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Research article

References

  1. Ahn I, Son HS. 2010. Comparative study of the nucleotide bias between the novel H1N1 and H5N1 subtypes of influenza A viruses using bioinformatics techniques. J. Microbiol. Biotechnol. 20: 63-70.
    CrossRef
  2. Akashi H. 1994. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136: 927-935.
    Pubmed PMC
  3. Boycheva S, Chkodrov G, Ivanov I. 2003. Codon pairs in the genome of Escherichia coli. Bioinformatics 19: 987-998.
    Pubmed CrossRef
  4. Chen Y. 2013. A comparison of synonymous codon usage bias patterns in DNA and RNA virus genomes: quantifying the relative importance of mutational pressure and natural selection. Biomed. Res. Int. 2013: 406342.
    CrossRef
  5. Cheng X, Virk N, Chen W, Ji S, Sun Y, Wu X. 2013. CpG usage in RNA viruses: data and hypotheses. PLoS One 8:e74109.
    Pubmed PMC CrossRef
  6. Chiapello H, Ollivier E, Landes-Devauchelle C, Nitschke P, Risler JL. 1999. Codon usage as a tool to predict the cellular location of eukaryotic ribosomal proteins and aminoacyltRNA synthetases. Nucleic Acids Res. 27: 2848-2851.
    Pubmed PMC CrossRef
  7. Comeron JM, Aguade M. 1998. An evaluation of measures of synonymous codon usage bias. J. Mol. Evol. 47: 268-274.
    Pubmed CrossRef
  8. Gill PW. 1971. Hong Kong 68 variant of influenza A2. Br. Med. J. 3: 308.
    Pubmed PMC CrossRef
  9. Goni N, Iriarte A, Comas V, Sonora M, Moreno P, Moratorio G, et al. 2012. Pandemic influenza A virus codon usage revisited: biases, adaptation and implications for vaccine strain development. Virol. J. 9: 263.
    Pubmed PMC CrossRef
  10. Gouy M, Gautier C. 1982. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 10: 7055-7074.
    Pubmed PMC CrossRef
  11. Gramer MR, Lee JH, Choi YK, Goyal SM, Joo HS. 2007. Serologic and genetic characterization of North American H3N2 swine influenza A viruses. Can. J. Vet. Res. 71: 201-206.
    Pubmed PMC
  12. Grantham R, Gautier C, Gouy M, Mercier R, Pave A. 1980. Codon catalog usage and the genome hypothesis. Nucleic Acids Res. 8: r49-r62.
    Pubmed PMC CrossRef
  13. Greenacre M, Hastie T. 1987. The geometric interpretation of correspondence analysis. J. Am. Stat. Assoc. 82: 437-447.
    CrossRef
  14. Greenacre M, Vrba E. 1984. Graphical display and interpretation of antelope census data in African wildlife areas, using correspondence analysis. Ecology 65: 984-997.
    CrossRef
  15. Greenbaum BD, Levine AJ, Bhanot G, Rabadan R. 2008. Patterns of evolution and host gene mimicry in influenza and other RNA viruses. PLoS Pathog. 4: e1000079.
    Pubmed PMC CrossRef
  16. Hammer Ø, Harper D, Ryan P. 2001. PAST - PAlaeontological STatistics, ver. 1.89. Palaeontol. Electron. 4: 1-9.
  17. Jenkins GM, Holmes EC. 2003. The extent of codon usage bias in human RNA viruses and its evolutionary origin. Virus Res. 92: 1-7.
    CrossRef
  18. Karlin S, Doerfler W, Cardon LR. 1994. Why is CpG suppressed in the genomes of virtually all small eukaryotic viruses but not in those of large eukaryotic viruses? J. Virol. 68: 2889-2897.
    Pubmed PMC
  19. Karlin S, Mrazek J. 1997. Compositional differences within and between eukaryotic genomes. Proc. Natl. Acad. Sci. USA 94: 10227-10232.
    Pubmed PMC CrossRef
  20. Korteweg C, Gu J. 2008. Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am. J. Pathol. 172: 1155-1170.
    Pubmed PMC CrossRef
  21. Moriyama EN, Powell JR. 1998. Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. Nucleic Acids Res. 26: 3188-3193.
    Pubmed PMC CrossRef
  22. Moura G, Pinheiro M, Arrais J, Gomes AC, Carreto L, Freitas A, et al. 2007. Large scale comparative codon-pair context analysis unveils general rules that fine-tune evolution of mRNA primary structure. PLoS One 2: e847.
    Pubmed PMC CrossRef
  23. Moura G, Pinheiro M, Silva R, Miranda I, Afreixo V, Dias G, et al. 2005. Comparative context analysis of codon pairs on an ORFeome scale. Genome Biol. 6: R28.
    Pubmed PMC CrossRef
  24. Novembre JA. 2002. Accounting for background nucleotide composition when measuring codon usage bias. Mol. Biol. Evol. 19: 1390-1394.
    Pubmed CrossRef
  25. Ogle JM, Ramakrishnan V. 2005. Structural insights into translational fidelity. Annu. Rev. Biochem. 74: 129-177.
    Pubmed CrossRef
  26. Osawa S, Ohama T, Yamao F, Muto A, Jukes TH, Ozeki H, Umesono K. 1988. Directional mutation pressure and transfer RNA in choice of the third nucleotide of synonymous twocodon sets. Proc. Natl. Acad. Sci. USA 85: 1124-1128.
    Pubmed PMC CrossRef
  27. Post LE, Nomura M. 1980. DNA sequences from the str operon of Escherichia coli. J. Biol. Chem. 255: 4660-4666.
    Pubmed
  28. Rabadan R, Levine AJ, Robins H. 2006. Comparison of avian and human influenza A viruses reveals a mutational bias on the viral genomes. J. Virol. 80: 11887-11891.
    Pubmed PMC CrossRef
  29. Romero H, Zavala A, Musto H. 2000. Codon usage in Chlamydia trachomatis is the result of strand-specific mutational biases and a complex pattern of selective forces. Nucleic Acids Res. 28: 2084-2090.
    Pubmed PMC CrossRef
  30. Shackelton LA, Parrish CR, Holmes EC. 2006. Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. J. Mol. Evol. 62: 551-563.
    Pubmed CrossRef
  31. Sharp PM, Li WH. 1987. The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 15: 1281-1295.
    Pubmed PMC CrossRef
  32. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, et al. 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122-1125.
    Pubmed CrossRef
  33. Sueoka N. 1988. Directional mutation pressure and neutral molecular evolution. Proc. Natl. Acad. Sci. USA 85: 2653-2657.
    Pubmed PMC CrossRef
  34. Ungchusak K, Auewarakul P, Dowell SF, Kitphati R, Auwanit W, Puthavathana P, et al. 2005. Probable person-toperson transmission of avian influenza A (H5N1). N. Engl. J. Med. 352: 333-340.
    Pubmed CrossRef
  35. Wong EH, Smith DK, Rabadan R, Peiris M, Poon LL. 2010. Codon usage bias and the evolution of influenza A viruses. Codon Usage Biases of Influenza Virus. BMC Evol. Biol. 10: 253.
    Pubmed PMC CrossRef
  36. Wright F. 1990. The ‘effective number of codons’ used in a gene. Gene 87: 23-29.
    CrossRef
  37. Xiang H, Zhang R, Butler RR 3rd, Liu T, Zhang L, Pombert JF, Zhou Z. 2015. Comparative analysis of codon usage bias patterns in microsporidian genomes. PLoS One 10: e0129223.
    Pubmed PMC CrossRef
  38. Zhong J, Li Y, Zhao S, Liu S, Zhang Z. 2007. Mutation pressure shapes codon usage in the GC-rich genome of footandmouth disease virus. Virus Genes 35: 767-776.
    Pubmed CrossRef
  39. Zhou T, Gu W, Ma J, Sun X, Lu Z. 2005. Analysis of synonymous codon usage in H5N1 virus and other influenza A viruses. Biosystems 81: 77-86.
    Pubmed CrossRef

