Analyze Diet
Virus research2023; 328; 199081; doi: 10.1016/j.virusres.2023.199081

Codon usage bias of Venezuelan equine encephalitis virus and its host adaption.

Abstract: Venezuelan equine encephalitis virus (VEEV) is an emerging zoonotic virus in the alphavirus genus. It can be transmitted to humans due to spillover from equid-mosquito cycles. The symptoms caused by VEEV include fever, headache, myalgia, nausea, and vomiting. It can also cause encephalitis in severe cases. The evolutionary features of VEEV are largely unknown. In this study, we comprehensively analyzed the codon usage pattern of VEEV by computing a variety of indicators, such as effective number of codons (ENc), codon adaptation index (CAI), relative synonymous codon usage (RSCU), on 130 VEEV coding sequences retrieved from GenBank. The results showed that the codon usage bias of VEEV is relatively low. ENc-GC3s plot, neutrality plot, and CAI-ENc correlation analyses supported that translational selection plays an important role in shaping the codon usage pattern of VEEV whereas the mutation pressure has a minor influence. Analysis of RSCU values showed that most of the preferred codons in VEEV are C/G-ended. Analysis of dinucleotide composition found that all CG- and UA-containing codons are not preferentially used. Phylogenetic analysis showed that VEEV isolates can be clustered into three genera and evolutionary force affects the codon usage pattern. Furthermore, a correspondence analysis (COA) showed that aromaticity and hydrophobicity as well as geographical distribution also have certain effects on the codon usage variation of VEEV, suggesting the possible involvement of translational selection. Overall, the codon usage of VEEV is comparatively slight and translational selection might be the main factor that shapes the codon usage pattern of VEEV. This study will promote our understanding about the evolution of VEEV and its host adaption, and might provide some clues for preventing the cross-species transmission of VEEV.
Publication Date: 2023-03-03 PubMed ID: 36854361PubMed Central: PMC10194294DOI: 10.1016/j.virusres.2023.199081Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article explored the codon usage pattern of the Venezuelan equine encephalitis virus (VEEV) and the possible factors that shape it, and found evidence that translational selections plays a significant role in its evolution and host adaptation.

Context and Objective of the Research

  • The Venezuelan equine encephalitis virus is an emerging zoonotic virus, which means it can be transmitted from animals (particularly equid-mosquito cycles) to humans.
  • The research aimed to understand VEEV’s evolutionary features, which are largely unknown, by analyzing its codon usage pattern.

Methodology

  • The researchers used 130 VEEV coding sequences from GenBank and computed a various indicators such as effective number of codons (ENc), codon adaptation index (CAI), and relative synonymous codon usage (RSCU).
  • They also conducted analysis of the ENc-GC3s plot, neutrality plot, CAI-ENc correlation, RSCU values and dinucleotide composition.

Findings

  • The results showed that the codon usage bias of VEEV is relatively low, and most of VEEV’s preferred codons are C/G-ended.
  • Analyses suggested that translational selection plays an important role in shaping the codon usage pattern of VEEV, while mutation pressure has less influence.
  • All CG- and UA-containing codons are not preferentially used by VEEV.
  • Phylogenetic analysis showed that VEEV isolates can be grouped into three genera and that evolutionary force impacts the codon usage pattern.
  • Correspondence analysis revealed that aromaticity and hydrophobicity along with geographical distribution also affect the codon usage variation of VEEV.

Significance

  • Understanding the codon usage pattern of VEEV can enhance knowledge about its evolution and its adaptation to hosts, which could provide insights for prevention strategies against cross-specie transmission of VEEV.

Cite This Article

APA
Wang H, Liu S, Lv Y, Wei W. (2023). Codon usage bias of Venezuelan equine encephalitis virus and its host adaption. Virus Res, 328, 199081. https://doi.org/10.1016/j.virusres.2023.199081

Publication

ISSN: 1872-7492
NlmUniqueID: 8410979
Country: Netherlands
Language: English
Volume: 328
Pages: 199081
PII: 199081

Researcher Affiliations

Wang, Hongju
  • Kaifeng Key Laboratory of Infection and Biological Safety, School of Basic Medical Sciences, Henan University, Kaifeng, China.
Liu, Shijie
  • School of Clinical Medicine, Henan University, Kaifeng, China.
Lv, Yao
  • School of Clinical Medicine, Henan University, Kaifeng, China.
Wei, Wenqiang
  • Kaifeng Key Laboratory of Infection and Biological Safety, School of Basic Medical Sciences, Henan University, Kaifeng, China. Electronic address: weiwq168@163.com.

