5.9
CiteScore
5.9
Impact Factor
Volume 47 Issue 1
Jan.  2020
Turn off MathJax
Article Contents

Genome-wide evolution analysis reveals low CpG contents of fast-evolving genes and identifies antiviral microRNAs

doi: 10.1016/j.jgg.2019.12.001
More Information
  • Noncoding RNAs (ncRNAs) play important roles in many biological processes and provide materials for evolutionary adaptations beyond protein-coding genes, such as in the arms race between the host and pathogen. However, currently, a comprehensive high-resolution analysis of primate genomes that includes the latest annotated ncRNAs is not available. Here, we developed a computational pipeline to estimate the selections that act on noncoding regions based on comparisons with a large number of reference sequences in introns adjacent to the interested regions. Our method yields result comparable with those of the established codon-based method and phyloP method for coding genes; thus, it provides a holistic framework for estimating the selection on the entire genome. We further showed that fast-evolving protein-coding genes and their corresponding 5′ UTRs have a significantly lower frequency of the CpG dinucleotides than those evolving at an average pace, and these fast-evolving genes are enriched in the process of immunity and host defense. We also identified fast-evolving miRNAs with antiviral functions in cells. Our results provide a resource for high-resolution evolution analysis of the primate genomes.
  • loading
  • [1]
    Agarwal, V., Bell, G.W., Nam, J.W., Bartel, D.P., 2015. Predicting effective microRNA target sites in mammalian mRNAs. elife 4. DOI: 10.7554/eLife.05005.
    [2]
    Alinejad-Rokny, H., Anwar, F., Waters, S.A., Davenport, M.P., Ebrahimi, D., 2016. Source of CpG depletion in the HIV-1 genome. Mol. Biol. Evol. 33, 3205-3212.
    [3]
    Amaral, A.J., Andrade, J., Foxall, R.B., Matoso, P., Matos, A.M., Soares, R.S., Rocha, C., Ramos, C.G., Tendeiro, R., Serra-Caetano, A., 2017. miRNA profiling of human naive CD4 T cells links miR-34c-5p to cell activation and HIV replication. EMBO J. 36, 346-360.
    [4]
    Atkinson, N.J., Witteveldt, J., Evans, D.J., Simmonds, P., 2014. The influence of CpG and UpA dinucleotide frequencies on RNA virus replication and characterization of the innate cellular pathways underlying virus attenuation and enhanced replication. Nucleic Acids Res. 42, 4527-4545.
    [5]
    Barreiro, L.B., Quintana-Murci, L., 2009. From evolutionary genetics to human immunology: how selection shapes host defence genes. Nat. Rev. Genet. 11, 17.
    [6]
    Bergelson, J.M., Chan, M., Solomon, K.R., St John, N.F., Lin, H., Finberg, R.W., 1994. Decay-accelerating factor (CD55), a glycosylphosphatidylinositol-anchored complement regulatory protein, is a receptor for several echoviruses. Proc. Natl. Acad. Sci. U.S.A. 91, 6245-6248.
    [7]
    Blanchette, M., Kent, W.J., Riemer, C., Elnitski, L., Smit, A.F.A., Roskin, K.M., Baertsch, R., Rosenbloom, K., Clawson, H., Green, E.D., Haussler, D., Miller, W., 2004. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14, 708-715.
    [8]
    Blanco-Melo, D., Venkatesh, S., Bieniasz, Paul D., 2012. Intrinsic cellular defenses against human immunodeficiency viruses. Immunity 37, 399-411.
    [9]
    Boliar, S., Gludish, D.W., Jambo, K.C., Kamng’ona, R., Mvaya, L., Mwandumba, H.C., Russell, D.G., 2019. Inhibition of the lncRNA SAF drives activation of apoptotic effector caspases in HIV-1-infected human macrophages. Proc. Natl. Acad. Sci. U.S.A., 201818662.
    [10]
    Bruscella, P., Bottini, S., Baudesson, C., Pawlotsky, J.M., Feray, C., Trabucchi, M., 2017. Viruses and miRNAs: More friends than foes. Front. Microbiol. 8, 824.
