Differential stepwise evolution of SARS coronavirus functional proteins in different host species

BMC Evolutionary Biology

Volumn 9, Issue 1, 2009, Pages

  Tang, Xianchun ^a,b   Li, Gang ^a   Vasilakis, Nikos ^b   Zhang, Yuan ^c   Shi, Zhengli ^d   Zhong, Yang ^c   Wang, Lin Fa ^a,e   Zhang, Shuyi ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c FUDAN UNIVERSITY   (China)

^d WUHAN INSTITUTE OF VIROLOGY   (China)

^e CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; PROTEIN VP4; VIRUS ENZYME; VIRUS PROTEIN; MEMBRANE PROTEIN; RNA DIRECTED RNA POLYMERASE; SPIKE GLYCOPROTEIN, CORONAVIRUS; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

ARTICLE; BAT; BINDING SITE; CONTROLLED STUDY; FUNCTIONAL PROTEOMICS; GENETIC SELECTION; HOST; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN STABILITY; SARS CORONAVIRUS; VIRUS TRANSMISSION; ANIMAL; BIOLOGICAL MODEL; GENETICS; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEVERE ACUTE RESPIRATORY SYNDROME; SPECIES DIFFERENCE; VIROLOGY;

ANIMALIA; SARS CORONAVIRUS; VIVERRIDAE;

ANIMALS; CHIROPTERA; EVOLUTION, MOLECULAR; HUMANS; MEMBRANE GLYCOPROTEINS; MODELS, GENETIC; PHYLOGENY; RNA REPLICASE; RNA, VIRAL; SARS VIRUS; SELECTION (GENETICS); SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, RNA; SEVERE ACUTE RESPIRATORY SYNDROME; SPECIES SPECIFICITY; VIRAL ENVELOPE PROTEINS;

EID: 65449167637     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-9-52     Document Type: Article

References (65)