MeSH Terms

  • Animals
  • Humans
  • Codon Usage
  • Encephalitis Virus, Venezuelan Equine / genetics
  • Phylogeny
  • Selection, Genetic
  • Codon
  • Mutation
  • Evolution, Molecular

Conflict of Interest Statement

Declaration of Competing Interest All authors declare that they have no conflict of interest.

References

This article includes 60 references
  1. Aguilar PV, Estrada-Franco JG, Navarro-Lopez R, Ferro C, Haddow AD, Weaver SC. Endemic Venezuelan equine encephalitis in the Americas: hidden under the dengue umbrella.. Future Virol 2011;6(6):721-740.
    pmc: PMC3134406pubmed: 21765860doi: 10.2217/fvl.11.5google scholar: lookup
  2. Aguilar PV, Greene IP, Coffey LL, Medina G, Moncayo AC, Anishchenko M, Ludwig GV, Turell MJ, O'Guinn ML, Lee J, Tesh RB, Watts DM, Russell KL, Hice C, Yanoviak S, Morrison AC, Klein TA, Dohm DJ, Guzman H, Travassos da Rosa AP, Guevara C, Kochel T, Olson J, Cabezas C, Weaver SC. Endemic Venezuelan equine encephalitis in northern Peru.. Emerg Infect Dis 2004 May;10(5):880-8.
    pmc: PMC3323213pubmed: 15200823doi: 10.3201/eid1005.030634google scholar: lookup
  3. Carrara AS, Gonzales G, Ferro C, Tamayo M, Aronson J, Paessler S, Anishchenko M, Boshell J, Weaver SC. Venezuelan equine encephalitis virus infection of spiny rats.. Emerg Infect Dis 2005 May;11(5):663-9.
    pmc: PMC3320368pubmed: 15890116doi: 10.3201/eid1105.041251google scholar: lookup
  4. Babbitt GA, Alawad MA, Schulze KV, Hudson AO. Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid.. Nucleic Acids Res 2014;42(17):10915-26.
    pmc: PMC4176184pubmed: 25200075doi: 10.1093/nar/gku811google scholar: lookup
  5. Bowerman CJ, Liyanage W, Federation AJ, Nilsson BL. Tuning β-sheet peptide self-assembly and hydrogelation behavior by modification of sequence hydrophobicity and aromaticity.. Biomacromolecules 2011 Jul 11;12(7):2735-45.
    pubmed: 21568346doi: 10.1021/bm200510kgoogle scholar: lookup
  6. Brooke CB, Deming DJ, Whitmore AC, White LJ, Johnston RE. T cells facilitate recovery from Venezuelan equine encephalitis virus-induced encephalomyelitis in the absence of antibody.. J Virol 2010 May;84(9):4556-68.
    pmc: PMC2863737pubmed: 20181704doi: 10.1128/jvi.02545-09google scholar: lookup
  7. Bulmer M. The selection-mutation-drift theory of synonymous codon usage.. Genetics 1991 Nov;129(3):897-907.
    pmc: PMC1204756pubmed: 1752426doi: 10.1093/genetics/129.3.897google scholar: lookup
  8. Burge C, Campbell AM, Karlin S. Over- and under-representation of short oligonucleotides in DNA sequences.. Proc Natl Acad Sci U S A 1992 Feb 15;89(4):1358-62.
    pmc: PMC48449pubmed: 1741388doi: 10.1073/pnas.89.4.1358google scholar: lookup
  9. Chan PP, Lowe TM. GtRNAdb: a database of transfer RNA genes detected in genomic sequence.. Nucleic Acids Res 2009 Jan;37(Database issue):D93-7.
    pmc: PMC2686519pubmed: 18984615doi: 10.1093/nar/gkn787google scholar: lookup
  10. Coffey LL, Vasilakis N, Brault AC, Powers AM, Tripet F, Weaver SC. Arbovirus evolution in vivo is constrained by host alternation.. Proc Natl Acad Sci U S A 2008 May 13;105(19):6970-5.
    pmc: PMC2383930pubmed: 18458341doi: 10.1073/pnas.0712130105google scholar: lookup
