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Review

Influenza genome analysis using pyrosequencing method: current applications for a moving target

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Pages 493-509 | Published online: 09 Jan 2014

References

  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA74(12), 5463–5467 (1977).
  • Ronaghi M, Karamohamed S, Pettersson B, Uhlen M, Nyren P. Real-time DNA sequencing using detection of pyrophosphate release. Anal. Biochem.242(1), 84–89 (1996).
  • Ronaghi M, Uhlen M, Nyren P. A sequencing method based on real-time pyrophosphate. Science281(5375), 363–365 (1998).
  • Agaton C, Unneberg P, Sievertzon M et al. Gene expression analysis by signature pyrosequencing. Gene289(1–2), 31–39 (2002).
  • Ahmadian A, Gharizadeh B, Gustafsson AC et al. Single-nucleotide polymorphism analysis by pyrosequencing. Anal. Biochem.280(1), 103–110 (2000).
  • Gustafsson AC, Guo Z, Hu X et al. HPV-related cancer susceptibility and p53 codon 72 polymorphism. Acta Derm. Venereol.81(2), 125–129 (2001).
  • Monstein H, Nikpour-Badr S, Jonasson J. Rapid molecular identification and subtyping of Helicobacter pylori by pyrosequencing of the 16S rDNA variable V1 and V3 regions. FEMS Microbiol Lett.199(1), 103–107 (2001).
  • Nygren M, Ronaghi M, Nyren P, Albert J, Lundeberg J. Quantification of HIV-1 using multiple quantitative polymerase chain reaction standards and bioluminometric detection. Anal. Biochem.288(1), 28–38 (2001).
  • O’Meara D, Wilbe K, Leitner T, Hejdeman B, Albert J, Lundeberg J. Monitoring resistance to human immunodeficiency virus type 1 protease inhibitors by pyrosequencing. J. Clin. Microbiol.39(2), 464–473 (2001).
  • Unnerstad H, Ericsson H, Alderborn A, Tham W, Nielsson-Tham ML, Mattsson JG. Pyrosequencing as a method for grouping of Listeria monocytogenes strains on the basis of single-nucleotide polymorphisms in the inlB gene. Appl. Environ. Microbiol.67(11), 5339–5342 (2001).
  • Deyde VM, Okomo-Adhiambo M, Sheu TG et al. Pyrosequencing as a tool to detect molecular markers of resistance to NAIs in seasonal influenza A viruses. Antiviral Res.81(1), 16–24 (2009).
  • Duwe S, Schweiger B. A new and rapid genotypic assay for the detection of neuraminidase inhibitor resistant influenza A viruses of subtype H1N1, H3N2, and H5N1. J. Virol. Methods153(2), 134–141 (2008).
  • Lackenby A, Democratis J, Siqueira MM, Zambon MC. Rapid quantitation of neuraminidase inhibitor drug resistance in influenza virus quasispecies. Antivir. Ther.13(6), 809–820 (2008).
  • Margulies M, Egholm M, Altman WE et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature437(7057), 376–380 (2005).
  • Deyde VM, Nguyen T, Bright RA et al. Detection of molecular markers of antiviral resistance in influenza A (H5N1) viruses using pyrosequencing method. Antimicrob. Agents Chemother.53(2), 1039 (2009).
  • Ellis JS, Smith JD, Braham S, Lock M, Barlow K, Zambon MC. Design and validation of an H5 TaqMan real-time one-step RT-PCR and confirmatory assays for detection and verification of influenza A H5 infections in humans. J. Clin. Microbiol.45(5), 1535–1543 (2007).
  • Pourmand N, Diamond L, Garten R et al. Rapid and highly informative diagnostic assay for H5N1 influenza viruses. PLoS ONE1, e95 (2006).
  • Waybright N, Petrangelo E, Lowary P, Bogan J, Mulholland N. Detection of human virulence signatures in H5N1. J. Virol. Methods154(1–2), 200–205 (2008).
  • Kruckeberg KE, Thibodeau SN. Pyrosequencing technology as a method for the diagnosis of multiple endocrine neoplasia type 2. Clin Chem.50(3), 522–529 (2004).