Article

Research article

J. Microbiol. Biotechnol. 2016; 26(11): 1972-1982

Published online November 28, 2016 https://doi.org/10.4014/jmb.1605.05016

Copyright © The Korean Society for Microbiology and Biotechnology.

Insights into the Usage of Nucleobase Triplets and Codon Context Pattern in Five Influenza A Virus Subtypes

Himangshu Deka 1 and Supriyo Chakraborty 1*

Department of Biotechnology, Assam University, Silchar-788011, Assam, India

Received: May 9, 2016; Accepted: July 20, 2016

Abstract

Influenza A virus is a single-stranded RNA virus with a genome of negative polarity. Owing
to the antigenic diversity and cross concrete shift, an immense number of novel strains have
developed astronomically over the years. The present work deals with the codon utilization
partialness among five different influenza A viruses isolated from human hosts. All the
subtypes showed the homogeneous pattern of nucleotide utilization with a little variation in
their utilization frequencies. A lower bias in codon utilization was observed in all the subtypes
as reflected by higher magnitudes of an efficacious number of codons. Dinucleotide analysis
showed very low CpG utilization and a high predilection of A/T-ending codons. The H5N1
subtype showed noticeable deviation from the rest. Codon pair context analysis showed
remarkable depletion of NNC-GNN and NNT-ANN contexts. The findings alluded towards
GC-compositional partialness playing a vital role, which is reflected in the consequential
positive correlation between the GC contents at different codon positions. Untangling the
codon utilization profile would significantly contribute to identifying novel drug targets that
will pacify the search for antivirals against this virus.