  11. Cristina J, Fajardo A, Soñora M, Moratorio G, Musto H. A detailed comparative analysis of codon usage bias in Zika virus.. Virus Res 2016 Sep 2;223:147-52.
  12. Deardorff ER, Forrester NL, Travassos-da-Rosa AP, Estrada-Franco JG, Navarro-Lopez R, Tesh RB, Weaver SC. Experimental infection of potential reservoir hosts with Venezuelan equine encephalitis virus, Mexico.. Emerg Infect Dis 2009 Apr;15(4):519-25.
    pmc: PMC2671456pubmed: 19331726doi: 10.3201/eid1504.081008google scholar: lookup
  13. Deb B, Uddin A, Chakraborty S. Genome-wide analysis of codon usage pattern in herpesviruses and its relation to evolution.. Virus Res 2021 Jan 15;292:198248.
  14. Dutta R, Buragohain L, Borah P. Analysis of codon usage of severe acute respiratory syndrome corona virus 2 (SARS-CoV-2) and its adaptability in dog.. Virus Res 2020 Oct 15;288:198113.
  15. Estes DM, Zacks MA, Paessler S. Evaluation of host responses to vaccination and infection with venezuelan equine encephalitis virus (VEEV). Current Trends Immunol 2009;10:61–71.
  16. Etibor TA, Yamauchi Y, Amorim MJ. Liquid Biomolecular Condensates and Viral Lifecycles: Review and Perspectives.. Viruses 2021 Feb 25;13(3).
    pmc: PMC7996568pubmed: 33669141doi: 10.3390/v13030366google scholar: lookup
  17. Fan RL, Valkenburg SA, Wong CK, Li OT, Nicholls JM, Rabadan R, Peiris JS, Poon LL. Generation of Live Attenuated Influenza Virus by Using Codon Usage Bias.. J Virol 2015 Nov;89(21):10762-73.
    pmc: PMC4621104pubmed: 26269186doi: 10.1128/jvi.01443-15google scholar: lookup
  18. Forrester NL, Wertheim JO, Dugan VG, Auguste AJ, Lin D, Adams AP, Chen R, Gorchakov R, Leal G, Estrada-Franco JG, Pandya J, Halpin RA, Hari K, Jain R, Stockwell TB, Das SR, Wentworth DE, Smith MD, Kosakovsky Pond SL, Weaver SC. Evolution and spread of Venezuelan equine encephalitis complex alphavirus in the Americas.. PLoS Negl Trop Dis 2017 Aug;11(8):e0005693.
  19. Fros JJ, Pijlman GP. Alphavirus Infection: Host Cell Shut-Off and Inhibition of Antiviral Responses.. Viruses 2016 Jun 11;8(6).
    pmc: PMC4926186pubmed: 27294951doi: 10.3390/v8060166google scholar: lookup
  20. Fu M. Codon usage bias in herpesvirus.. Arch Virol 2010 Mar;155(3):391-6.
    pubmed: 20107845doi: 10.1007/s00705-010-0597-0google scholar: lookup
  21. Garmashova N, Atasheva S, Kang W, Weaver SC, Frolova E, Frolov I. Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription.. J Virol 2007 Dec;81(24):13552-65.
    pmc: PMC2168819pubmed: 17913819doi: 10.1128/jvi.01576-07google scholar: lookup
  22. Greene IP, Paessler S, Austgen L, Anishchenko M, Brault AC, Bowen RA, Weaver SC. Envelope glycoprotein mutations mediate equine amplification and virulence of epizootic venezuelan equine encephalitis virus.. J Virol 2005 Jul;79(14):9128-33.
  23. Gupta P, Sharma A, Han J, Yang A, Bhomia M, Knollmann-Ritschel B, Puri RK, Maheshwari RK. Differential host gene responses from infection with neurovirulent and partially-neurovirulent strains of Venezuelan equine encephalitis virus.. BMC Infect Dis 2017 Apr 26;17(1):309.
    pmc: PMC5405508pubmed: 28446152doi: 10.1186/s12879-017-2355-3google scholar: lookup
