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Evolution of influenza a nucleotide segments through the Lens of different complexity measures. (English) Zbl 07825207

Summary: Evolution of influenza viruses is a highly complex process that is still poorly understood. Multiyear persistence of similar variants and accumulating evidences of existence of multigenic traits indicates that influenza viruses operate as integrated units and not only as sets of distinct genes. However, there is still no consensus on whether it is the case, and to what extent. One of the main problems is the lack of framework for analyzing and interpreting large body of available high dimensional genomic, clinical and epidemiological data. By reducing dimensionality of data we intend to show whether in addition to gene-centric selective pressure, the evolution of influenza RNA segments is also shaped by their mutual interactions. Therefore, we will analyze how different complexity/entropy measures (Shannon entropy, topological entropy and Lempel-Ziv complexity) can be used to study evolution of nucleotide segments of different influenza subtypes, while reducing data dimensionality. We show that, at the nucleotide level, multiyear clusters of genome-wide entropy/complexity correlations emerged during the H1N1 pandemic in 2009. Our data are the first empirical results that indirectly support the suggestion that a component of influenza evolutionary dynamics involves correlation between RNA segments. Of all used complexity/entropy measures, Shannon entropy shows the best correlation with epidemiological data.

MSC:

91-XX Game theory, economics, finance, and other social and behavioral sciences
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[1] Adami, C., Information theory in molecular biology, Phys. Life Rev.1 (2014) 3-22.
[2] Alyass, A., Turcotte, M. and Meyre, D., From big data analysis to personalized medicine for all: Challenges and opportunities, BMC Med. Genomics8 (2015) 33.
[3] Amigó, J. M., Monetti, R., Aschenbrenner, T. and Bunk, W., Transcripts: An algebraic approach to coupled time series, Chaos22 (2012) 013105. · Zbl 1331.37118
[4] Amigó, J. M., Szczepanski, J., Wajnryb, E. and Sanchez-Vives, M. V., Estimating the entropy rate of spike trains via Lempel-Ziv complexity, Neural Comput.16 (2004) 717-736. · Zbl 1054.62130
[5] Bandt, C. and Pompe, B., Permutation entropy: A natural complexity measure for time series, Phys. Rev. Lett.88 (2002) 174102.
[6] Benjamini, Y. and Hochberg, Y., Controlling the false discovery rate: A practical and powerful approach to multiple testing, J. R. Stat. Soc. B57 (1995) 289-300. · Zbl 0809.62014
[7] Benjamini, Y. and Yekutieli, D., The control of the false discovery rate in multiple testing under dependency, Ann. Stat.29 (2001) 1165-1188. · Zbl 1041.62061
[8] Bush, R. M., Smith, C. B., Cox, N. J. and Fitch, W. M., Effects of passage history and sampling bias on phylogenetic reconstruction of human influenza A evolution, Proc. Natl. Acad. Sci. USA97 (2000) 6974-6980.
[9] , Update: Influenza activity: United States, 2003-04 season, MMWR Morb. Mortal. Wkly. Rep.53 (2004) 284-287.
[10] Centers for Disease Control and Prevention (CDC), CDC: Flu activity expands; severity similar to past H3N2 seasons (2015), https://www.cdc.gov/flu/news/flu-activity-expands.htm.
[11] Chen, R. and Holmes, E. C., Avian influenza virus exhibits rapid evolutionary dynamics, Mol. Biol. Evol.23 (2006) 2336-2341.
[12] Clarke, R., Ressom, H. W., Wang, A., Xuan, J., Liu, M. C., Gehan, E. A. and Wang, Y., The properties of high-dimensional data spaces: Implications for exploring gene and protein expression data, Nat. Rev. Cancer8 (2008) 37-49.
[13] Deem, M. W. and Pan, K., The epitope regions of H1-subtype influenza A, with application to vaccine efficacy, Protein Eng. Des. Sel.22 (2009) 543-546.
[14] Doshi, P., Trends in recorded influenza mortality: United States, 1900-2004, Am. J. Public Health98 (2008) 939-945.
[15] Galiano, M., Johnson, B. F., Myers, R., Ellis, J., Daniels, R. and Zambon, M., Fatal cases of influenza A(H3N2) in children: Insights from whole genome sequence analysis, PLoS ONE7 (2012) e33166.
[16] Gao, Q., Chou, Y. Y., Doganay, S., Vafabakhsh, R., Ha, T. and Palese, P., The Influenza A virus PB2, PA, NP, and M sequences play a pivotal role during genome packaging, J. Virol.86 (2012) 7043-7051.
[17] Ghedin, Eet al., Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution, Nature437 (2005) 1162-1166.