    [11]
    Burns, C.C., Campagnoli, R., Shaw, J., Vincent, A., Jorba, J., Kew, O., 2009. Genetic inactivation of Poliovirus infectivity by increasing the frequencies of CpG and UpA dinucleotides within and across synonymous capsid region codons. J. Virol. 83, 9957.
    [12]
    Casanova, J.-L., Abel, L., Quintana-Murci, L., 2013. Immunology taught by human genetics. Cold Spring Harb. Symp. Quant. Biol. 78, 157-172.
    [13]
    Chamary, J.V., Parmley, J.L., Hurst, L.D., 2006. Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat. Rev. Genet. 7, 98-108.
    [14]
    Cheng, X., Virk, N., Chen, W., Ji, S., Ji, S., Sun, Y., Wu, X., 2013. CpG usage in RNA viruses: Data and hypotheses. PLoS One 8, e74109.
    [15]
    Compton, A.A., Hirsch, V.M., Emerman, M., 2012. The host restriction factor APOBEC3G and retroviral Vif protein coevolve due to ongoing genetic conflict. Cell Host Microbe 11, 91-98.
    [16]
    Compton, A.A., Malik, H.S., Emerman, M., 2013. Host gene evolution traces the evolutionary history of ancient primate lentiviruses. Philosophical Transactions of the Royal Society of London B: Biological Sciences 368.
    [17]
    Daub, J.T., Moretti, S., Davydov, I.I., Excoffier, L., Robinson-Rechavi, M., 2017. Detection of pathways affected by positive selection in primate lineages ancestral to humans. Mol. Biol. Evol. 34, 1391-1402.
    [18]
    Daugherty, M.D., Malik, H.S., 2012. Rules of engagement: molecular insights from host-virus arms races. Annu. Rev. Genet. 46, 677-700.
    [19]
    Deaton, A.M., Bird, A., 2011. CpG islands and the regulation of transcription. Genes Dev. 25, 1010-1022.
    [20]
    Dorig, R.E., Marcil, A., Chopra, A., Richardson, C.D., 1993. The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75, 295-305.
    [21]
    Duggal, N.K., Emerman, M., 2012. Evolutionary conflicts between viruses and restriction factors shape immunity. Nat. Rev. Immunol. 12, 687-695.
    [22]
    Dutheil, J.Y., Gaillard, S., Stukenbrock, E.H., 2014. MafFilter: a highly flexible and extensible multiple genome alignment files processor. BMC Genom. 15, 53.
    [23]
    Fumagalli, M., Sironi, M., Pozzoli, U., Ferrer-Admettla, A., Pattini, L., Nielsen, R., 2011. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective oressure through human evolution. PLoS Genet. 7, e1002355.
    [24]
    Gaggar, A., Shayakhmetov, D.M., Lieber, A., 2003. CD46 is a cellular receptor for group B adenoviruses. Nat. Med. 9, 1408-1412.
    [25]
    Gaunt, E., Wise, H.M., Zhang, H., Lee, L.N., Atkinson, N.J., Nicol, M.Q., Highton, A.J., Klenerman, P., Beard, P.M., Dutia, B.M., 2016. Elevation of CpG frequencies in influenza A genome attenuates pathogenicity but enhances host response to infection. eLife 5, e12735.
    [26]
    Girardi, E., Lopez, P., Pfeffer, S., 2018. On the importance of host microRNAs during viral infection. Front. Genet. 9, 439.
    [27]
    Goldman, N., Yang, Z., 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 11, 725-736.
    [28]
    Goymer, P., 2007. Synonymous mutations break their silence. Nat. Rev. Genet. 8, 92.
    [29]
    Greenbaum, B.D., Cocco, S., Levine, A.J., Monasson, R., 2014. Quantitative theory of entropic forces acting on constrained nucleotide sequences applied to viruses. Proc. Natl. Acad. Sci. U.S.A. 111, 5054.
