The utility of protein structure as a predictor of site-wise dN/dS varies widely among HIV-1 proteins

Journal of the Royal Society Interface

Volumn 12, Issue 111, 2015, Pages

  Meyer, Austin G ^a,b   Wilke, Claus O ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

DN dS; HIV; Molecular evolution; Proteins; Viruses

Indexed keywords

BINDING SITES; COMPUTER VIRUSES; DISEASES; ENZYMES; MOLECULAR BIOLOGY; VIRUSES;

DN/DS; GENERAL CONSTRAINTS; GLYCOSYLATION SITES; HIV; MOLECULAR EVOLUTION; SOLVENT ACCESSIBILITY; STRUCTURAL CONSTRAINTS; STRUCTURAL PROTEINS;

PROTEINS;

CAPSID PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS 1 PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; INTEGRASE; PROTEINASE; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; VIRUS SPIKE PROTEIN; CODON; GLYCOPROTEIN GP 120; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN BINDING; SOLVENT;

AMINO ACID SEQUENCE; ARTICLE; ENZYME ACTIVE SITE; EVOLUTIONARY RATE; GLYCOSYLATION; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; PURIFYING SELECTION; RECEPTOR BINDING; VIRUS CAPSID; BIOLOGY; CHEMISTRY; CODON; COMPUTER SIMULATION; GENETIC VARIATION; GENETICS; MOLECULAR EVOLUTION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; REGRESSION ANALYSIS;

CAPSID; CODON; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; EVOLUTION, MOLECULAR; GENETIC VARIATION; GLYCOSYLATION; HIV ENVELOPE PROTEIN GP120; HIV-1; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; REGRESSION ANALYSIS; SOLVENTS;

EID: 84945970225     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2015.0579     Document Type: Article

References (53)