[18] Hale, B. G., Albrecht, R. A. and Garcia-Sastre, A., Innate immune evasion strategies of inluenza viruses, Future Microbiol.5 (2010) 23-41.
[19] Hamming, O. J., Lutfalla, G., Levraud, J. P. and Hartmann, R., Crystal structure of zebrafish interferons I and II reveals conservation of type I interferon structure in vertebrates, J. Virol.85 (2011) 8181-8187.
[20] Hay, A., Gregory, V., Douglas, A. and Lin, Y., The evolution of human influenza viruses, Philos. Trans. R. Soc. Lond. B, Biol. Sci.356 (2001) 1861-1870.
[21] Heiny, A. T., Miotto, O., Srinivasan, K. N., Khan, A. M., Zhang, G. L., Brusic, V., Tan, T. W. and August, J. T., Evolutionarily conserved protein sequences of influenza A viruses, avian and human, as vaccine targets, PLoS ONE2 (2007) e1190.
[22] Holmes, E. C.et al., Whole-genome analysis of human influenza A virus reveals multiple persistent lineages and reassortment among recent H3N2 viruses, PLoS Biol.3 (2005) e300.
[23] Hu, M.et al., PB2 substitutions V598T/I increase the virulence of H7N9 influenza A virus in mammals, Virology501 (2017) 92-101.
[24] Ince, W. L., Gueye-Mbaye, A., Bennink, J. R. and Yewdell, J. W., Reassortment complements spontaneous mutation in influenza A virus NP and M1 genes to accelerate adaptation to a new host, J. Virol.87 (2013) 4330-4338.
[25] Jin, S., Tan, R., Jiang, Q., Xu, L., Peng, J., Wang, Y. and Wang, Y., A generalized topological entropy for analyzing the complexity of DNA sequences, PLoS ONE9 (2014) e88519.
[26] Jolliffe, I. T., Principal Component Analysis, 2nd edn. (Springer-Verlag, New York, 2002). · Zbl 1011.62064
[27] Kaspar, F. and Schuster, H. G., Easily calculable measure for the complexity of spatiotemporal patterns, Phys. Rev. A36 (1987) 842-848.
[28] Kaverin, N. V.et al., Postreassortment changes in influenza A virus hemagglutinin restoring HA-NA functional match, Virology244 (1998) 315-321.
[29] Kilander, A., Rykkvin, R., Dudman, S. G. and Hungnes, O., Observed association between the HA1 mutation D222G in the 2009 pandemic influenza A(H1N1) virus and severe clinical outcome, Norway 2009-2010, Euro. Surveill.15 (2010) 19498.
[30] Kitano, H., Foundations of Systems Biology (MIT Press, Boston, 2001).
[31] Koelle, K., Cobey, S., Grenfell, B. and Pascual, M., Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans, Science314 (2006) 1898-1903.
[32] Koslicki, D., Topological entropy of DNA sequences, Bioinformatics27 (2011) 1061-1067.
[33] Lindstrom, S. E., Cox, N. J. and Klimov, A., Genetic analysis of human H2N2 and early H3N2 influenza viruses, 1957-1972: Evidence for genetic divergence and multiple reassortment events, Virology328 (2004) 101-119.
[34] Loos, R. J. and Schadt, E. E., This I believe: Gaining new insights through integrating “old” data, Front. Genet.3 (2012) 137.
[35] López-Ruiz, R., Mancini, H. L. and Calbet, X., A statistical measure of complexity, Phys. Lett. A209 (1995) 321-326.
[36] Monetti, R., Bunk, W., Aschenbernner, T. and Jamitzky, F., Characterizing synchronization in time series using information measures extracted from symbolic representations, Phys. Rev. E79 (2009) 046207.
[37] Nelson, M. I., Simonsen, L., Viboud, C., Miller, M. A. and Holmes, E. C., Phylogenetic analysis reveals the global migration of seasonal influenza A viruses, PLoS Pathog.3 (2007) 1220-1228.
[38] Neverov, A. D., Lezhnina, K. V., Kondrashov, A. S. and Bazykin, G. A., Intrasubtype reassortments cause adaptive amino acid replacements in H3N2 influenza genes, PLoS Genet.10 (2014) e1004037.
[39] Noble, W. S., How does multiple testing correction work?Nat. Biotechnol.27 (2009) 1135-1137.
[40] Plotkin, J., Dushoff, J. and Levin, S., Hemagglutinin sequence clusters and the anti-genic evolution of influenza A virus, Proc. Natl. Acad. Sci. USA99 (2002) 6263-6268.
[41] Rambaut, A., Pybus, O. G., Nelson, M. I., Viboud, C., Taubenberger, J. K. and Holmes, E. C., The genomic and epidemiological dynamics of human influenza A virus, Nature453 (2008) 615-619.