  • Gharizadeh B, Nordstrom T, Ahmadian A, Ronaghi M, Nyren P. Long-read pyrosequencing using pure 2´-deoxyadenosine-5´-O´-(1-thiotriphosphate) Sp-isomer. Anal. Biochem.301(1), 82–90 (2002).
  • Ahmadian A, Ehn M, Hober S. Pyrosequencing: history, biochemistry and future. Clin. Chim. Acta363(1–2), 83–94 (2006).
  • Chapman KL, Mortier GR, Chapman K, Loughlin J, Grant ME, Briggs MD. Mutations in the region encoding the von Willebrand factor A domain of matrilin-3 are associated with multiple epiphyseal dysplasia. Nat. Genet.28(4), 393–396 (2001).
  • Magnusson V, Johanneson B, Lima G, Odeberg J, Arcon-Segovia D, Arcon-Riquelme ME. Both risk alleles for FcγRIIA and FcγRIIIA are susceptibility factors for SLE: a unifying hypothesis. Genes Immun.5(2), 130–137 (2004).
  • Magnusson V, Zunec R, Odeberg J et al. Polymorphisms of the Fc g receptor type IIB gene are not associated with systemic lupus erythematosus in the Swedish population. Arthritis Rheum.50(4), 1348–1350 (2004).
  • Ronaghi M, Elahi E. Discovery of single nucleotide polymorphisms and mutations by pyrosequencing. Comp. Funct. Genomics3(1), 51–56 (2002).
  • Gruber JD, Colligan PB, Wolford JK. Estimation of single nucleotide polymorphism allele frequency in DNA pools by using Pyrosequencing. Hum. Genet.110(5), 395–401 (2002).
  • Rajeevan MS, Swan DC, Duncan K, Lee DR, Limor, JR, Unger ER. Quantitation of site-specific HPV 16 DNA methylation by pyrosequencing. J. Virol. Methods138(1–2), 170–176 (2006).
  • Uhlmann K, Brinckmann A, Toliat MR, Ritter H, Nurnberg P. Evaluation of a potential epigenetic biomarker by quantitative methyl-single nucleotide polymorphism analysis. Electrophoresis23(24), 4072–4079 (2002).
  • McCabe KM, Khan G, Zhang YH, Mason EO, McCabe ER. Amplification of bacterial DNA using highly conserved sequences: automated analysis and potential for molecular triage of sepsis. Pediatrics95(2), 165–169 (1995).
  • Gharizadeh B, Ohlin A, Molling P et al. Multiple group-specific sequencing primers for reliable and rapid DNA sequencing. Mol. Cell. Probes17(4), 203–210 (2003).
  • Jonasson J, Olofsson M, Monstein HJ. Classification, identification and subtyping of bacteria based on pyrosequencing and signature matching of 16S rDNA fragments. APMIS110(3), 263–272 (2002).
  • Gharizadeh B, Ghaderi M, Donnelly D, Amini B, Wallin KL, Nyren P. Multiple-primer DNA sequencing method. Electrophoresis24(7–8), 1145–1151 (2003).
  • Gharizadeh B, Kalantari M, Garcia CA, Johansson B, Nyren P. Typing of human papillomavirus by pyrosequencing. Lab. Invest.81(5), 673–679 (2001).
  • Elahi E, Pourmand N, Chaung R et al. Determination of hepatitis C virus genotype by Pyrosequencing. J. Virol. Methods109(2), 171–176 (2003).
  • Towner JS, Sealy TK, Khristova ML et al. Newly discovered ebola virus associated with hemorrhagic fever outbreak in Uganda. PLoS Pathog.4(11), e1000212 (2008).
  • Yamao T, Eshita Y, Kihara Y et al. Novel virus discovery in field-collected mosquito larvae using an improved system for rapid determination of viral RNA sequences (RDV ver4.0). Arch. Virol.154(1), 153–158 (2009).
  • Roszera G, Abbate I, Bruselles A et al. Massively parallel pyrosequencing highlights minority variants in the HIV-1 env quasispecies deriving from lymphomonocyte sub-populations. Retrovirology6(1), 15 (2009).
  • Simen B, Simons S, Hullsiek K et al. Low-abundance drug-resistant viral variants in chronically HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes. J. Infect. Dis.199(5), 693–701 (2009).
