Sequence amplification via cell passaging creates spurious signals of positive adaptation in influenza virus H3N2 hemagglutinin

Virus Evolution

Volumn 2, Issue 2, 2016, Pages

  McWhite, Claire D ^a   Meyer, Austin G ^a   Wilke, Claus O ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Cell Passaging; Egg Passaging; Hemagglutinin; Influenza Virus; Positive Adaptation

Indexed keywords

EID: 85011367093     PISSN: None     EISSN: 20571577     Source Type: Journal    
DOI: 10.1093/ve/vew026     Document Type: Article

References (56)

1. Balish, A. L., Katz, J. M., Klimov, A. I. (2013) Influenza: Propagation, Quantification, Storage. Current Protocols in Microbiology. 29:G:15G.1:15G.1.115G.1.24.
2. Bao, Y., et al. (2008) 'The Influenza Virus Resource at the National Center for Biotechnology Information', Journal of Virology, 82: 596-601.
3. Bedford, T., et al. (2014) 'Integrating Influenza Antigenic Dynamics with Molecular Evolution', eLife, 3: E01914.
4. Belanov, S. S., et al. (2015) 'Genome-Wide Analysis of Evolutionary Markers of Human Influenza A(H1N1)pdm09 and A(H3N2) Viruses May Guide Selection of Vaccine Strain Candidates', Genome Biology and Evolution, 7: 3472-83.
5. Benson, D. A., et al. (2012) 'GenBank', Nucleic Acids Research, 40: D48-53.
6. Blackburne, B. P., Hay, A. J., Goldstein, R. A. (2008) 'Changing Selective Pressure during Antigenic Changes in Human Influenza H3', PLoS Pathogens, 4: E1000058.
7. Bogner, P., et al. (2006) 'A Global Initiative on Sharing Avian Flu Data', Nature, 442: 981.
8. Bush, R. M., et al. (1999) 'Positive Selection on the H3 Hemagglutinin Gene of Human Influenza Virus A', Molecular Biology and Evolution, 16: 1457-65.
9. et al. (2001) 'Predicting Influenza Evolution: The Impact of Terminal and Egg-Adapted Mutations', International Congress Series, 1219: 147-53.
10. et al. (2000) 'Effects of Passage History and Sampling Bias on Phylogenetic Reconstruction of Human Influenza A Evolution', Proceedings of the National Academy of Sciences, 97: 6974-80.
11. Echave, J., Spielman, S. J., Wilke, C. O. (2016) 'Causes of Evolutionary Rate Variation Among Protein Sites', Nature Reviews Genetics, 17: 109-121.
12. Gatherer, D. (2010) 'Passage in Egg Culture is a Major Cause of Apparent Positive Selection in Influenza B Hemagglutinin', Journal of Medical Virology, 82: 123-7.
13. Hamamoto, I., et al. (2013) 'High Yield Production of Influenza Virus in Madin Darby Canine Kidney (MDCK) Cells with Stable Knockdown of IRF7', PLoS One, 8: E59892.
14. Ihaka, R., Gentleman, R. (1996) 'R: A Language for Data Analysis and Graphics', Journal of Computational and Graphical Statistics, 5: 299-314.
15. Ilyushina, N. A., et al. (2012) 'Comparative Study of Influenza Virus Replication in MDCK Cells and in Primary Cells Derived from Adenoids and Airway Epithelium', Journal of Virology, 86: 11725-34.
16. Katoh, K., Standley, D. M. (2013) 'MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability', Molecular Biology and Evolution, 30: 772-80.
17. Katz, J. M., Webster, R. G. (1989) 'Efficacy of Inactivated Influenza A Virus (H3N2) Vaccines Grown in Mammalian Cells or Embryonated Eggs', Journal of Infectious Diseases, 160: 191-8.
