Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017 (2017), Article ID 1734151, 15 pages
https://doi.org/10.1155/2017/1734151
Research Article

New Targets for Zika Virus Determined by Human-Viral Interactomic: A Bioinformatics Approach

1Universidade Católica Portuguesa, Center for Interdisciplinary Research in Health (CIIS), Institute of Health Sciences (ICS), Viseu, Portugal
2Department of Informatics Engineering (DEI), Centre for Informatics and Systems of the University of Coimbra (CISUC), University of Coimbra, Coimbra, Portugal

Correspondence should be addressed to Marlene Barros

Received 2 May 2017; Revised 6 October 2017; Accepted 11 October 2017; Published 12 December 2017

Academic Editor: Momiao Xiong

Copyright © 2017 Eduardo Esteves et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V.-M. Cao-Lormeau, A. Blake, S. Mons et al., “Guillain-barré syndrome outbreak associated with zika virus infection in french polynesia: a case-control study,” The Lancet, vol. 387, no. 10027, pp. 1531–1539, 2016. View at Publisher · View at Google Scholar · View at Scopus
  2. C. S. De Oliveira and P. F. Da Costa Vasconcelos, “Microcephaly and Zika virus,” Jornal de Pediatria, vol. 92, no. 2, pp. 103–105, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. A. S. Fauci and D. M. Morens, “Zika virus in the americas—yet another arbovirus threat,” The New England Journal of Medicine, vol. 374, no. 7, pp. 601–604, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. E. A. Gould and T. Solomon, “Pathogenic flaviviruses,” The Lancet, vol. 371, no. 9611, pp. 500–509, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. J. S. Mackenzie, D. J. Gubler, and L. R. Petersen, “Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses,” Nature Medicine, vol. 10, no. 12, pp. S98–S109, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Oehler, L. Watrin, P. Larre et al., “Zika virus infection complicated by Guillain-Barré syndrome – case report, French Polynesia, December 2013,” Eurosurveillance, vol. 19, no. 9, 2014. View at Publisher · View at Google Scholar
  7. C. V. Ventura, M. Maia, V. Bravo-Filho, A. L. Góis, and R. Belfort, “Zika virus in Brazil and macular atrophy in a child with microcephaly,” The Lancet, vol. 387, no. 10015, p. 228, 2016. View at Publisher · View at Google Scholar · View at Scopus
  8. S. L. Cumberworth, J. J. Clark, A. Kohl, and C. L. Donald, “Inhibition of type I interferon induction and signalling by mosquito-borne flaviviruses,” Cellular Microbiology, vol. 19, no. 5, Article ID e12737, 2017. View at Publisher · View at Google Scholar · View at Scopus
  9. B. D. Lindenbach and C. M. Rice, “Molecular biology of flaviviruses,” Advances in Virus Research, vol. 59, pp. 23–61, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Mukhopadhyay, R. J. Kuhn, and M. G. Rossmann, “A structural perspective of the Flavivirus life cycle,” Nature Reviews Microbiology, vol. 3, no. 1, pp. 13–22, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. J. N. Conde, E. M. Silva, A. S. Barbosa, and R. Mohana-Borges, “The complement system in flavivirus infections,” Frontiers in Microbiology, vol. 8, article no. 213, 2017. View at Publisher · View at Google Scholar · View at Scopus
  12. N. K. Routhu and S. N. Byrareddy, “Host-Virus Interaction of ZIKA Virus in Modulating Disease Pathogenesis,” Journal of Neuroimmune Pharmacology, vol. 12, no. 2, pp. 219–232, 2017. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Wu, Q. Liu, J. Zhou et al., “Zika virus evades interferon-mediated antiviral response through the co-operation of multiple nonstructural proteins in vitro,” Cell Discovery, vol. 3, p. 17006, 2017. View at Publisher · View at Google Scholar