  24. He W, Wang N, Tan J, Wang R, Yang Y, Li G, Guan H, Zheng Y, Shi X, Ye R, Su S, Zhou J. Comprehensive codon usage analysis of porcine deltacoronavirus.. Mol Phylogenet Evol 2019 Dec;141:106618.
    pmc: PMC7111727pubmed: 31536759doi: 10.1016/j.ympev.2019.106618google scholar: lookup
  25. Heinrich BS, Maliga Z, Stein DA, Hyman AA, Whelan SPJ. Phase Transitions Drive the Formation of Vesicular Stomatitis Virus Replication Compartments.. mBio 2018 Sep 4;9(5).
    pmc: PMC6123442pubmed: 30181255doi: 10.1128/mbio.02290-17google scholar: lookup
  26. van Hemert F, Berkhout B. Nucleotide composition of the Zika virus RNA genome and its codon usage.. Virol J 2016 Jun 8;13:95.
    pmc: PMC4898363pubmed: 27278486doi: 10.1186/s12985-016-0551-1google scholar: lookup
  27. Jenkins GM, Holmes EC. The extent of codon usage bias in human RNA viruses and its evolutionary origin.. Virus Res 2003 Mar;92(1):1-7.
    pubmed: 12606071doi: 10.1016/s0168-1702(02)00309-xgoogle scholar: lookup
  28. Johnson DM, Sokoloski KJ, Jokinen JD, Pfeffer TL, Chu YK, Adcock RS, Chung D, Tretyakova I, Pushko P, Lukashevich IS. Advanced Safety and Genetic Stability in Mice of a Novel DNA-Launched Venezuelan Equine Encephalitis Virus Vaccine with Rearranged Structural Genes.. Vaccines (Basel) 2020 Mar 2;8(1).
    pmc: PMC7157698pubmed: 32121666doi: 10.3390/vaccines8010114google scholar: lookup
  29. Juarez D, Guevara C, Wiley M, Torre A, Palacios G, Halsey ES, Ampuero S, Leguia M. Isolation of Complete Equine Encephalitis Virus Genome from Human Swab Specimen, Peru.. Emerg Infect Dis 2018 Aug;24(8):1578-1580.
    pmc: PMC6056129pubmed: 30016240doi: 10.3201/eid2408.171274google scholar: lookup
  30. Saikh KU, Lee JS, Kissner TL, Dyas B, Ulrich RG. Toll-like receptor and cytokine expression patterns of CD56+ T cells are similar to natural killer cells in response to infection with Venezuelan equine encephalitis virus replicons.. J Infect Dis 2003 Nov 15;188(10):1562-70.
    pubmed: 14624383doi: 10.1086/379196google scholar: lookup
  31. Kegel WK, Schoot Pv Pv. Competing hydrophobic and screened-coulomb interactions in hepatitis B virus capsid assembly.. Biophys J 2004 Jun;86(6):3905-13.
    pmc: PMC1304292pubmed: 15189887doi: 10.1529/biophysj.104.040055google scholar: lookup
  32. Khandia R, Singhal S, Kumar U, Ansari A, Tiwari R, Dhama K, Das J, Munjal A, Singh RK. Analysis of Nipah Virus Codon Usage and Adaptation to Hosts.. Front Microbiol 2019;10:886.
    pmc: PMC6530375pubmed: 31156564doi: 10.3389/fmicb.2019.00886google scholar: lookup
  33. Kinney RM, Johnson BJ, Welch JB, Tsuchiya KR, Trent DW. The full-length nucleotide sequences of the virulent Trinidad donkey strain of Venezuelan equine encephalitis virus and its attenuated vaccine derivative, strain TC-83.. Virology 1989 May;170(1):19-30.
    pubmed: 2524126doi: 10.1016/0042-6822(89)90347-4google scholar: lookup
  34. Kustin T, Stern A. Biased Mutation and Selection in RNA Viruses.. Mol Biol Evol 2021 Jan 23;38(2):575-588.
    pmc: PMC7543401pubmed: 32986832doi: 10.1093/molbev/msaa247google scholar: lookup