18. Wang, M., Webster, R. G. (1990) 'Direct Sequencing of the HA Gene of Influenza (H3N2) Virus in Original Clinical Samples Reveals Sequence Identity with Mammalian Cell-Grown Virus', Journal of Virology, 64: 1808-11.
19. Koel, B.F., et al. (2013) 'Substitutions Near the Receptor Binding Site Determine Major Antigenic Change During Influenza Virus Evolution', Science, 342: 976-9.
20. Koelle, K., et al. (2006) 'Epochal Evolution Shapes the Phylodynamics of Interpandemic Influenza A (H3N2) in Humans', Science, 314: 1898-903.
21. Kratsch, C., et al. (2016) 'Determination of Antigenicity-Altering Patches on the Major Surface Protein of Human Influenza A/H3N2 Viruses', Virus Evolution, 2: Vev025.
22. Kryazhimskiy, S., Plotkin, J. B. (2008) 'The Population Genetics of dN/dS', PLoS Genetics, 4: E1000304.
23. Kumar, S., Henrickson, K. J. (2012) 'Update on Influenza Diagnostics: Lessons from the Novel H1N1 Influenza A Pandemic', Clinical Microbiology Reviews, 25: 344-61.
24. Lee, H. K., et al. (2013a) 'Simplified Large-Scale Sanger Genome Sequencing for Influenza A/H3N2 Virus', PLoS One, 8: E64785.
25. et al. (2013b) 'Comparison of Mutation Patterns in Full-Genome A/H3N2 Influenza Sequences Obtained Directly from Clinical Samples and the Same Samples after a Single MDCK Passage', PLoS One, 8: E79252.
26. Liechti, R., et al. (2010) 'OpenFluDB, A Database for Human and Animal Influenza Virus', Database, 2010: Baq004.
27. Lin, Y. P., et al. (2012) 'Evolution of the Receptor Binding Properties of the Influenza A(H3N2) Hemagglutinin', Proceedings of the National Academy of Sciences, 109: 21474-9.
28. Luksza, M., Lassig, M. (2014) 'A Predictive Fitness Model for Influenza', Nature, 507: 57-61.
29. Matrosovich, M., et al. (2003) 'Overexpression of the Alpha-2, 6-sialyltransferase in MDCK Cells Increases Influenza Virus Sensitivity to Neuraminidase Inhibitors', Journal of Virology, 77: 8418-25.
30. Meyer, A. G., Wilke, C. O. (2013) 'Integrating Sequence Variation and Protein Structure to Identify Sites under Selection', Molecular Biology and Evolution, 30: 36-44.
31. (2015) 'Geometric Constraints Dominate the Antigenic Evolution of Influenza H3N2 Hemagglutinin', PLoS Pathogens, 11: E1004940.
32. Neher, R. A., Bedford, T. (2015) 'nextflu: Real-Time Tracking of Seasonal Influenza Virus Evolution in Humans', Bioinformatics, btv381, 31: 3546-48.
33. Russell, C. A., Shraiman, B. I. (2014) 'Predicting Evolution From the Shape of Genealogical Trees', eLife, 3: E03568.
34. Nelson, M. I., et al. (2006) 'Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus', PLoS Pathogens, 2: E125.
35. Oh, D. Y., et al. (2008) 'MDCK-SIAT1 Cells Show Improved Isolation Rates for Recent Human Influenza Viruses Compared to Conventional MDCK Cells', Journal of Clinical Microbiology, 46: 2189-94.
36. Pan, K., Deem, M. W. (2011) 'Quantifying Selection and Diversity in Viruses by Entropy Methods, with Application to the Haemagglutinin of H3N2 Influenza', Journal of the Royal Society, Interface, 8: 1644-53.
37. Pond, S. L. K., Frost, S. D. W., Muse, S. V. (2005) 'HyPhy: Hypothesis Testing Using Phylogenies', Bioinformatics, 21: 676-9.