    [30]
    Greve, J.M., Davis, G., Meyer, A.M., Forte, C.P., Yost, S.C., Marlor, C.W., Kamarck, M.E., McClelland, A., 1989. The major human rhinovirus receptor is ICAM-1. Cell 56, 839-847.
    [31]
    Hamilton, W.D., Axelrod, R., Tanese, R., 1990. Sexual reproduction as an adaptation to resist parasites (a review). Proc. Natl. Acad. Sci. U.S.A. 87, 3566-3573.
    [32]
    Hodgkinson, A., Eyre-Walker, A., 2011. Variation in the mutation rate across mammalian genomes. Nat. Rev. Genet. 12, 756-766.
    [33]
    Hoover, K.C., Gokcumen, O., Qureshy, Z., Bruguera, E., Savangsuksa, A., Cobb, M., Matsunami, H., 2015. Global survey of variation in a human olfactory receptor gene reveals signatures of non-neutral evolution. Chem. Senses 40, 481-488.
    [34]
    Jiang, C., Han, L., Su, B., Li, W.H., Zhao, Z., 2007. Features and trend of loss of promoter-associated CpG islands in the human and mouse genomes. Mol. Biol. Evol. 24, 1991-2000.
    [35]
    Jiang, M., Zhang, S., Yang, Z., Lin, H., Zhu, J., Liu, L., Wang, W., Liu, S., Liu, W., Ma, Y., 2018. Self-recognition of an inducible host lncRNA by RIG-I feedback restricts innate immune response. Cell 173, 906-919. e913.
    [36]
    Karlin, S., Doerfler, W., Cardon, L.R., 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.
    [37]
    Karlin, S., Mrazek, J., 1997. Compositional differences within and between eukaryoticgenomes. Proc. Natl. Acad. Sci. U.S.A. 94, 10227-10232.
    [38]
    Karlsson, E.K., Kwiatkowski, D.P., Sabeti, P.C., 2014. Natural selection and infectious disease in human populations. Nat. Rev. Genet. 15, 379.
    [39]
    Karnauchow, T.M., Tolson, D.L., Harrison, B.A., Altman, E., Lublin, D.M., Dimock, K., 1996. The HeLa cell receptor for enterovirus 70 is decay-accelerating factor (CD55). J. Virol. 70, 5143-5152.
    [40]
    Kimchi-Sarfaty, C., Oh, J.M., Kim, I.W., Sauna, Z.E., Calcagno, A.M., Ambudkar, S.V., Gottesman, M.M., 2007. A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science 315, 525-528.
    [41]
    Kimura, T., Jiang, S., Nishizawa, M., Yoshigai, E., Hashimoto, I., Nishikawa, M., Okumura, T., Yamada, H., 2013. Stabilization of human interferon-α1 mRNA by its antisense RNA. Cell. Mol. Life Sci. 70, 1451-1467.
    [42]
    Kimura, T., Jiang, S., Yoshida, N., Sakamoto, R., Nishizawa, M., 2015. Interferon-alpha competing endogenous RNA network antagonizes microRNA-1270. Cell. Mol. Life Sci. 72, 2749-2761.
    [43]
    Kirchhoff, F., 2010. Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 8, 55-67.
    [44]
    Knox, B., Wang, Y., Rogers, L.J., Xuan, J., Yu, D., Guan, H., Chen, J., Shi, T., Ning, B., Kadlubar, S.A., 2018. A functional SNP in the 3'-UTR of TAP2 gene interacts with microRNA hsa-miR-1270 to suppress the gene expression. Environ. Mol. Mutagen. 59, 134-143.
    [45]
    Kondratowicz, A.S., Lennemann, N.J., Sinn, P.L., Davey, R.A., Hunt, C.L., Moller-Tank, S., Meyerholz, D.K., Rennert, P., Mullins, R.F., Brindley, M., Sandersfeld, L.M., Quinn, K., Weller, M., McCray, P.B., Jr., Chiorini, J., Maury, W., 2011. T-cell immunoglobulin and mucin domain 1 (TIM-1) is a receptor for Zaire Ebolavirus and Lake Victoria Marburgvirus. Proc. Natl. Acad. Sci. U.S.A. 108, 8426-8431.
