Molecular modeling and dynamic simulation of chicken Mx protein with the S631N polymorphism

References

• Alvarez, F. J. D., He, S., Perilla, J. R., Jang, S., Schulten, K., Engelman, A. N., Scheres, S. H. W., & Zhang, P. (2017). CryoEM structure of MxB reveals a novel oligomerization interface critical for HIV restriction. Science Advances, 3(9), e1701264. https://doi.org/https://doi.org/10.1126/sciadv.1701264
   PubMed Web of Science ®Google Scholar
• Amadei, A., Ceruso, M. A., & Di Nola, A. (1999). On the convergence of the conformational coordinates basis set obtained by the essential dynamics analysis of proteins' molecular dynamics simulations. Proteins: Structure, Function, and Genetics, 36(4), 419–424. https://doi.org/https://doi.org/10.1002/(SICI)1097-0134(19990901)36:4<419::AID-PROT5>3.0.CO;2-U
   PubMed Web of Science ®Google Scholar
• Bazzigher, L., Schwarz, A., & Staeheli, P. (1993). No enhanced influenza virus resistance of murine and avian cells expressing cloned duck Mx protein. Virology, 195(1), 100–112. https://doi.org/https://doi.org/10.1006/viro.1993.1350
   PubMed Web of Science ®Google Scholar
• Benfield, C. T. O., Lyall, J. W., Kochs, G., & Tiley, L. S. (2008). Asparagine 631 variants of the chicken Mx protein do not inhibit influenza virus replication in primary chicken embryo fibroblasts or in vitro surrogate assays. Journal of Virology, 82(15), 7533–7539. https://doi.org/https://doi.org/10.1128/JVI.00185-08
   PubMed Web of Science ®Google Scholar
• Bernasconi, D., Schultz, U., & Staeheli, P. (1995). The interferon-induced Mx protein of chickens lacks antiviral activity. Journal of Interferon & Cytokine Research, 15(1), 47–53. https://doi.org/https://doi.org/10.1089/jir.1995.15.47
   PubMed Web of Science ®Google Scholar
• Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. The Journal of Chemical Physics, 126(1), 14101. https://doi.org/https://doi.org/10.1063/1.2408420
   PubMed Web of Science ®Google Scholar
• Chakrabarty, B., & Parekh, N. (2016). NAPS: Network Analysis of Protein Structures. Nucleic Acids Research, 44(W1), W375–W382. https://doi.org/https://doi.org/10.1093/nar/gkw383
   PubMed Web of Science ®Google Scholar
• Chen, Y., Zhang, L., Graf, L., Yu, B., Liu, Y., Kochs, G., Zhao, Y., & Gao, S. (2017). Conformational dynamics of dynamin-like MxA revealed by single-molecule FRET. Nature Communications, 8, 15744. https://doi.org/https://doi.org/10.1038/ncomms15744
   PubMed Web of Science ®Google Scholar
• Dillon, D., & Runstadler, J. (2010). Mx gene diversity and influenza association among five wild dabbling duck species (Anas spp.) in Alaska. Infection, Genetics and Evolution, 10(7), 1085–1093. https://doi.org/https://doi.org/10.1016/j.meegid.2010.07.004
   PubMed Web of Science ®Google Scholar
• Ewald, S. J., Kapczynski, D. R., Livant, E. J., Suarez, D. L., Ralph, J., McLeod, S., & Miller, C. (2011). Association of Mx1 Asn631 variant alleles with reductions in morbidity, early mortality, viral shedding, and cytokine responses in chickens infected with a highly pathogenic avian influenza virus. Immunogenetics, 63(6), 363–375. https://doi.org/https://doi.org/10.1007/s00251-010-0509-1
   PubMed Web of Science ®Google Scholar
• Gao, S., von der Malsburg, A., Dick, A., Faelber, K., Schroder, G. F., Haller, O., Kochs, G., & Daumke, O. (2011). Structure of myxovirus resistance protein a reveals intra- and intermolecular domain interactions required for the antiviral function. Immunity, 35(4), 514–525. https://doi.org/https://doi.org/10.1016/j.immuni.2011.07.012
   PubMed Web of Science ®Google Scholar
• Girdlestone, C., & Hayward, S. (2016). The DynDom3D webserver for the analysis of domain movements in multimeric proteins. Journal of Computational Biology: A Journal of Computational Molecular Cell Biology, 23(1), 21–26. https://doi.org/https://doi.org/10.1089/cmb.2015.0143
   PubMed Web of Science ®Google Scholar
• Gosu, V., Son, S., Shin, D., & Song, K.-D. (2019). Insights into the dynamic nature of the dsRNA-bound TLR3 complex. Scientific Reports, 9(1), 3652. https://doi.org/https://doi.org/10.1038/s41598-019-39984-8
   PubMed Web of Science ®Google Scholar
• Gosu, V., Won, K., Oh, J. D., & Shin, D. (2020). Conformational changes induced by S34Y and R98C variants in the death domain of Myd88. Frontiers in Molecular Biosciences, 7, 27. https://doi.org/https://doi.org/10.3389/fmolb.2020.00027