1. Severe acute respiratory syndrome. JS Peiris Y Guan KY Yuen, Nat Med 2004 10 12 Suppl S88 97 10.1038/nm1143 15577937 (Pubitemid 40018232)
2. A novel coronavirus associated with severe acute respiratory syndrome. TG Ksiazek D Erdman CS Goldsmith SR Zaki T Peret S Emery S Tong C Urbani JA Comer W Lim, N Engl J Med 2003 348 20 1953 1966 10.1056/NEJMoa030781 12690092 (Pubitemid 36569984)
3. Coronavirus as a possible cause of severe acute respiratory syndrome. JS Peiris ST Lai LL Poon Y Guan LY Yam W Lim J Nicholls WK Yee WW Yan MT Cheung, Lancet 2003 361 9366 1319 1325 10.1016/S0140-6736(03)13077-2 12711465 (Pubitemid 36514862)
4. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. C Drosten S Gunther W Preiser S van der Werf HR Brodt S Becker H Rabenau M Panning L Kolesnikova RA Fouchier, N Engl J Med 2003 348 20 1967 1976 10.1056/NEJMoa030747 12690091 (Pubitemid 36569985)
5. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. PA Rota MS Oberste SS Monroe WA Nix R Campagnoli JP Icenogle S Penaranda B Bankamp K Maher MH Chen, Science 2003 300 5624 1394 1399 10.1126/science.1085952 12730500 (Pubitemid 36638152)
6. The Genome sequence of the SARS-associated coronavirus. MA Marra SJ Jones CR Astell RA Holt A Brooks-Wilson YS Butterfield J Khattra JK Asano SA Barber SY Chan, Science 2003 300 5624 1399 1404 10.1126/science.1085953 12730501 (Pubitemid 36638153)
7. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Y Guan BJ Zheng YQ He XL Liu ZX Zhuang CL Cheung SW Luo PH Li LJ Zhang YJ Guan, Science 2003 302 5643 276 278 10.1126/science.1087139 12958366 (Pubitemid 37248756)
8. Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms. B Kan M Wang H Jing H Xu X Jiang M Yan W Liang H Zheng K Wan Q Liu, J Virol 2005 79 18 11892 11900 16140765 10.1128/JVI.79.18.11892-11900.2005 (Pubitemid 41279306)
9. Review of Bats and SARS. L Wang, Emerg Infect Dis 2006 12 12 1834 1840 17326933
10. Bats are natural reservoirs of SARS-like coronaviruses. W Li Z Shi M Yu W Ren C Smith JH Epstein H Wang G Crameri Z Hu H Zhang, Science 2005 310 5748 676 679 10.1126/science.1118391 16195424 (Pubitemid 41528160)
11. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. SK Lau PC Woo KS Li Y Huang HW Tsoi BH Wong SS Wong SY Leung KH Chan KY Yuen, Proc Natl Acad Sci USA 2005 102 39 14040 14045 16169905 10.1073/pnas.0506735102 (Pubitemid 41377699)
12. Prevalence and genetic diversity of coronaviruses in bats from China. XC Tang JX Zhang SY Zhang P Wang XH Fan LF Li G Li BQ Dong W Liu CL Cheung, J Virol 2006 80 15 7481 7490 16840328 10.1128/JVI.00697-06 (Pubitemid 44092570)
13. Evolutionary insights into the ecology of coronaviruses. D Vijaykrishna GJ Smith JX Zhang JS Peiris H Chen Y Guan, J Virol 2007 81 8 4012 4020 17267506 10.1128/JVI.02605-06 (Pubitemid 46586896)
14. Severe acute respiratory syndrome coronavirus phylogeny: toward consensus. AE Gorbalenya EJ Snijder WJ Spaan, J Virol 2004 78 15 7863 7866 15254158 10.1128/JVI.78.15.7863-7866.2004 (Pubitemid 38944271)
15. Severe acute respiratory syndrome coronavirus group-specific open reading frames encode nonessential functions for replication in cell cultures and mice. B Yount RS Roberts AC Sims D Deming MB Frieman J Sparks MR Denison N Davis RS Baric, J Virol 2005 79 23 14909 14922 16282490 10.1128/JVI.79.23.14909-14922. 2005 (Pubitemid 41636288)
16. Severe acute respiratory syndrome-associated coronavirus 3a protein forms an ion channel and modulates virus release. W Lu BJ Zheng K Xu W Schwarz L Du CK Wong J Chen S Duan V Deubel B Sun, Proc Natl Acad Sci USA 2006 103 33 12540 12545 16894145 10.1073/pnas.0605402103 (Pubitemid 44267294)
17. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. EJ Snijder PJ Bredenbeek JC Dobbe V Thiel J Ziebuhr LL Poon Y Guan M Rozanov WJ Spaan AE Gorbalenya, J Mol Biol 2003 331 5 991 1004 10.1016/S0022-2836(03)00865-9 12927536 (Pubitemid 36969960)
18. Computational Molecular Evolution. Z Yang, Oxford: Oxford University Press 2006
19. Phylogenetic relationships and differential selection pressures among genotypes of dengue-2 virus. SS Twiddy JJ Farrar N Vinh Chau B Wills EA Gould T Gritsun G Lloyd EC Holmes, Virology 2002 298 1 63 72 10.1006/viro.2002.1447 12093174 (Pubitemid 34734880)
20. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. SMEC Chinese, Science 2004 303 5664 1666 1669 10.1126/science.1092002 14752165 (Pubitemid 38338324)
21. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. HD Song CC Tu GW Zhang SY Wang K Zheng LC Lei QX Chen YW Gao HQ Zhou H Xiang, Proc Natl Acad Sci USA 2005 102 7 2430 2435 15695582 10.1073/pnas.0409608102 (Pubitemid 40279393)