  • Solmone M, Vincenti D, Prosperi MC, Bruselles A, Ippolito G, Capobianchi MR. Use of massively parallel ultradeep pyrosequencing to characterize the genetic diversity of hepatitis B virus in drug-resistant and drug-naive patients and to detect minor variants in reverse transcriptase and hepatitis B S antigen. J. Virol.83(4), 1718–1726 (2009).
  • Velculescu VE, Zhang L, Vogelstein B, Kinzler KW. Serial analysis of gene expression. Science270(5235), 484–487 (1995).
  • Nordstrom T, Gharizadeh B, Pourmand N, Nyren P, Ronaghi M. Method enabling fast partial sequencing of cDNA clones. Anal. Biochem.292(2), 266–271 (2001).
  • Englund JA. Antiviral therapy of influenza. Semin. Pediatr. Infect. Dis.13(2), 120–128 (2002).
  • Bridges CB, Winquist AG, Fukuda K, Cox NJ, Singleton JA, Strikas RA. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm. Rep.49(RR-3), 1–38 (2000).
  • Fox JP, Hall CE, Cooney MK, Foy HM. Influenza virus infections in Seattle families, 1975–1979. I. Study design, methods and the occurrence of infections by time and age. Am. J. Epidemiol.116(2), 212–227 (1982).
  • Glezen WP. Cold-adapted, live attenuated influenza vaccine. Expert Rev. Vaccines3(2), 131–139 (2004).
  • Thompson WW, Shay DK, Weintraub E et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA289(2), 179–186 (2003).
  • Bright RA, Medina MJ, Xu X et al. Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet366(9492), 1175–1181 (2005).
  • Bright RA, Shay DK, Shu B, Cox NJ, Klimov AI. Adamantane resistance among influenza A viruses isolated early during the 2005–2006 influenza season in the United States. JAMA295(8), 891–894 (2006).
  • Deyde VM, Garten R, Sheu TG, Gubareva LV, Klimov AI. Letter to the Editor: reply to Saito et al. J. Infect. Dis.197, 632–633 (2008).
  • Deyde VM, Xu X, Bright RA et al. Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide. J. Infect. Dis.196(2), 249–257 (2007).
  • Higgins RR, Eshaghi A, Burton L, Mazzulli T, Drews SJ. Differential patterns of amantadine-resistance in influenza A (H3N2) and (H1N1) isolates in Toronto, Canada. J. Clin. Virol.44(1), 91–93 (2009).
  • Hoper D, Hoffmann B, Beer M. Simple, sensitive, and swift sequencing of complete avian influenza H5N1 genomes. J. Clin. Microbiol. Forthcoming. (2008).
  • Carr MJ, Syare M, Duffy N, Connell J, Hall WW. Rapid molecular detection of the H275Y oseltamivir resistance gene mutation in circulating influenza A (H1N1) viruses. J. Virol. Methods153(2), 257–262 (2008).
  • Bolotin S, Robertson AV, Eshaghi A et al. Development of a novel real-time reverse-transcriptase PCR method for the detection of H275Y positive influenza A H1N1 isolates. J. Virol. Methods (2009) (In Press).
  • Boivin G, Goyette N, Bernatchez H. Prolonged excretion of amantadine-resistant influenza a virus quasi species after cessation of antiviral therapy in an immunocompromised patient. Clin. Infect. Dis.34(5), E23–E25 (2002).
  • Cheung CL, Rayner JM, Smith GJ et al. Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J. Infect. Dis.193(12), 1626–1629 (2006).
  • Hay AJ, Zambon MC, Wolstenholme AJ, Skehel JJ, Smith MH. Molecular basis of resistance of influenza A viruses to amantadine. J. Antimicrob. Chemother.18(Suppl. B), 19–29 (1986).
  • Klimov AI, Rocha E, Hayden FG, Shult PA, Roumillat LF, Cox NJ. Prolonged shedding of amantadine-resistant influenza A viruses by immunodeficient patients: detection by polymerase chain reaction-restriction analysis. J. Infect. Dis.172(5), 1352–1355 (1995).
  • Masuda H, Suzuki H, Oshitani H et al. Incidence of amantadine-resistant influenza A viruses in sentinel surveillance sites and nursing homes in Niigata, Japan. Microbiol Immunol.44(10), 833–839 (2000).