    [46]
    Kosakovsky Pond, S.L., Frost, S.D., 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 22, 1208-1222.
    [47]
    Kosiol, C., Vinar, T., da Fonseca, R.R., Hubisz, M.J., Bustamante, C.D., Nielsen, R., Siepel, A., 2008. Patterns of positive selection in six mammalian genomes. PLoS Genet. 4, e1000144.
    [48]
    Kotzin, J.J., Iseka, F., Wright, J., Basavappa, M.G., Clark, M.L., Ali, M.A., Abdel-Hakeem, M.S., Robertson, T.F., Mowel, W.K., Joannas, L., Neal, V.D., Spencer, S.P., Syrett, C.M., Anguera, M.C., Williams, A., Wherry, E.J., Henao-Mejia, J., 2019. The long noncoding RNA Morrbid regulates CD8 T cells in response to viral infection. Proc. Natl. Acad. Sci. U.S.A.
    [49]
    Kozomara, A., Birgaoanu, M., Griffiths-Jones, S., 2018. miRBase: from microRNA sequences to function. Nucleic Acids Res. 47, D155-D162.
    [50]
    Laguette, N., Rahm, N., Sobhian, B., Chable-Bessia, C., Munch, J., Snoeck, J., Sauter, D., Switzer, W.M., Heneine, W., Kirchhoff, F., Delsuc, F., Telenti, A., Benkirane, M., 2012. Evolutionary and functional analyses of the interaction between the myeloid restriction factor SAMHD1 and the lentiviral Vpx protein. Cell Host Microbe 11, 205-217.
    [51]
    Larsen, R., Roekenes, T.P., Robertsen, B., 2004. Inhibition of infectious pancreatic necrosis virus replication by atlantic salmon Mx1 protein. J. Virol. 78, 7938.
    [52]
    Lasky, L.A., Nakamura, G., Smith, D.H., Fennie, C., Shimasaki, C., Patzer, E., Berman, P., Gregory, T., Capon, D.J., 1987. Delineation of a region of the human immunodeficiency virus type 1 gp120 glycoprotein critical for interaction with the CD4 receptor. Cell 50, 975-985.
    [53]
    Li, Z., Chao, T.-C., Chang, K.-Y., Lin, N., Patil, V.S., Shimizu, C., Head, S.R., Burns, J.C., Rana, T.M., 2014. The long noncoding RNA THRIL regulates TNFα expression through its interaction with hnRNPL. Proc. Natl. Acad. Sci. U.S.A. 111, 1002-1007.
    [54]
    Li, J., Chen, C., Ma, X., Geng, G., Liu, B., Zhang, Y., Zhang, S., Zhong, F., Liu, C., Yin, Y., Cai, W., Zhang, H., 2016. Long noncoding RNA NRON contributes to HIV-1 latency by specifically inducing tat protein degradation. Nat. Commun. 7.
    [55]
    Li, W.H., 1993. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 36, 96-99.
    [56]
    Li, M.M.H., Lau, Z., Cheung, P., Aguilar, E.G., Schneider, W.M., Bozzacco, L., Molina, H., Buehler, E., Takaoka, A., Rice, C.M., Felsenfeld, D.P., MacDonald, M.R., 2017. TRIM25 enhances the antiviral action of zinc-finger antiviral protein (ZAP). PLoS Pathog. 13, e1006145.
    [57]
    Li, W.H., Wu, C.I., Luo, C.C., 1985. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol. Biol. Evol. 2, 150-174.
    [58]
    Lim, E.S., Fregoso, O.I., McCoy, C.O., Matsen, F.A., Malik, H.S., Emerman, M., 2012. The ability of primate lentiviruses to degrade the monocyte restriction factor SAMHD1 preceded the birth of the viral accessory protein Vpx. Cell Host Microbe 11, 194-204.