Keywords: Codon usage bias, dinucleotide, influenza A virus, codon pair context, preferred codon

References

  1. Ahn I, Son HS. 2010. Comparative study of the nucleotide bias between the novel H1N1 and H5N1 subtypes of influenza A viruses using bioinformatics techniques. J. Microbiol. Biotechnol. 20: 63-70.
    CrossRef
  2. Akashi H. 1994. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136: 927-935.
    Pubmed KoreaMed
  3. Boycheva S, Chkodrov G, Ivanov I. 2003. Codon pairs in the genome of Escherichia coli. Bioinformatics 19: 987-998.
    Pubmed CrossRef
  4. Chen Y. 2013. A comparison of synonymous codon usage bias patterns in DNA and RNA virus genomes: quantifying the relative importance of mutational pressure and natural selection. Biomed. Res. Int. 2013: 406342.
    CrossRef
  5. Cheng X, Virk N, Chen W, Ji S, Sun Y, Wu X. 2013. CpG usage in RNA viruses: data and hypotheses. PLoS One 8:e74109.
    Pubmed KoreaMed CrossRef
  6. Chiapello H, Ollivier E, Landes-Devauchelle C, Nitschke P, Risler JL. 1999. Codon usage as a tool to predict the cellular location of eukaryotic ribosomal proteins and aminoacyltRNA synthetases. Nucleic Acids Res. 27: 2848-2851.
    Pubmed KoreaMed CrossRef
  7. Comeron JM, Aguade M. 1998. An evaluation of measures of synonymous codon usage bias. J. Mol. Evol. 47: 268-274.
    Pubmed CrossRef
  8. Gill PW. 1971. Hong Kong 68 variant of influenza A2. Br. Med. J. 3: 308.
    Pubmed KoreaMed CrossRef
  9. Goni N, Iriarte A, Comas V, Sonora M, Moreno P, Moratorio G, et al. 2012. Pandemic influenza A virus codon usage revisited: biases, adaptation and implications for vaccine strain development. Virol. J. 9: 263.
    Pubmed KoreaMed CrossRef
  10. Gouy M, Gautier C. 1982. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 10: 7055-7074.
    Pubmed KoreaMed CrossRef
  11. Gramer MR, Lee JH, Choi YK, Goyal SM, Joo HS. 2007. Serologic and genetic characterization of North American H3N2 swine influenza A viruses. Can. J. Vet. Res. 71: 201-206.
    Pubmed KoreaMed
  12. Grantham R, Gautier C, Gouy M, Mercier R, Pave A. 1980. Codon catalog usage and the genome hypothesis. Nucleic Acids Res. 8: r49-r62.
    Pubmed KoreaMed CrossRef
  13. Greenacre M, Hastie T. 1987. The geometric interpretation of correspondence analysis. J. Am. Stat. Assoc. 82: 437-447.
    CrossRef
  14. Greenacre M, Vrba E. 1984. Graphical display and interpretation of antelope census data in African wildlife areas, using correspondence analysis. Ecology 65: 984-997.
    CrossRef
  15. Greenbaum BD, Levine AJ, Bhanot G, Rabadan R. 2008. Patterns of evolution and host gene mimicry in influenza and other RNA viruses. PLoS Pathog. 4: e1000079.
    Pubmed KoreaMed CrossRef
  16. Hammer Ø, Harper D, Ryan P. 2001. PAST - PAlaeontological STatistics, ver. 1.89. Palaeontol. Electron. 4: 1-9.
  17. Jenkins GM, Holmes EC. 2003. The extent of codon usage bias in human RNA viruses and its evolutionary origin. Virus Res. 92: 1-7.
    CrossRef
  18. Karlin S, Doerfler W, Cardon LR. 1994. Why is CpG suppressed in the genomes of virtually all small eukaryotic viruses but not in those of large eukaryotic viruses? J. Virol. 68: 2889-2897.
    Pubmed KoreaMed
  19. Karlin S, Mrazek J. 1997. Compositional differences within and between eukaryotic genomes. Proc. Natl. Acad. Sci. USA 94: 10227-10232.
    Pubmed KoreaMed CrossRef
  20. Korteweg C, Gu J. 2008. Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am. J. Pathol. 172: 1155-1170.