  • Gubareva LV, Webster RG, Hayden FG. Detection of influenza virus resistance to neuraminidase inhibitors by an enzyme inhibition assay. Antiviral Res.53(1), 47–61 (2002).
  • Mungall BA, Xu X, Klimov A. Assaying susceptibility of avian and other influenza A viruses to zanamivir: comparison of fluorescent and chemiluminescent neuraminidase assays. Avian Dis.47(3 Suppl.), 1141–1144 (2003).
  • Tisdale M. Monitoring of viral susceptibility: new challenges with the development of influenza NA inhibitors. Rev. Med. Virol.10(1), 45–55 (2000).
  • Wetherall NT, Trivedi T, Zeller J et al. Evaluation of neuraminidase enzyme assays using different substrates to measure susceptibility of influenza virus clinical isolates to neuraminidase inhibitors: report of the neuraminidase inhibitor susceptibility network. J. Clin. Microbiol.41(2), 742–750 (2003).
  • Ferraris O, Lina B. Mutations of neuraminidase implicated in neuraminidase inhibitors resistance. J. Clin. Virol.41(1), 13–19 (2008).
  • Hayden FG. Antiviral resistance in influenza viruses – implications for management and pandemic response. N. Engl. J. Med.354(8), 785–788 (2006).
  • McKimm-Breschkin J, Trivedi T, Hampson A et al. Neuraminidase sequence analysis and susceptibilities of influenza virus clinical isolates to zanamivir and oseltamivir. Antimicrob. Agents Chemother.47(7), 2264–2272 (2003).
  • Monto AS, Kimm-Breschkin JL, Macken C et al. Detection of influenza viruses resistant to neuraminidase inhibitors in global surveillance during the first 3 years of their use. Antimicrob. Agents Chemother.50(7), 2395–2402 (2006).
  • Sheu T, Deyde V, Okomo-Adhiambo M et al. Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide in 2004–2007. Antimicrob. Agents Chemother.52(9), 3284–3292 (2008).
  • Zambon M, Hayden FG. Position statement: global neuraminidase inhibitor susceptibility network. Antiviral Res.49(3), 147–156 (2001).
  • Abed Y, Bourgault AM, Fenton RJ et al. Characterization of 2 influenza A(H3N2) clinical isolates with reduced susceptibility to neuraminidase inhibitors due to mutations in the hemagglutinin gene. J. Infect. Dis.86(8), 1074–1080 (2002).
  • Gubareva LV, Kaiser L, Matrosovich MN, Soo-Hoo Y, Hayden FG. Selection of influenza virus mutants in experimentally infected volunteers treated with oseltamivir. J. Infect. Dis.183 (4), 523–531 (2001).
  • Hatakeyama S, Sugaya N, Ito M et al. Emergence of influenza B viruses with reduced sensitivity to neuraminidase inhibitors. JAMA297(13), 1435–1442 (2007).
  • Ison MG, Gubareva LV, Atmar RL, Treanor J, Hayden FG. Recovery of drug-resistant influenza virus from immunocompromised patients: a case series. J. Infect. Dis.193(6), 760–764 (2006).
  • Kiso M, Mitamura K, Sakai-Tagawa Y et al. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet364(9436), 759–765 (2004).
  • Ward P, Small I, Smith J, Suter P, Dutkowski R. Oseltamivir (Tamiflu) and its potential for use in the event of an influenza pandemic. J. Antimicrob. Chemother.55(Suppl. 1), i5–i21 (2005).
  • Whitley RJ, Hayden FG, Reisinger KS et al. Oral oseltamivir treatment of influenza in children. Pediatr. Infect. Dis. J.20(2), 127–133 (2001).
  • Kramarz P, Monnet D, Nicoll A, Yilmaz C, Ciancio B. Use of oseltamivir in 12 European countries between 2002 and 2007 – lack of association with the appearance of oseltamivir-resistant influenza A(H1N1) viruses. Euro Surveill.14(5), pii: 19112 (2009).
  • Dharan N, Gubareva L, Meyer J et al. Human infections with oseltamivir-resistant influenza A(H1N1) virus in the United States, 2007–2008. JAMA301(10), 1034–1041 (2009).