  35. Li G, Zhang W, Wang R, Xing G, Wang S, Ji X, Wang N, Su S, Zhou J. Genetic Analysis and Evolutionary Changes of the Torque teno sus Virus.. Int J Mol Sci 2019 Jun 13;20(12).
    pmc: PMC6628323pubmed: 31200479doi: 10.3390/ijms20122881google scholar: lookup
  36. Liu XS, Zhang YG, Fang YZ, Wang YL. Patterns and influencing factor of synonymous codon usage in porcine circovirus.. Virol J 2012 Mar 15;9:68.
    pmc: PMC3341187pubmed: 22416942doi: 10.1186/1743-422x-9-68google scholar: lookup
  37. Lundberg L, Fontenot J, Lin SC, Pinkham C, Carey BD, Campbell CE, Kehn-Hall K. Venezuelan Equine Encephalitis Virus Capsid Implicated in Infection-Induced Cell Cycle Delay in vitro.. Front Microbiol 2018;9:3126.
    pmc: PMC6315117pubmed: 30631316doi: 10.3389/fmicb.2018.03126google scholar: lookup
  38. Ma YP, Zhou ZW, Liu ZX, Hao L, Ma JY, Feng GQ, Liang ZL, Ke H. Codon usage bias of the phosphoprotein gene of spring viraemia of carp virus and high codon adaptation to the host.. Arch Virol 2014 Jul;159(7):1841-7.
    pubmed: 24519460doi: 10.1007/s00705-014-2000-zgoogle scholar: lookup
  39. Nikolic J, Lagaudrière-Gesbert C, Scrima N, Blondel D, Gaudin Y. [Rabies virus factories are formed by liquid-liquid phase separation].. Med Sci (Paris) 2018 Mar;34(3):203-205.
    pubmed: 29547102doi: 10.1051/medsci/20183403004google scholar: lookup
  40. Auewarakul P. Composition bias and genome polarity of RNA viruses.. Virus Res 2005 Apr;109(1):33-7.
  41. Puigbò P, Bravo IG, Garcia-Vallvé S. E-CAI: a novel server to estimate an expected value of Codon Adaptation Index (eCAI).. BMC Bioinformatics 2008 Jan 29;9:65.
    pmc: PMC2246156pubmed: 18230160doi: 10.1186/1471-2105-9-65google scholar: lookup
  42. Rice P, Longden I, Bleasby A. EMBOSS: the European Molecular Biology Open Software Suite.. Trends Genet 2000 Jun;16(6):276-7.
    pubmed: 10827456doi: 10.1016/s0168-9525(00)02024-2google scholar: lookup
  43. Rossi SL, Russell-Lodrigue KE, Plante KS, Bergren NA, Gorchakov R, Roy CJ, Weaver SC. Rationally Attenuated Vaccines for Venezuelan Equine Encephalitis Protect Against Epidemic Strains with a Single Dose.. Vaccines (Basel) 2020 Sep 2;8(3).
    pmc: PMC7563393pubmed: 32887313doi: 10.3390/vaccines8030497google scholar: lookup
  44. Roy A, Guo F, Singh B, Gupta S, Paul K, Chen X, Sharma NR, Jaishee N, Irwin DM, Shen Y. Base Composition and Host Adaptation of the SARS-CoV-2: Insight From the Codon Usage Perspective.. Front Microbiol 2021;12:548275.
    pmc: PMC8057303pubmed: 33889134doi: 10.3389/fmicb.2021.548275google scholar: lookup
  45. Seyffert M, Georgi F, Tobler K, Bourqui L, Anfossi M, Michaelsen K, Vogt B, Greber UF, Fraefel C. The HSV-1 Transcription Factor ICP4 Confers Liquid-Like Properties to Viral Replication Compartments.. Int J Mol Sci 2021 Apr 24;22(9).
    pmc: PMC8123221pubmed: 33923223doi: 10.3390/ijms22094447google scholar: lookup
  46. Shackelton LA, Parrish CR, Holmes EC. Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses.. J Mol Evol 2006 May;62(5):551-63.
    pubmed: 16557338doi: 10.1007/s00239-005-0221-1google scholar: lookup
  47. Sharma A, Knollmann-Ritschel B. Current Understanding of the Molecular Basis of Venezuelan Equine Encephalitis Virus Pathogenesis and Vaccine Development.. Viruses 2019 Feb 18;11(2).