    Pubmed KoreaMed CrossRef
  21. Moriyama EN, Powell JR. 1998. Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. Nucleic Acids Res. 26: 3188-3193.
    Pubmed KoreaMed CrossRef
  22. Moura G, Pinheiro M, Arrais J, Gomes AC, Carreto L, Freitas A, et al. 2007. Large scale comparative codon-pair context analysis unveils general rules that fine-tune evolution of mRNA primary structure. PLoS One 2: e847.
    Pubmed KoreaMed CrossRef
  23. Moura G, Pinheiro M, Silva R, Miranda I, Afreixo V, Dias G, et al. 2005. Comparative context analysis of codon pairs on an ORFeome scale. Genome Biol. 6: R28.
    Pubmed KoreaMed CrossRef
  24. Novembre JA. 2002. Accounting for background nucleotide composition when measuring codon usage bias. Mol. Biol. Evol. 19: 1390-1394.
    Pubmed CrossRef
  25. Ogle JM, Ramakrishnan V. 2005. Structural insights into translational fidelity. Annu. Rev. Biochem. 74: 129-177.
    Pubmed CrossRef
  26. Osawa S, Ohama T, Yamao F, Muto A, Jukes TH, Ozeki H, Umesono K. 1988. Directional mutation pressure and transfer RNA in choice of the third nucleotide of synonymous twocodon sets. Proc. Natl. Acad. Sci. USA 85: 1124-1128.
    Pubmed KoreaMed CrossRef
  27. Post LE, Nomura M. 1980. DNA sequences from the str operon of Escherichia coli. J. Biol. Chem. 255: 4660-4666.
    Pubmed
  28. Rabadan R, Levine AJ, Robins H. 2006. Comparison of avian and human influenza A viruses reveals a mutational bias on the viral genomes. J. Virol. 80: 11887-11891.
    Pubmed KoreaMed CrossRef
  29. Romero H, Zavala A, Musto H. 2000. Codon usage in Chlamydia trachomatis is the result of strand-specific mutational biases and a complex pattern of selective forces. Nucleic Acids Res. 28: 2084-2090.
    Pubmed KoreaMed CrossRef
  30. Shackelton LA, Parrish CR, Holmes EC. 2006. Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. J. Mol. Evol. 62: 551-563.
    Pubmed CrossRef
  31. Sharp PM, Li WH. 1987. The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 15: 1281-1295.
    Pubmed KoreaMed CrossRef
  32. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, et al. 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122-1125.
    Pubmed CrossRef
  33. Sueoka N. 1988. Directional mutation pressure and neutral molecular evolution. Proc. Natl. Acad. Sci. USA 85: 2653-2657.
    Pubmed KoreaMed CrossRef
  34. Ungchusak K, Auewarakul P, Dowell SF, Kitphati R, Auwanit W, Puthavathana P, et al. 2005. Probable person-toperson transmission of avian influenza A (H5N1). N. Engl. J. Med. 352: 333-340.
    Pubmed CrossRef
  35. Wong EH, Smith DK, Rabadan R, Peiris M, Poon LL. 2010. Codon usage bias and the evolution of influenza A viruses. Codon Usage Biases of Influenza Virus. BMC Evol. Biol. 10: 253.
    Pubmed KoreaMed CrossRef
  36. Wright F. 1990. The ‘effective number of codons’ used in a gene. Gene 87: 23-29.
    CrossRef
  37. Xiang H, Zhang R, Butler RR 3rd, Liu T, Zhang L, Pombert JF, Zhou Z. 2015. Comparative analysis of codon usage bias patterns in microsporidian genomes. PLoS One 10: e0129223.
    Pubmed KoreaMed CrossRef
  38. Zhong J, Li Y, Zhao S, Liu S, Zhang Z. 2007. Mutation pressure shapes codon usage in the GC-rich genome of footandmouth disease virus. Virus Genes 35: 767-776.
    Pubmed CrossRef
  39. Zhou T, Gu W, Ma J, Sun X, Lu Z. 2005. Analysis of synonymous codon usage in H5N1 virus and other influenza A viruses. Biosystems 81: 77-86.
    Pubmed CrossRef