  • Rameix-Welti MA, Enouf V, Cuvelier F, Jeannin P, Van der Werf S. Enzymatic properties of the neuraminidase of seasonal H1N1 influenza viruses provide insights for the emergence of natural resistance to oseltamivir. PLOS Pathog.4(7), e1000103 (2008).
  • Gubareva LV, Kaiser L, Matrosovich MN, Soo-Hoo Y, Hayden FG. Selection of influenza virus mutants in experimentally infected volunteers treated with oseltamivir. J. Infect. Dis.183(4), 523–531 (2001).
  • Lackenby A, Hungnes O, Dudman SG et al. Emergence of resistance to oseltamivir among influenza A (H1N1) viruses in Europe. Euro Surveill.13(5), (2008)
  • Barnett JM, Cadman A, Burrell FM et al.In vitro selection and characterization of influenza B/Beijing/1/87 isolates with altered susceptibility to zanamivir. Virology265(2), 286–295 (1999).
  • Jackson D, Barclay W, Zurcher T. Characterization of recombinant influenza B viruses with key neuraminidase inhibitor resistance mutations. J. Antimicrob. Chemother.55(2), 162–169 (2005).
  • de Jong MD, Tran TT, Truong HK et al. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N. Engl. J. Med.353(25), 2667–2672 (2005).
  • Le QM, Kiso M, Someya K et al. Avian flu: isolation of drug-resistant H5N1 virus. Nature437(7062), 1108 (2005).
  • Collins PJ, Haire LF, Lin YP et al. Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature453(7199), 1258–1261 (2008).
  • Hurt AC, Selleck P, Komadina N, Shaw R, Brown L, Barr IG. Susceptibility of highly pathogenic A(H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes. Antiviral Res.73(3), 228–231 (2007).
  • McKimm-Breschkin JL, Selleck PW, Usman TB, Johnson MA. Reduced sensitivity of influenza A (H5N1) to oseltamivir. Emerg. Infect. Dis.13(9), 1354–1357 (2007).
  • Rameix-Welti MA, Agou F, Buchy P et al. Natural variation can significantly alter the sensitivity of influenza A (H5N1) viruses to oseltamivir. Antimicrob. Agents Chemother.50(11), 3809–3815 (2006).
  • Cheng LS, Amaro RE, Xu D, Li WW, Arzberger PW, McCammon JA. Ensemble-based virtual screening reveals potential novel antiviral compounds for avian influenza neuraminidase. J Med Chem.51(13), 3878–3894 (2008).
  • Luo M. Structural biology: antiviral drugs fit for a purpose. Nature443(7107), 37–38 (2006).
  • Russell RJ, Haire LF, Stevens DJ et al.The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature443(7107), 45–49 (2006).
  • Xu X, Zhu X, Dwek RA, Stevens J, Wilson IA. Structural characterization of the 1918 influenza H1N1 neuraminidase. J. Virol.82(21), 10493–10501 (2008).
  • Gubareva LV, Matrosovich MN, Brenner MK, Bethell RC, Webster RG. Evidence for zanamivir resistance in an immunocompromised child infected with influenza B virus. J. Infect. Dis.178(5), 1257–1262 (1998).
  • Shu B, Sheu TG, Deyde V et al. Pyrosequencing of real-time RT-PCR amplicons for rapid sequence confirmation and characterization of highly pathogenic avian influenza A(H5N1) viruses. Presented at: Third European Influenza Conference. Vilamoura, Portugal, 14–17 September 2008.
  • Chen GW, Chang SC, Mok CK et al. Genomic signatures of human versus avian influenza A viruses. Emerg. Infect. Dis.12(9), 1353–1360 (2006).
  • Dharan N, Patton M, Siston A et al. First Reported Outbreak of Oseltamivir-Resistant Influenza A(H1N1) in the United States, Illinois 2008. Emerg. Infect. Dis. (2009) (In Press).
  • Larder BA, Kohli A, Kellam P, Kemp SD, Kronick M, Henfrey RD. Quantitative detection of HIV-1 drug resistance mutations by automated DNA sequencing. Nature365(6447), 671–673 (1993).
  • Mashayekhi F, Ronaghi M. Analysis of read length limiting factors in Pyrosequencing chemistry. Anal. Biochem.363(2), 275–287 (2007).

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