    pmc: PMC6410161pubmed: 30781656doi: 10.3390/v11020164google scholar: lookup
  48. Sharp PM, Matassi G. Codon usage and genome evolution.. Curr Opin Genet Dev 1994 Dec;4(6):851-60.
    pubmed: 7888755doi: 10.1016/0959-437x(94)90070-1google scholar: lookup
  49. Singh NK, Tyagi A. A detailed analysis of codon usage patterns and influencing factors in Zika virus.. Arch Virol 2017 Jul;162(7):1963-1973.
    pubmed: 28324177doi: 10.1007/s00705-017-3324-2google scholar: lookup
  50. Singh NK, Tyagi A, Kaur R, Verma R, Gupta PK. Characterization of codon usage pattern and influencing factors in Japanese encephalitis virus.. Virus Res 2016 Aug 2;221:58-65.
  51. Sueoka N. Translation-coupled violation of Parity Rule 2 in human genes is not the cause of heterogeneity of the DNA G+C content of third codon position.. Gene 1999 Sep 30;238(1):53-8.
    pubmed: 10570983doi: 10.1016/s0378-1119(99)00320-0google scholar: lookup
  52. Tao P, Dai L, Luo M, Tang F, Tien P, Pan Z. Analysis of synonymous codon usage in classical swine fever virus.. Virus Genes 2009 Feb;38(1):104-12.
    pmc: PMC7089228pubmed: 18958611doi: 10.1007/s11262-008-0296-zgoogle scholar: lookup
  53. Taylor KG, Paessler S. Pathogenesis of Venezuelan equine encephalitis.. Vet Microbiol 2013 Nov 29;167(1-2):145-50.
    pubmed: 23968890doi: 10.1016/j.vetmic.2013.07.012google scholar: lookup
  54. Vilcarromero S, Aguilar PV, Halsey ES, Laguna-Torres VA, Razuri H, Perez J, Valderrama Y, Gotuzzo E, Suarez L, Cespedes M, Kochel TJ. Venezuelan equine encephalitis and 2 human deaths, Peru.. Emerg Infect Dis 2010 Mar;16(3):553-6.
    pmc: PMC3322018pubmed: 20202445doi: 10.3201/eid1603.090970google scholar: lookup
  55. Wang H, Liu S, Zhang B, Wei W. Analysis of Synonymous Codon Usage Bias of Zika Virus and Its Adaption to the Hosts.. PLoS One 2016;11(11):e0166260.
  56. Wang L, Li Y, Guo Z, Yi Y, Zhang H, Shangguan H, Huang C, Ge J. Genetic changes and evolutionary analysis of canine circovirus.. Arch Virol 2021 Aug;166(8):2235-2247.
    pubmed: 34104994doi: 10.1007/s00705-021-05125-8google scholar: lookup
  57. Wright F. The 'effective number of codons' used in a gene.. Gene 1990 Mar 1;87(1):23-9.
    pubmed: 2110097doi: 10.1016/0378-1119(90)90491-9google scholar: lookup
  58. Yu GY, Wiley MR, Kugelman JR, Ladner JT, Beitzel BF, Eccleston LT, Morazzani EM, Glass PJ, Palacios GF. Complete coding sequences of eastern equine encephalitis virus and venezuelan equine encephalitis virus strains isolated from human cases.. Genome Announc 2015 Apr 23;3(2).
    pmc: PMC4408325pubmed: 25908124doi: 10.1128/genomea.00243-15google scholar: lookup
  59. Zhang Y, Liu Y, Liu W, Zhou J, Chen H, Wang Y, Ma L, Ding Y, Zhang J. Analysis of synonymous codon usage in hepatitis A virus.. Virol J 2011 Apr 16;8:174.
    pmc: PMC3087699pubmed: 21496278doi: 10.1186/1743-422x-8-174google scholar: lookup
  60. Zhou JH, Zhang J, Sun DJ, Ma Q, Chen HT, Ma LN, Ding YZ, Liu YS. The distribution of synonymous codon choice in the translation initiation region of dengue virus.. PLoS One 2013;8(10):e77239.

Citations

This article has been cited 0 times.