   PubMed Web of Science ®Google Scholar
• Goujon, C., Moncorge, O., Bauby, H., Doyle, T., Ward, C. C., Schaller, T., Hue, S., Barclay, W. S., Schulz, R., & Malim, M. H. (2013). Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature, 502(7472), 559–562. https://doi.org/https://doi.org/10.1038/nature12542
   PubMed Web of Science ®Google Scholar
• Haller, O., & Kochs, G. (2002). Interferon-induced mx proteins: Dynamin-like GTPases with antiviral activity. Traffic (Copenhagen, Denmark), 3(10), 710–717. https://doi.org/https://doi.org/10.1034/j.1600-0854.2002.31003.x
   PubMed Web of Science ®Google Scholar
• Haller, O., & Kochs, G. (2011). Human MxA protein: An interferon-induced dynamin-like GTPase with broad antiviral activity. Journal of Interferon & Cytokine Research: The Official Journal of the International Society for Interferon and Cytokine Research, 31(1), 79–87. https://doi.org/https://doi.org/10.1089/jir.2010.0076
   PubMed Web of Science ®Google Scholar
• Haller, O., Staeheli, P., Schwemmle, M., & Kochs, G. (2015). Mx GTPases: Dynamin-like antiviral machines of innate immunity. Trends in Microbiology, 23(3), 154–163. https://doi.org/https://doi.org/10.1016/j.tim.2014.12.003
   PubMed Web of Science ®Google Scholar
• Haller, O., Stertz, S., & Kochs, G. (2007). The Mx GTPase family of interferon-induced antiviral proteins. Microbes and Infection, 9(14–15), 1636–1643. https://doi.org/https://doi.org/10.1016/j.micinf.2007.09.010
   PubMed Web of Science ®Google Scholar
• Hamby, S. E., & Hirst, J. D. (2008). Prediction of glycosylation sites using random forests. BMC Bioinformatics, 9, 500. https://doi.org/https://doi.org/10.1186/1471-2105-9-500
   PubMed Web of Science ®Google Scholar
• Hayward, S. (1999). Structural principles governing domain motions in proteins. Proteins: Structure, Function, and Genetics, 36(4), 425–435. https://doi.org/https://doi.org/10.1002/(SICI)1097-0134(19990901)36:4<425::AID-PROT6>3.0.CO;2-S
   PubMed Web of Science ®Google Scholar
• Hayward, S., & Berendsen, H. J. (1998). Systematic analysis of domain motions in proteins from conformational change: New results on citrate synthase and T4 lysozyme. Proteins: Structure, Function, and Genetics, 30(2), 144–154. https://doi.org/https://doi.org/10.1002/(SICI)1097-0134(19980201)30:2<144::AID-PROT4>3.0.CO;2-N
   PubMed Web of Science ®Google Scholar
• Kane, M., Yadav, S. S., Bitzegeio, J., Kutluay, S. B., Zang, T., Wilson, S. J., Schoggins, J. W., Rice, C. M., Yamashita, M., Hatziioannou, T., & Bieniasz, P. D. (2013). MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature, 502(7472), 563–566. https://doi.org/https://doi.org/10.1038/nature12653
   PubMed Web of Science ®Google Scholar
• Ko, J. H., Takada, A., Mitsuhashi, T., Agui, T., & Watanabe, T. (2004). Native antiviral specificity of chicken Mx protein depends on amino acid variation at position 631. Animal Genetics, 35(2), 119–122. https://doi.org/https://doi.org/10.1111/j.1365-2052.2004.01096.x
   PubMed Web of Science ®Google Scholar
• Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J. L., Dror, R. O., & Shaw, D. E. (2010). Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins, 78(8), 1950–1958. https://doi.org/https://doi.org/10.1002/prot.22711
   PubMed Web of Science ®Google Scholar
• Liu, Z., Pan, Q., Ding, S., Qian, J., Xu, F., Zhou, J., Cen, S., Guo, F., & Liang, C. (2013). The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host & Microbe, 14(4), 398–410. https://doi.org/https://doi.org/10.1016/j.chom.2013.08.015
   PubMed Web of Science ®Google Scholar
• Muller, U., Steinhoff, U., Reis, L. F., Hemmi, S., Pavlovic, J., Zinkernagel, R. M., & Aguet, M. (1994). Functional role of type I and type II interferons in antiviral defense. Science (New York, N.Y.), 264(5167), 1918–1921. https://doi.org/https://doi.org/10.1126/science.8009221
   PubMed Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/https://doi.org/10.1063/1.328693
   Web of Science ®Google Scholar
• Pavlovic, J., & Staeheli, P. (1991). The antiviral potentials of Mx proteins. Journal of Interferon Research, 11(4), 215–219. https://doi.org/https://doi.org/10.1089/jir.1991.11.215
   PubMedGoogle Scholar
• Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England), 29(7), 845–854. https://doi.org/https://doi.org/10.1093/bioinformatics/btt055
   PubMed Web of Science ®Google Scholar