[42] Rosso, O. A., Larrondo, H. A., Martin, M. T., Plastino, A. and Fuentes, M. A., Distinguishing noise from chaos, Phys. Rev. Lett.99 (2007) 154102.
[43] Scholz, M. B., Lo, C. C. and Chain, P. S., Next generation sequencing and bioinformatic bottlenecks: The current state of metagenomic data analysis, Curr. Opin. Biotechnol.23 (2012) 9-15.
[44] Secombes, C. J. and Zou, J., Evolution of interferons and interferon receptors, Front. Immunol.8 (2017) 209.
[45] Shaw, M. L. and Palese, P., Orthomyxoviridae, in Fields Virology, 6th edn., Knipe, D. M. and Howley, P. M. (eds.) (Lippincott Williams & Wilkins, Philadelphia, 2013), pp. 1151-1185.
[46] Smith, D. J., Lapedes, A. S., de Jong, J. C., Bestebroer, T. M., Rimmelzwaan, G. F. and Osterhaus, A. D., Mapping the antigenic and genetic evolution of influenza virus, Science305 (2004) 371-376.
[47] Smith, G. J., Vijaykrishna, D., Bahl, J., Lycett, S. J., Worobey, M. and Pybus, O. G., Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic, Nature459 (2009) 1122-1125.
[48] Song, M. S., Pascua, P. N., Lee, J. H., Baek, Y. H., Lee, O.-J. and Kim, C.-J., The polymerase acidic protein gene of influenza A virus contributes to pathogenicity in a mouse model, J. Virol.83 (2009) 12325-12335.
[49] Steel, J. and Lowen, A. C., Influenza A virus reassortment, Curr. Top. Microbiol. Immunol.385 (2014) 377-401.
[50] Steinhauer, D. A. and Skehel, J. J., Genetics of influenza viruses, Annu. Rev. Genet.36 (2002) 305-332.
[51] Suptawiwat, O., Ninpan, K., Boonarkart, C., Ruangrung, K. and Auewarakul, P., Evolutionary dynamic of antigenic residues on influenza B hemagglutinin, Virology502 (2017) 84-96.
[52] Taubenberger, J. K. and Morens, D. M., 1918 Influenza: The mother of all pandemics, Emerg. Infect. Dis.12 (2006) 15-22.
[53] Taubenberger, J. K. and Morens, D. M., The pathology of influenza virus infections, Annu. Rev. Pathol.3 (2008) 499-522.
[54] Taubes, G., Epidemiology faces its limits, Science269 (1995) 164-169.
[55] Tawfik, D. S., Messy biology and the origins of evolutionary innovations, Nat. Chem. Biol.6 (2010) 692-696.
[56] Wagner, R., Matrosovich, M. and Klenk, H. D., Functional balance between haemagglutinin and neuraminidase in influenza virus infections, Rev. Med. Virol.12 (2002) 159-166.
[57] Watanabe, T., Watanabe, S. and Kawaoka, Y., Cellular networks involved in the inluenza virus life cycle, Cell Host Microbe7 (2010) 427-439.
[58] Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M. and Kawaoka, Y., Evolution and ecology of influenza A viruses, Microbiol. Mol. Biol. Rev.56 (1992) 152-179.
[59] Weinreich, D. M., Delaney, N. F., Depristo, M. A. and Hartl, D. L., Darwinian evolution can follow only very few mutational paths to fitter proteins, Science312 (2006) 111-114.
[60] Wolf, Y. I., Viboud, C., Holmes, E. C., Koonin, E. V. and Lipman, D. J., Long intervals of stasis punctuated by bursts of positive selection in the seasonal evolution of influenza A virus, Biol. Direct1 (2006) 34.
[61] Wolff, T. and Ludwig, S., Inluenza viruses control the vertebrate type I interferon system: factors, mechanisms, and consequences, J. Interferon Cytokine Res.29 (2009) 549-557.
[62] Xu, J., Liu, Z., Liu, R. and Yang, Q. F., Information transformation in human cerebral cortex, Physica D106 (1997) 363-374.
[63] Yen, H. L., Liang, C. H., Wu, C. Y., Forrest, H. L., Ferguson, A. and Choy, K. T., Hemagglutinin-neuraminidase balance confers respiratory-droplet transmissibility of the pandemic H1N1 influenza virus in ferrets, Proc. Natl. Acad. Sci. USA108 (2011) 14264-14269.
[64] Zhang, X. S., Zhu, Y. S., Thakor, N. V. and Wang, Z. Z., Detecting ventricular tachycardia and fibrillation by complexity measure, IEEE Trans. Biomed. Eng.46 (1999) 548-555.
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