  14. L. Meertens, X. Carnec, M. P. Lecoin et al., “The TIM and TAM families of phosphatidylserine receptors mediate dengue virus entry,” Cell Host & Microbe, vol. 12, no. 4, pp. 544–557, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Lemke and C. V. Rothlin, “Immunobiology of the TAM receptors,” Nature Reviews Immunology, vol. 8, no. 5, pp. 327–336, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. C. V. Rothlin, S. Ghosh, E. I. Zuniga, M. B. A. Oldstone, and G. Lemke, “TAM Receptors Are Pleiotropic Inhibitors of the Innate Immune Response,” Cell, vol. 131, no. 6, pp. 1124–1136, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Hamel, O. Dejarnac, S. Wichit et al., “Biology of Zika virus infection in human skin cells,” Journal of Virology, vol. 89, no. 17, pp. 8880–8896, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. P. P. Garcez, E. C. Loiola, R. M. Da Costa et al., “Zika virus impairs growth in human neurospheres and brain organoids,” Science, vol. 352, no. 6287, pp. 816–818, 2016. View at Publisher · View at Google Scholar · View at Scopus
  19. Q. Shao, S. Herrlinger, S.-L. Yang et al., “Zika virus infection disrupts neurovascular development and results in postnatal microcephaly with brain damage,” Development, vol. 143, no. 22, pp. 4127–4136, 2016. View at Publisher · View at Google Scholar · View at Scopus
  20. M. F. Wells, M. R. Salick, O. Wiskow et al., “Genetic Ablation of AXL Does Not Protect Human Neural Progenitor Cells and Cerebral Organoids from Zika Virus Infection,” Cell Stem Cell, vol. 19, no. 6, pp. 703–708, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Gerold, J. Bruening, B. Weigel, and T. Pietschmann, “Protein interactions during the Flavivirus and hepacivirus life cycle,” Molecular & Cellular Proteomics, vol. 16, no. 4, pp. S75–S91, 2017. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Miller and J. Krijnse-Locker, “Modification of intracellular membrane structures for virus replication,” Nature Reviews Microbiology, vol. 6, no. 5, pp. 363–374, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. D. A. Muller and P. R. Young, “The flavivirus NS1 protein: molecular and structural biology, immunology, role in pathogenesis and application as a diagnostic biomarker,” Antiviral Research, vol. 98, no. 2, pp. 192–208, 2013. View at Publisher · View at Google Scholar
  24. M. A. Edeling, M. S. Diamond, and D. H. Fremont, “Structural basis of flavivirus NS1 assembly and antibody recognition,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 111, no. 11, pp. 4285–4290, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Zhang, C. Hammack, S. C. Ogden et al., “Molecular signatures associated with ZIKV exposure in human cortical neural progenitors,” Nucleic Acids Research, vol. 44, no. 18, pp. 8610–8620, 2016. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Falgout and L. Markoff, “Evidence that flavivirus NS1-NS2A cleavage is mediated by a membrane- bound host protease in the endoplasmic reticulum,” Journal of Virology, vol. 69, no. 11, pp. 7232–7243, 1995. View at Google Scholar · View at Scopus
  27. M. J. Pryor and P. J. Wright, “Glycosylation mutants of dengue virus NS1 protein,” Journal of General Virology, vol. 75, no. 5, pp. 1183–1187, 1994. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Winkler, S. E. Maxwell, C. Ruemmler, and V. Stollar, “Newly synthesized dengue-2 virus nonstructural protein NS1 is a soluble protein but becomes partially hydrophobic and membrane-associated after dimerization,” Virology, vol. 171, no. 1, pp. 302–305, 1989. View at Publisher · View at Google Scholar · View at Scopus
  29. J. J. Schlesinger, M. W. Brandriss, J. R. Putnak, and E. E. Walsh, “Cell surface expression of yellow fever virus non-structural glycoprotein NS1: Consequences of interaction with antibody,” Journal of General Virology, vol. 71, no. 3, pp. 593–599, 1990. View at Publisher · View at Google Scholar · View at Scopus