1. Mansky LM, Temin HM. 1995 Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J. Virol. 69, 5087-5094.
2. Frost SD et al. 2005 Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc. Natl Acad. Sci. USA 102, 18 514-18 519. (doi:10.1073/pnas.0504658102)
3. Wei X et al. 1995 Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373, 117-122. (doi:10.1038/373117a0)
4. Wei X et al. 2002 Antibody neutralization and escape by HIV-1. Nature 422, 307-312. (doi:10.1038/nature01470)
5. Perelson AS, Neumann All, Markowitz M, Leonard JM, Ho DD. 1996 HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271,1582-1586. (doi:10.1126/science.271.5255.1582)
6. Perelson AS, Essunger P, Cao Y, Vesanen M, Hurley A, Saksela K, Markowitz M, Ho DD. 1997 Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387,188-191. (doi:10.1038/387188a0)
7. Chun TW et al. 1997 Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387, 183-188. (doi:10.1038/387183a0)
8. Franzosa EA, Xia Y. 2009 Structural determinants of protein evolution are context-sensitive at the residue level. Mol. Biol. Evol. 26, 2387-2395. (doi:10.1093J. Molbev/msp146)
9. Scherrer MP, Meyer AG, Wilke CO. 2012 Modeling coding-sequence evolution within the context of residue solvent accessibility. BMC Evol. Biol. 12,179. (doi :10.1186/1471-2148-12-179)
10. Bustamante CD, Townsend JP, Haiti DL. 2000 Solvent accessibility and purifying selection within proteins of Escherichia coli and Salmonella enterica. Mol. Biol. Evol. 17, 301-308. (doi:10.1093/oxfordjournals.molbev.a026310)
11. Shahmoradi A, Sydykova DK, Spielman SJ, Jackson EL, Dawson ET, Meyer AG, Wilke CO. 2014 Predicting evolutionary site variability from structure in viral proteins: buriedness, packing, flexibility, and design. J. Mol. Evol. 79, 130-142. (doi:10.1007/s00239-014-9644-x)
12. Yeh SW, Liu JW, Yu SH, Shih CH, Hwang JK, Echave J. 2014 Site-specific structural constraints on protein sequence evolutionary divergence: local packing density versus solvent exposure. Mol. Biol. Evol. 31, 135-139. (doi:10.1093J.Molbev/mstl78)
13. Echave J, Jackson EL, Wilke CO. 2014 Relationship between protein thermodynamic constraints and variation of evolutionary rates among sites. Phys. Biol. 12, 025002. (doi:10.1088/1478-3975/12/2/025002)
14. Marcos M, Echave J. 2015 Too packed to change: side-chain packing and site-specific substitution rates in protein evolution. PeerJ 3, e911. (doi:10. 7717/peerj.911)
15. Huang TT, Marcos ML, Hwang JK, Echave J. 2014 A mechanistic stress mode1of protein evolution accounts for site-specific evolutionary rates and their relationship with packing density and flexibility. BMC Evol. Biol. 14, 78. (doi:10.1186/1471-2148-14-78)
16. Sikosek T, Chan HS. 2014 Biophysics of protein evolution and evolutionary protein biophysics. J. R. Soc. Interface 11, 20140419. (doi:10.1098/rsif.2014.0419)
17. Meyer AG, Wilke CO. 2013 Integrating sequence variation and protein structure to identify sites under selection. Mol. Biol. Evol. 30, 36-44. (doi:10.1093J. Molbev/mss217)
18. Meyer AG, Wilke CO. 2015 Geometric constraints dominate the antigenic evolution of influenza H3N2 hemagglutinin. PLoS Pathog. 11, e1004940. (doi:10.1371/journal.ppat.1004940)
19. Meyer AG, Spielman SJ, Bedford T, Wilke CO. 2015 Time dependence of evolutionary metrics during the 2009 pandemic influenza virus outbreak. Virus Evol. 1, vev006. (doi:10.1093/ve/vev006)
20. Yang Z, Nielsen R, Goldman N, Pedersen AM. 2000 Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155, 431-449.
21. Kosakovsky Pond SL, Frost SDW. 2005 Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 11, 1208-1222. (doi:10.1093J. Molbev/msi105)
22. Pupko T, Bell RE, Mayrose I, Glaser F, Ben-Tal N. 2002 Rate4Site: an algorithmic tool for the identification of functional regions in proteins by surface mapping of evolutionary determinants within their homologues. Bioinformatics 18, S71-S77. (doi:10.1093/bioinformatics/18.suppl-1.S71)
23. Ramsey DC, Scherrer MP, Zhou T, Wilke CO. 2011 The relationship between relative solvent accessibility and evolutionary rate in protein evolution. Genetics 188, 479-488. (doi:10.1534/genetics.111.128025)
24. Grahnen JA, Nandakumar P, Kubelka J, Liberies DA. 2011 Biophysical and structural considerations for protein sequence evolution. BMC Evol. Biol. 11, 2455-2464. (doi:10.1186/1471-2148-11-361)
25. Kryazhimskiy S, Plotkin JB. 2008 The population genetics of iN/iS. PLoS Genet. 4, e1000304. (doi:10.1371/journal.pgen.1000304)