• Rothman, J. H., Raymond, C. K., Gilbert, T., O'Hara, P. J., & Stevens, T. H. (1990). A putative GTP binding protein homologous to interferon-inducible Mx proteins performs an essential function in yeast protein sorting. Cell, 61(6), 1063–1074. https://doi.org/https://doi.org/10.1016/0092-8674(90)90070-U
   PubMed Web of Science ®Google Scholar
• Roy, A., Kucukural, A., & Zhang, Y. (2010). I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols, 5(4), 725–738. https://doi.org/https://doi.org/10.1038/nprot.2010.5
   PubMed Web of Science ®Google Scholar
• Sasaki, K., Yoneda, A., Ninomiya, A., Kawahara, M., & Watanabe, T. (2013). Both antiviral activity and intracellular localization of chicken Mx protein depend on a polymorphism at amino acid position 631. Biochemical and Biophysical Research Communications, 430(1), 161–166. https://doi.org/https://doi.org/10.1016/j.bbrc.2012.11.053
   PubMed Web of Science ®Google Scholar
• Schusser, B., Reuter, A., von der Malsburg, A., Penski, N., Weigend, S., Kaspers, B., Staeheli, P., & Härtle, S. (2011). Mx is dispensable for interferon-mediated resistance of chicken cells against influenza A virus. Journal of Virology, 85(16), 8307–8315. https://doi.org/https://doi.org/10.1128/JVI.00535-11
   PubMed Web of Science ®Google Scholar
• Sneha, P., Kumar Thirumal, D., Tanwar, H., Siva, R., George Priya Doss, C., & Zayed, H. (2017). Structural analysis of G1691S variant in the human filamin B gene responsible for Larsen Syndrome: A comparative computational approach. Journal of Cellular Biochemistry, 118(7), 1900–1910. https://doi.org/https://doi.org/10.1002/jcb.25920
   PubMed Web of Science ®Google Scholar
• Staeheli, P. (1990). Interferon-induced proteins and the antiviral state. Advances in Virus Research, 38, 147–200. https://doi.org/https://doi.org/10.1016/s0065-3527(08)60862-3
   PubMedGoogle Scholar
• Thirumal Kumar, D., & George Priya Doss, C. (2017). Role of E542 and E545 missense mutations of PIK3CA in breast cancer: A comparative computational approach. Journal of Biomolecular Structure & Dynamics, 35(12), 2745–2757. https://doi.org/https://doi.org/10.1080/07391102.2016.1231082
   PubMed Web of Science ®Google Scholar
• Thirumal Kumar, D., George Priya Doss, C., Sneha, P., Tayubi, I. A., Siva, R., Chakraborty, C., & Magesh, R. (2017). Influence of V54M mutation in giant muscle protein titin: A computational screening and molecular dynamics approach. Journal of Biomolecular Structure & Dynamics, 35(5), 917–928. https://doi.org/https://doi.org/10.1080/07391102.2016.1166456
   PubMed Web of Science ®Google Scholar
• van Aalten, D. M., Findlay, J. B., Amadei, A., & Berendsen, H. J. (1995). Essential dynamics of the cellular retinol-binding protein-evidence for ligand-induced conformational changes. Protein Engineering, 8(11), 1129–1135. https://doi.org/https://doi.org/10.1093/protein/8.11.1129
   PubMedGoogle Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/https://doi.org/10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Wang, Y., Brahmakshatriya, V., Lupiani, B., Reddy, S., Okimoto, R., Li, X., Chiang, H., & Zhou, H. (2012). Associations of chicken Mx1 polymorphism with antiviral responses in avian influenza virus infected embryos and broilers. Poultry Science, 91(12), 3019–3024. https://doi.org/https://doi.org/10.3382/ps.2012-02471
   PubMed Web of Science ®Google Scholar
• Xu, D., & Zhang, Y. (2011). Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophysical Journal, 101(10), 2525–2534. https://doi.org/https://doi.org/10.1016/j.bpj.2011.10.024
   PubMed Web of Science ®Google Scholar
• Yamaguchi, H., van Aalten, D. M., Pinak, M., Furukawa, A., & Osman, R. (1998). Essential dynamics of DNA containing a cis.syn cyclobutane thymine dimer lesion. Nucleic Acids Research, 26(8), 1939–1946. https://doi.org/https://doi.org/10.1093/nar/26.8.1939
   PubMed Web of Science ®Google Scholar
• Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015). The I-TASSER Suite: Protein structure and function prediction. Nature Methods, 12(1), 7–8. https://doi.org/https://doi.org/10.1038/nmeth.3213
   PubMed Web of Science ®Google Scholar
• Zürcher, T., Pavlovic, J., & Staeheli, P. (1992). Nuclear localization of mouse Mx1 protein is necessary for inhibition of influenza virus. Journal of Virology, 66(8), 5059–5066. https://doi.org/https://doi.org/10.1128/JVI.66.8.5059-5066.1992
   PubMed Web of Science ®Google Scholar