    [59]
    Lim, E.S., Malik, H.S., Emerman, M., 2010. Ancient adaptive evolution of tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses. J. Virol. 84, 7124-7134.
    [60]
    Lin, H., Jiang, M., Liu, L., Yang, Z., Ma, Z., Liu, S., Ma, Y., Zhang, L., Cao, X., 2019. The long noncoding RNA Lnczc3h7a promotes a TRIM25-mediated RIG-I antiviral innate immune response. Nat. Immunol.
    [61]
    Lindblad-Toh, K., Garber, M., Zuk, O., Lin, M.F., Parker, B.J., Washietl, S., Kheradpour, P., Ernst, J., Jordan, G., Mauceli, E., Ward, L.D., Lowe, C.B., Holloway, A.K., Clamp, M., Gnerre, S., Alfoldi, J., Beal, K., Chang, J., Clawson, H., Cuff, J., Di Palma, F., Fitzgerald, S., Flicek, P., Guttman, M., Hubisz, M.J., Jaffe, D.B., Jungreis, I., Kent, W.J., Kostka, D., Lara, M., Martins, A.L., Massingham, T., Moltke, I., Raney, B.J., Rasmussen, M.D., Robinson, J., Stark, A., Vilella, A.J., Wen, J., Xie, X., Zody, M.C., Broad Institute Sequencing, P., Whole Genome Assembly, T., Baldwin, J., Bloom, T., Chin, C.W., Heiman, D., Nicol, R., Nusbaum, C., Young, S., Wilkinson, J, Worley, K.C, Kovar, C.L., Muzny, D.M., Gibbs, R.A., Baylor College of Medicine Human Gensome Sequencing Center Sequencing, T., Cree, A., Dihn, H.H., Fowler, G., Jhangiani, S., Joshi, V., Lee, S., Lewis, L.R., Nazareth, L.V., Okwuonu, G., Santibanez, J., Warren, Mardis, E.R., Weinstock, G.M., Wilson, R.K., Genome Institute at Washington, Delehaunty, K. Dooling, Fronik, C., Fulton, L., Fulton, B., Graves, T., Minx, P., Sodergren, E., Birney, E., Margulies, E.H., Herrero, J., Green, E.D., Haussler, D., Siepel, A., Goldman, N., Pollard, K.S., Pedersen, J.S., Lander, E.S., Kellis, M., 2011. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478, 476-482.
    [62]
    Liu, Y., Fu, Y., Wang, Q., Li, M., Zhou, Z., Dabbagh, D., Fu, C., Zhang, H., Li, S., Zhang, T., Gong, J., Kong, X., Zhai, W., Su, J., Sun, J., Zhang, Y., Yu, X.F., Shao, Z., Zhou, F., Wu, Y., Tan, X., 2019. Proteomic profiling of HIV-1 infection of human CD4(+) T cells identifies PSGL-1 as an HIV restriction factor. Nat. Microbiol. 4, 813-825.
    [63]
    Lodge, R., Ferreira Barbosa, J.A., Lombard-Vadnais, F., Gilmore, J.C., Deshiere, A., Gosselin, A., Wiche Salinas, T.R., Bego, M.G., Power, C., Routy, J.P., Ancuta, P., Tremblay, M.J., Cohen, E.A., 2017. Host microRNAs-221 and -222 inhibit HIV-1 entry in macrophages by targeting the CD4 viral receptor. Cell Rep. 21, 141-153.
    [64]
    Londrigan, S.L., Turville, S.G., Tate, M.D., Deng, Y.M., Brooks, A.G., Reading, P.C., 2011. N-linked glycosylation facilitates sialic acid-independent attachment and entry of influenza A viruses into cells expressing DC-SIGN or L-SIGN. J. Virol. 85, 2990-3000.
    [65]
    Love, M.I., Huber, W., Anders, S., 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550.