26. Mugal CF, Wolf JBW, Kaj I. 2014 Why time matters: codon evolution and the temporal dynamics of dN/dS. Mol. Biol. Evol. 31, 212-231. (doi:10.1093J. Molbev/mst192)
27. Tokuriki N, Oldfield CJ, Uversky VN, Berezovsky IN, Tawfik DS. 2009 Do viral proteins possess unique biophysical features? Trends Biochem. Sci. 34, 53-59. (doi:10.1016/j.tibs.2008.10.009)
28. Nielsen R, Yang Z. 1998 Clikelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148, 929-936.
29. Yang Z, Bielawski J. 2000 Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15, 496-503. (doi:10.1016/S0169-5347(00)01994-7)
30. Yang Z, Wong W, Nielsen R. 2005 Bayes empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 11, 1107-1118. (doi:10.1093J.Molbev/msi097)
31. Wilke CO. 2012 Bringing molecules back into molecular evolution. PLoS Comput. Biol. 8, e1002572. (doi:10.1371/journal.pcbi.1002572)
32. Susko E, Field C, Blouin C, Roger AJ. 2003 Estimation of rates-across-sites distributions in phylogenetic substitution models. Syst. Biol. 52, 594-603. (doi:10.1080/10635150390235395)
33. Foley B, Leitner T, Apetrei C, Hahn B, Mizrachi I, Mullins J, Rambaut A, Wolinsky S, Korber B. 2013 HIV sequence compendium. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, NM, LA-UR 13-26007.
34. Cock PJ et al. 2009 Biopython: freely available python tools for computational molecular biology and bioinformatics. Bioinformatics 25, 1422-1423. (doi:10.1093/bioinformatics/btpl63)
35. Price MN, Dehal PS, Arkin AP. 2009 FastTree 2: approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490. (doi:10.1371/journal.pone.0009490)
36. Kosakovsky Pond SL, Frost SDW, Muse SV. 2005 HyPhy: hypothesis testing using phylogenies. Bioinformatia 21, 676-679. (doi:10.1093/bioinformatics/bti079)
37. Muse SV, Gaut BS. 1994 A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol. Biol. Evol. 11, 715-724.
38. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Wessig H, Shindyalov IN, Bourne PE. 2000 The protein data bank. Nucleic Acids Res. 28, 235-242. (doi:10.1093/nar/28.1.235)
39. Sarafianos SG, Das K, Tantillo C, Clark ADJ, Ding J, Whitcomb JM, Boyer PL, Hughes SH, Arnold E. 2001 Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J. 20, 1449-1461. (doi:10.1093/emboj/20.6.1449)
40. Chen JC, Krucinski J, Miercke LJ, Finer-Moore JS, Tang AH, Leavitt AD, Stroud RM. 2000 A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Proc. Natl Acad. Sci. USA 97, 8233-8238. (doi:10.1073/pnas.150220297)
41. Wang JY, Ling H, Yang W, Craigie R. 2001 Structure of a two-domain fragment of HIV-1 integrase: implications for domain organization in the intact protein. EMBO J. 20, 7333-7343. (doi:10.1093/emboj/20.24.7333)
42. Kim EE, Baker CT, Dwyer MD, Murcko MA, Rao BG, Tung RD, Navia MA. 1995 Crystal structure of HIV-1 protease in complex with VX-478, a potent and orally bioavailable inhibitor of the enzyme. J. Am. Chem. Soc. 117, 1181-1182. (doi:10.1021/ja00108a056)
43. Pornillos O et al. 2009 X-ray structures of the hexameric building block of the HIV capsid. Cel1137, 1282-1292. (doi:10.1016/j.cell.2009. 04.063)
44. Hill CP, Worthylake D, Bancroft DP, Christensen AM, Sundquist Wl. 1996 Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly. Proc. Natl Acad. Sci. USA 93, 3099-3104. (doi:10.1073/pnas.93.7.3099)
45. Pancera M et al. 1994 Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514, 455-461. (doi:10.1038/nature13808)
46. Katoh K, Frith MC. 2012 Adding unaligned sequences into an existing alignment using MAFFT and LAST. Bioinformatics 28, 3144-3146. (doi:10.1093/bioinformatics/bts578)
47. Katoh K, Standley DM. 2013 MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. (doi:10.1093J. Molbev/mst010)
48. Katoh K, Standley DM. 2014 MAFFT: iterative refinement and additional methods. Methods Mol. Biol. 1079, 131-146. (doi:10.1007/978-1-62703-646-7-8)
49. Meyer AG, Dawson ET, Wilke CO. 2013 Cross-species comparison of site-specific evolutionary-rate variation in influenza hemagglutinin. Phil. Trans. R. Soc. B 368, 20120334. (doi:10.1098/rstb.2012.0334)
50. Kabsch W, Sander C. 1983 Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637. (doi:10.1002/bip.360221211)
51. Tien MZ, Meyer AG, Sydykova DK, Spielman SJ, Wilke CO. 2013 Maximum allowed solvent accessibilites of residues in proteins. PLoS ONE 8, e80635. (doi:10.1371/journal.pone.0080635)
52. Ihaka R, Gentleman R. 1996 R: a language for data analysis and graphics. J. Comput. Graph. Stat. 5, 299-314.
53. Wickham H. 2009 ggplotl: elegant graphics for data analysis. New York, NY: Springer.