22. Adaptive evolution of the spike gene of SARS coronavirus: changes in positively selected sites in different epidemic groups. CY Zhang JF Wei SH He, BMC Microbiol 2006 6 1 88 97 17020602 10.1186/1471-2180-6-88 (Pubitemid 44596151)
23. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. JD Thompson DG Higgins TJ Gibson, Nucleic Acids Res 1994 22 22 4673 4680 7984417 10.1093/nar/22.22.4673 (Pubitemid 24354800)
24. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. TA Hall, Nucl Acids Symp Ser 1999 41 95 98
25. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Z Yang, Mol Biol Evol 1998 15 5 568 573 9580986 (Pubitemid 28194621)
26. Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. K Anand J Ziebuhr P Wadhwani JR Mesters R Hilgenfeld, Science 2003 300 5626 1763 1767 10.1126/science.1085658 12746549 (Pubitemid 36712575)
27. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. N Barretto D Jukneliene K Ratia Z Chen AD Mesecar SC Baker, J Virol 2005 79 24 15189 15198 16306590 10.1128/JVI.79.24. 15189-15198.2005 (Pubitemid 43032301)
28. Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. E Prentice J McAuliffe X Lu K Subbarao MR Denison, J Virol 2004 78 18 9977 9986 15331731 10.1128/JVI.78.18.9977-9986.2004 (Pubitemid 39187116)
29. MrBayes 3: Bayesian phylogenetic inference under mixed models. F Ronquist JP Huelsenbeck, Bioinformatics 2003 19 12 1572 1574 10.1093/bioinformatics/ btg180 12912839 (Pubitemid 37038874)
30. Automated phylogenetic detection of recombination using a genetic algorithm. SL Kosakovsky Pond D Posada MB Gravenor CH Woelk SD Frost, Mol Biol Evol 2006 23 10 1891 1901 10.1093/molbev/msl051 16818476 (Pubitemid 44412875)
31. HyPhy: hypothesis testing using phylogenies. SL Pond SD Frost SV Muse, Bioinformatics 2005 21 5 676 679 10.1093/bioinformatics/bti079 15509596 (Pubitemid 40424796)
32. PAML: a program package for phylogenetic analysis by maximum likelihood. Z Yang, Comput Appl Biosci 1997 13 5 555 556 9367129
33. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Z Yang R Nielsen, Mol Biol Evol 2002 19 6 908 917 12032247 (Pubitemid 34602960)
34. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. J Zhang R Nielsen Z Yang, Mol Biol Evol 2005 22 12 2472 2479 10.1093/molbev/msi237 16107592 (Pubitemid 41661383)
35. Bayes empirical bayes inference of amino acid sites under positive selection. Z Yang WS Wong R Nielsen, Mol Biol Evol 2005 22 4 1107 1118 10.1093/molbev/msi097 15689528 (Pubitemid 40471423)
36. Multiple hypothesis testing to detect lineages under positive selection that affects only a few sites. M Anisimova Z Yang, Mol Biol Evol 2007 24 5 1219 1228 10.1093/molbev/msm042 17339634 (Pubitemid 47343648)
37. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. SL Pond SD Frost, Bioinformatics 2005 21 10 2531 2533 10.1093/bioinformatics/bti320 15713735 (Pubitemid 40731616)
38. Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes. Z Yang WJ Swanson, Mol Biol Evol 2002 19 1 49 57 11752189 (Pubitemid 34008046)
39. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Z Yang R Nielsen N Goldman AM Pedersen, Genetics 2000 155 1 431 449 10790415 (Pubitemid 30257141)
40. A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. JP Bielawski Z Yang, J Mol Evol 2004 59 1 121 132 10.1007/s00239-004-2597-8 15383915 (Pubitemid 38858437)
41. Likelihood analysis of the chalcone synthase genes suggests the role of positive selection in morning glories (Ipomoea). J Yang H Gu Z Yang, J Mol Evol 2004 58 1 54 63 10.1007/s00239-003-2525-3 14743314 (Pubitemid 38117598)
42. Widespread adaptive evolution in the human immunodeficiency virus type 1 genome. W Yang JP Bielawski Z Yang, J Mol Evol 2003 57 2 212 221 10.1007/s00239-003-2467-9 14562964 (Pubitemid 37026543)
43. Mechanisms and enzymes involved in SARS coronavirus genome expression. V Thiel KA Ivanov A Putics T Hertzig B Schelle S Bayer B Weissbrich EJ Snijder H Rabenau HW Doerr, J Gen Virol 2003 84 Pt 9 2305 2315 10.1099/vir.0.19424-0 12917450 (Pubitemid 37063118)
44. Structural insights into SARS coronavirus proteins. M Bartlam H Yang Z Rao, Curr Opin Struct Biol 2005 15 6 664 672 10.1016/j.sbi.2005.10.004 16263266 (Pubitemid 41668523)
45. The power of phylogenetic comparison in revealing protein function. Z Yang, Proc Natl Acad Sci USA 2005 102 9 3179 3180 15728394 10.1073/pnas. 0500371102 (Pubitemid 40328018)
46. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. M Anisimova R Nielsen Z Yang, Genetics 2003 164 3 1229 1236 12871927 (Pubitemid 36935693)