    [66]
    Ma, R., Wang, C., Wang, J., Wang, D., Xu, J., 2016. miRNA-mRNA Interaction Network in Non-small Cell Lung Cancer. Interdisciplinary Sciences: Computational Life Sciences 8, 209-219.
    [67]
    Maenner, S., Muller, M., Frohlich, J., Langer, D., Becker, Peter B., 2013. ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. Mol. Cell 51, 174-184.
    [68]
    Makova, K.D., Hardison, R.C., 2015. The effects of chromatin organization on variation in mutation rates in the genome. Nat. Rev. Genet. 16, 213-223.
    [69]
    Malik, H.S., Bayes, J.J., 2006. Genetic conflicts during meiosis and the evolutionary origins of centromere complexity. Behav. Ecol. Sociobiol. 34, 569.
    [70]
    Malim, M.H., Emerman, M., 2008. HIV-1 Accessory Proteins-Ensuring Viral Survival in a Hostile Environment. Cell Host Microbe 3, 388-398.
    [71]
    Mangeat, B., Turelli, P., Caron, G., Friedli, M., Perrin, L., Trono, D., 2003. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424, 99-103.
    [72]
    Martin, M., 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. journal 17, 10-12.
    [73]
    McNatt, M.W., Zang, T., Hatziioannou, T., Bartlett, M., Fofana, I.B., Johnson, W.E., Neil, S.J., Bieniasz, P.D., 2009. Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog. 5, e1000300.
    [74]
    Mitchell, P.S., Patzina, C., Emerman, M., Haller, O., Malik, H.S., Kochs, G., 2012. Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12, 598-604.
    [75]
    Miyata, T., Yasunaga, T., 1980. Molecular evolution of mRNA: a method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application. J. Mol. Evol. 16, 23-36.
    [76]
    Mourtada-Maarabouni, M., Hedge, V.L., Kirkham, L., Farzaneh, F., Williams, G.T., 2008. Growth arrest in human T-cells is controlled by the non-coding RNA growth-arrest-specific transcript 5 (GAS5). Journal of cell science 121, 939-946.
    [77]
    Muller, U., Steinhoff, U., Reis, L., Hemmi, S., Pavlovic, J., Zinkernagel, R., Aguet, M., 1994. Functional role of type I and type II interferons in antiviral defense. Science 264, 1918-1921.
    [78]
    Muse, S.V., Gaut, B.S., 1994. A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol. Biol. Evol. 11, 715-724.
    [79]
    Nei, M., Gojobori, T., 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418-426.
    [80]
    Neil, S.J.D., Zang, T., Bieniasz, P.D., 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425.
    [81]
    Nguyen, T.H., Liu, X., Su, Z.Z., Hsu, A.C., Foster, P.S., Yang, M., 2018. Potential role of microRNAs in the regulation of antiviral responses to influenza infection. Front. Immunol. 9, 1541.
    [82]
    Nickel, G.C., Tefft, D., Adams, M.D., 2007. Human PAML browser: a database of positive selection on human genes using phylogenetic methods. Nucleic Acids Res. 36, D800-D808.
    [83]
    Nielsen, R., Bustamante, C., Clark, A.G., Glanowski, S., Sackton, T.B., Hubisz, M.J., Fledel-Alon, A., Tanenbaum, D.M., Civello, D., White, T.J., J, J.S., Adams, M.D., Cargill, M., 2005. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS. Biol. 3, e170.
    [84]
    Nishimura, Y., Shimojima, M., Tano, Y., Miyamura, T., Wakita, T., Shimizu, H., 2009. Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat. Med. 15, 794.
    [85]
    Ogembo, J.G., Kannan, L., Ghiran, I., Nicholson-Weller, A., Finberg, R.W., Tsokos, George C., Fingeroth, Joyce D., 2013. Human complement receptor type 1/CD35 Is an Epstein-Barr virus receptor. Cell Rep. 3, 371-385.
    [86]
    Pal, C., Macia, M.D., Oliver, A., Schachar, I., Buckling, A., 2007. Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 450, 1079-1081.
    [87]
    Paradis, E., Claude, J., Strimmer, K., 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290.
