, (2011) Learning generative models for protein fold families. Proteins 79: 1061-1078.
65. Gallicchio E, Levy RM, (2004) AGBNP: An analytic impicit solvent model suitable for molecular dynamics simulations and high-resolution modeling. J Comput Chem 25: 479-499.
66. Sheridan RP, Levy RM, Salemme FR, (1982) Alpha-helix dipole model and electrostatic stabiliza-tion of 4-alpha-helical proteins. Proc Natl Acad Sci U S A 79: 4545-4549.
67. Jaynes ET, (1982) On the rationale of maximum-entropy methods. Proc IEEE 70: 939-952.