47. Testing the hypothesis of a recombinant origin of the SARS-associated coronavirus. XW Zhang YL Yap A Danchin, Arch Virol 2005 150 1 1 20 10.1007/s00705-004-0413-9 15480857 (Pubitemid 40171946)
48. Evidence from the evolutionary analysis of nucleotide sequences for a recombinant history of SARS-CoV. MJ Stanhope JR Brown H Amrine-Madsen, Infect Genet Evol 2004 4 1 15 19 10.1016/j.meegid.2003.10.001 15019585 (Pubitemid 38305027)
49. Evidence of the recombinant origin of a bat severe acute respiratory syndrome (SARS)-like coronavirus and its implications on the direct ancestor of SARS coronavirus. CC Hon TY Lam ZL Shi AJ Drummond CW Yip F Zeng PY Lam FC Leung, J Virol 2008 82 4 1819 1826 18057240 10.1128/JVI.01926-07 (Pubitemid 350309175)
50. Evidence for recombination in natural populations of dengue virus type 1 based on the analysis of complete genome sequences. HJ Tolou P Couissinier-Paris JP Durand V Mercier JJ de Pina P de Micco F Billoir RN Charrel X de Lamballerie, J Gen Virol 2001 82 Pt 6 1283 1290 11369871 (Pubitemid 32519758)
51. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. F Li W Li M Farzan SC Harrison, Science 2005 309 5742 1864 1868 10.1126/science.1116480 16166518 (Pubitemid 41325098)
52. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. W Li C Zhang J Sui JH Kuhn MJ Moore S Luo SK Wong IC Huang K Xu N Vasilieva, Embo J 2005 24 8 1634 1643 15791205 10.1038/sj.emboj.7600640 (Pubitemid 40646452)
53. Identification of two critical amino acid residues of the severe acute respiratory syndrome coronavirus spike protein for its variation in zoonotic tropism transition via a double substitution strategy. XX Qu P Hao XJ Song SM Jiang YX Liu PG Wang X Rao HD Song SY Wang Y Zuo, J Biol Chem 2005 280 33 29588 29595 10.1074/jbc.M500662200 15980414
54. The SARS coronavirus S glycoprotein receptor binding domain: fine mapping and functional characterization. S Chakraborti P Prabakaran X Xiao DS Dimitrov, Virol J 2005 2 73 82 16122388 10.1186/1743-422X-2-73
55. Potent cross-reactive neutralization of SARS coronavirus isolates by human monoclonal antibodies. Z Zhu S Chakraborti Y He A Roberts T Sheahan X Xiao LE Hensley P Prabakaran B Rockx IA Sidorov, Proc Natl Acad Sci USA 2007 104 29 12123 12128 17620608 10.1073/pnas.0701000104 (Pubitemid 47185640)
56. Moderate mutation rate in the SARS coronavirus genome and its implications. Z Zhao H Li X Wu Y Zhong K Zhang YP Zhang E Boerwinkle YX Fu, BMC evolutionary biology 2004 4 21 29 15222897 10.1186/1471-2148-4-21
57. The Severe Acute Respiratory Syndrome (SARS)-coronavirus 3a protein may function as a modulator of the trafficking properties of the spike protein. YJ Tan, Virol J 2005 2 5 9 15703085 10.1186/1743-422X-2-5
58. Characterization of the 3a protein of SARS-associated coronavirus in infected vero E6 cells and SARS patients. R Zeng RF Yang MD Shi MR Jiang YH Xie HQ Ruan XS Jiang L Shi H Zhou L Zhang, J Mol Biol 2004 341 1 271 279 10.1016/j.jmb.2004.06.016 15312778
59. Assembly of human severe acute respiratory syndrome coronavirus-like particles. Y Ho PH Lin CY Liu SP Lee YC Chao, Biochem Biophys Res Commun 2004 318 4 833 838 10.1016/j.bbrc.2004.04.111 15147946
60. Nucleocapsid-independent specific viral RNA packaging via viral envelope protein and viral RNA signal. K Narayanan CJ Chen J Maeda S Makino, J Virol 2003 77 5 2922 2927 12584316 10.1128/JVI.77.5.2922-2927.2003
61. A severe acute respiratory syndrome-associated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus. L Pewe H Zhou J Netland C Tangudu H Olivares L Shi D Look T Gallagher S Perlman, J Virol 2005 79 17 11335 11342 16103185 10.1128/JVI.79.17.11335-11342.2005
62. The putative protein 6 of the severe acute respiratory syndrome-associated coronavirus: expression and functional characterization. H Geng YM Liu WS Chan AW Lo DM Au MM Waye YY Ho, FEBS Lett 2005 579 30 6763 6768 10.1016/j.febslet.2005.11.007 16310783
63. Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. SA Kopecky-Bromberg L Martinez-Sobrido M Frieman RA Baric P Palese, J Virol 2007 81 2 548 557 17108024 10.1128/JVI.01782-06
64. 7a protein of severe acute respiratory syndrome coronavirus inhibits cellular protein synthesis and activates p38 mitogen-activated protein kinase. SA Kopecky-Bromberg L Martinez-Sobrido P Palese, J Virol 2006 80 2 785 793 16378980 10.1128/JVI.80.2.785-793.2006
65. SARS coronavirus 7a protein blocks cell cycle progression at G0/G1 phase via the cyclin D3/pRb pathway. X Yuan J Wu Y Shan Z Yao B Dong B Chen Z Zhao S Wang J Chen Y Cong, Virology 2006 346 1 74 85 10.1016/j.virol.2005.10.015 16303160