    [88]
    Perez, J.T., Garcia-Sastre, A., Manicassamy, B., 2013. Insertion of a GFP reporter gene in influenza virus. Curr. Protoc. Microbiol. Chapter 15, Unit 15G.14.
    [89]
    Pheasant, M., Mattick, J.S., 2007. Raising the estimate of functional human sequences. Genome Res. 17, 1245-1253.
    [90]
    Pohl, A., Beato, M., 2014. bwtool: a tool for bigWig files. Bioinformatics 30, 1618-1619.
    [91]
    Pollard, K.S., Hubisz, M.J., Rosenbloom, K.R., Siepel, A., 2010. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res. 20, 110-121.
    [92]
    Pollard, K.S., Salama, S.R., Lambert, N., Lambot, M.A., Coppens, S., Pedersen, J.S., Katzman, S., King, B., Onodera, C., Siepel, A., Kern, A.D., Dehay, C., Igel, H., Ares, M., Jr., Vanderhaeghen, P., Haussler, D., 2006. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443, 167-172.
    [93]
    Quintana-Murci, L., 2019. Human immunology through the lens of evolutionary genetics. Cell 177, 184-199.
    [94]
    Ramani, R., Krumholz, K., Huang, Y.-F., Siepel, A., 2018. PhastWeb: a web interface for evolutionary conservation scoring of multiple sequence alignments using phastCons and phyloP. Bioinformatics 35, 2320-2322.
    [95]
    Rothenburg, S., Seo, E.J., Gibbs, J.S., Dever, T.E., Dittmar, K., 2008. Rapid evolution of protein kinase PKR alters sensitivity to viral inhibitors. Nat. Struct. Mol. Biol. 16, 63.
    [96]
    Santoro, F., Kennedy, P.E., Locatelli, G., Malnati, M.S., Berger, E.A., Lusso, P., 1999. CD46 is a cellular receptor for human herpesvirus 6. Cell 99, 817-827.
    [97]
    Sawyer, S.L., Wu, L.I., Emerman, M., Malik, H.S., 2005. Positive selection of primate TRIM5α identifies a critical species-specific retroviral restriction domain. Proc. Natl. Acad. Sci. U.S.A. 102, 2832.
    [98]
    Saxonov, S., Berg, P., Brutlag, D.L., 2006. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc. Natl. Acad. Sci. U.S.A. 103, 1412.
    [99]
    Schwefel, D., Boucherit, Virginie C., Christodoulou, E., Walker, Philip A., Stoye, Jonathan P., Bishop, Kate N., Taylor, Ian A., 2015. Molecular determinants for recognition of divergent SAMHD1 proteins by the lentiviral accessory protein Vpx. Cell Host Microbe 17, 489-499.
    [100]
    Short, J.J., Vasu, C., Holterman, M.J., Curiel, D.T., Pereboev, A., 2006. Members of adenovirus species B utilize CD80 and CD86 as cellular attachment receptors. Virus Res. 122, 144-153.
    [101]
    Shultz, A.J., Sackton, T.B., 2019. Immune genes are hotspots of shared positive selection across birds and mammals. eLife 8, e41815.
    [102]
    Siepel, A., Bejerano, G., Pedersen, J.S., Hinrichs, A.S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L.W., Richards, S., 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034-1050.
    [103]
    Sironi, M., Cagliani, R., Forni, D., Clerici, M., 2015. Evolutionary insights into host-pathogen interactions from mammalian sequence data. Nat. Rev. Genet. 16, 224-236.
    [104]
    Staunton, D.E., Merluzzi, V.J., Rothlein, R., Barton, R., Marlin, S.D., Springer, T.A., 1989. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56, 849-853.
    [105]
    Stremlau, M., Owens, C.M., Perron, M.J., Kiessling, M., Autissier, P., Sodroski, J., 2004. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427, 848.
    [106]
    Takata, M.A., Goncalves-Carneiro, D., Zang, T.M., Soll, S.J., York, A., Blanco-Melo, D., Bieniasz, P.D., 2017. CG dinucleotide suppression enables antiviral defence targeting non-self RNA. Nature 550, 124-127.