38. Price, M. N., Dehal, P. S., Arkin, A. P. (2010) 'FastTree 2-Approximately Maximum-Likelihood Trees for Large Alignments', PLoS One, 5: E9490.
39. Robertson, J. S., et al. (1993) 'The Role of Amniotic Passage in the Egg-Adaptation of Human Influenza Virus is Revealed by Haemagglutinin Sequence Analyses', Journal of General Virology, 74(Pt 10): 2047-51.
40. Shih, A. C. C., et al. (2007) 'Simultaneous Amino Acid Substitutions at Antigenic Sites Drive Influenza A Hemagglutinin Evolution', Proceedings of the National Academy of Sciences, 104: 6283-8.
41. Skowronski, D. M., et al. (2014) 'Low 2012-13 Influenza Vaccine Effectiveness Associated with Mutation in the Egg-Adapted H3N2 Vaccine Strain Not Antigenic Drift in Circulating Viruses', PLoS One, 9: E92153.
42. Spielman, S., Wan, S., Wilke, C. O. (2016) 'A Comparison of One-Rate and Two-Rate Inference Frameworks for Site-Specific dN/dS Estimation', Genetics, Early online August 17, 2016; DOI: 10.1534/genetics.115.185264.
43. Squires, R. B., et al. (2012) 'Influenza Research Database: An Integrated Bioinformatics Resource for Influenza Research and Surveillance', Influenza and Other Respiratory Viruses, 6: 404-16.
44. Stö hr, K., et al. (2012) 'Influenza Virus Surveillance, Vaccine Strain Selection, Manufacture', in Y., Kawaoka and G., Neumann (eds) Influenza Virus, pp. 147-62. Totowa, NJ: Humana Press.
45. Strelkowa, N., Lassig, M. (2012) 'Clonal Interference in the Evolution of Influenza', Genetics, 192: 671-82.
46. Suzuki, Y. (2006) 'Natural Selection on the Influenza Virus Genome', Molecular Biology and Evolution, 23: 1902-11.
47. et al. (2008) 'Positive Selection Operates Continuously on Hemagglutinin During Evolution of H3N2 Human Influenza A Virus', Gene, 427: 111-6.
48. The World Health Organization (2015) Recommended Composition of Influenza Virus Vaccines for Use in the 2015-2016 Northern Hemisphere Influenza Season. Geneva: WHO Press.
49. Tien, M. Z., et al. (2013) 'Maximum Allowed Solvent Accessibilites of Residues in Proteins', PloS One, 8: E80635.
50. Tusche, C., Steinbrü ck, L., McHardy, A. C. (2012) 'Detecting Patches of Protein Sites of Influenza A Viruses Under Positive Selection', Molecular Biology and Evolution, 29: 2063-71.
51. WHO Writing Group, et al. (2012) 'Improving Influenza Vaccine Virus Selection: Report of a WHO Informal Consultation Held at WHO Headquarters, Geneva, Switzerland, 14-16 June 2010', Influenza and Other Respiratory Viruses, 6: 142-52.
52. Wickham, H. (2009) ggplot2: Elegant Graphics for Data Analysis. New York: Springer.
53. Wolf, Y. I., et al. (2006) 'Long Intervals of Stasis Punctuated by Bursts of Positive Selection in the Seasonal Evolution of Influenza A Virus', Biology Direct, 1: 34.
54. World Health Organization Global Influenza Surveillance Network (2011) Manual for the Laboratory Diagnosis and Virological Surveillance of Influenza. Geneva: WHO Press.
55. Wyde, P. R., et al. (1977) 'Effects of Low-A nd High-Passage Influenza Virus Infection in Normal and Nude Mice', Infection and Immunity, 15: 221-9.
56. Xie, H., et al. (2015) 'H3N2 Mismatch of 2014-15 Northern Hemisphere Influenza Vaccines and Head-to-head Comparison between Human and Ferret Antisera derived Antigenic Maps', Scientific Reports, 5: 15279.