    [107]
    Tambyah, P.A., Ching, C.S., Sepramaniam, S., Ali, J.M., Armugam, A., Jeyaseelan, K., 2016. microRNA expression in blood of dengue patients. Ann. Clin. Biochem. 53, 466-476.
    [108]
    Trobaugh, D.W., Klimstra, W.B., 2017. MicroRNA regulation of RNA virus replication and pathogenesis. Trends Mol. Med 23, 80-93.
    [109]
    Tulloch, F., Atkinson, N.J., Evans, D.J., Ryan, M.D., Simmonds, P., 2014. RNA virus attenuation by codon pair deoptimisation is an artefact of increases in CpG/UpA dinucleotide frequencies. elife 3, e04531.
    [110]
    van der Lee, R., Wiel, L., van Dam, T.J.P., Huynen, M.A., 2017. Genome-scale detection of positive selection in nine primates predicts human-virus evolutionary conflicts. Nucleic Acids Res. 45, 10634-10648.
    [111]
    Vitti, J.J., Grossman, S.R., Sabeti, P.C., 2013. Detecting natural selection in genomic data. Annu. Rev. Genet. 47, 97-120.
    [112]
    Wang, N., Dong, Q., Li, J., Jangra, R.K., Fan, M., Brasier, A.R., Lemon, S.M., Pfeffer, L.M., Li, K., 2010. Viral induction of the zinc finger antiviral protein is IRF3-dependent but NF-κB-independent. J. Biol. Chem. 285, 6080-6090.
    [113]
    Wang, P., Xu, J., Wang, Y., Cao, X., 2017. An interferon-independent lncRNA promotes viral replication by modulating cellular metabolism. Science 358, 1051.
    [114]
    Wang, P., Xue, Y., Han, Y., Lin, L., Wu, C., Xu, S., Jiang, Z., Xu, J., Liu, Q., Cao, X., 2014. The STAT3-binding long noncoding RNA lnc-DC controls human dendritic cell differentiation. Science 344, 310-313.
    [115]
    Wang, Y., Fan, J., Yang, H., Chen, J., 2012. Changes of microRNA expression profiles in Vero cells induced by HSV-2 LAT overexpression. Journal of Southern Medical University 32, 1440-1444.
    [116]
    Wong, W.S.W., Nielsen, R., 2004. Detecting selection in noncoding regions of nucleotide sequences. Genetics 167, 949.
    [117]
    Yan, N., Chen, Z.J., 2012. Intrinsic antiviral immunity. Nat. Immunol. 13, 214.
    [118]
    Yang, Z., 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15, 568-573.
    [119]
    Yang, Z., 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591.
    [120]
    Yi, T., Zhou, X., Sang, K., Zhou, J., Ge, L., 2019. MicroRNA-1270 modulates papillary thyroid cancer cell development by regulating SCAI. Biomed. Pharmacother. 109, 2357-2364.
    [121]
    Zerbino, D.R., Wilder, S.P., Johnson, N., Juettemann, T., Flicek, P.R., 2015. The ensembl regulatory build, Genome Biol., p. 56.
    [122]
    Zhao, Z., Han, C., Liu, J., Wang, C., Wang, Y., Cheng, L.J.M.m.r., 2014. GPC5, a tumor suppressor, is regulated by miR-620 in lung adenocarcinoma. 9, 2540-2546.
    [123]
    Zhao, Z., Jiang, C., 2007. Methylation-dependent transition rates are dependent on local sequence lengths and genomic regions. Mol. Biol. Evol. 24, 23-25.
    [124]
    Zheng, X., Wang, X., Tu, F., Wang, Q., Fan, Z., Gao, G., 2017. TRIM25 is required for the antiviral activity of zinc finger antiviral protein. J. Virol. 91, e00088-00017.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures (6)

    Article Metrics

    Article views (93) PDF downloads (2) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return