  30. M. G. Jacobs, P. J. Robinson, C. Bletchly, J. M. Mackenzie, and P. R. Young, “Dengue virus nonstructural protein 1 is expressed in a glycosyl-phosphatidylinositol-linked form that is capable of signal transduction,” The FASEB Journal, vol. 14, no. 11, pp. 1603–1610, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. A. J. Crooks, J. M. Lee, A. B. Dowsett, and J. R. Stephenson, “Purification and analysis of infectious virions and native non-structural antigens from cells infected with tick-borne encephalitis virus,” Journal of Chromatography A, vol. 502, no. C, pp. 59–68, 1990. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Flamand, F. Megret, M. Mathieu, J. Lepault, F. A. Rey, and V. Deubel, “Dengue virus type 1 nonstructural glycoprotein NS1 is secreted from mammalian cells as a soluble hexamer in a glycosylation-dependent fashion,” Journal of Virology, vol. 73, no. 7, pp. 6104–6110, 1999. View at Google Scholar · View at Scopus
  33. I. Gutsche, F. Coulibaly, J. E. Voss et al., “Secreted dengue virus nonstructural protein NS1 is an atypical barrel-shaped high-density lipoprotein,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 108, no. 19, pp. 8003–8008, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. B. M. Kümmerer and C. M. Rice, “Mutations in the yellow fever virus nonstructural protein NS2A selectively block production of infectious particles,” Journal of Virology, vol. 76, no. 10, pp. 4773–4784, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Y. Leung, G. P. Pijlman, N. Kondratieva, J. Hyde, J. M. Mackenzie, and A. A. Khromykh, “Role of nonstructural protein NS2A in flavivirus assembly,” Journal of Virology, vol. 82, no. 10, pp. 4731–4741, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. J. M. MacKenzie, A. A. Khromykh, M. K. Jones, and E. G. Westaway, “Subcellular localization and some biochemical properties of the flavivirus Kunjin nonstructural proteins NS2A and NS4A,” Virology, vol. 245, no. 2, pp. 203–215, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. S. L. Rossi, R. Fayzulin, N. Dewsbury, N. Bourne, and P. W. Mason, “Mutations in West Nile virus nonstructural proteins that facilitate replicon persistence in vitro attenuate virus replication in vitro and in vivo,” Virology, vol. 364, no. 1, pp. 184–195, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. S. Chang, C. L. Liao, C. H. Tsao et al., “Membrane permeabilization by small hydrophobic nonstructural proteins of Japanese encephalitis virus,” J. Virol, vol. 73, no. 8, pp. 6257–6264, 1999. View at Google Scholar
  39. K. L. McElroy, K. A. Tsetsarkin, D. L. Vanlandingham, and S. Higgs, “Manipulation of the yellow fever virus non-structural genes 2A and 4B and the 3non-coding region to evaluate genetic determinants of viral dissemination from the Aedes Aegypti midgut,” The American Journal of Tropical Medicine and Hygiene, vol. 75, no. 6, pp. 1158–1164, 2006. View at Google Scholar · View at Scopus
  40. X. Xie, S. Gayen, C. Kang, Z. Yuan, and P.-Y. Shi, “Membrane topology and function of dengue virus NS2A protein,” Journal of Virology, vol. 87, no. 8, pp. 4609–4622, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. W. J. Liu, X. J. Wang, D. C. Clark, M. Lobigs, R. A. Hall, and A. A. Khromykh, “A single amino acid substitution in the West Nile virus nonstructural protein NS2A disables its ability to inhibit alpha/beta interferon induction and attenuates virus virulence in mice,” Journal of Virology, vol. 80, no. 5, pp. 2396–2404, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. W. J. Liu, X. J. Wang, V. V. Mokhonov, P.-Y. Shi, R. Randall, and A. A. Khromykh, “Inhibition of interferon signaling by the New York 99 strain and Kunjin subtype of West Nile virus involves blockage of STAT1 and STAT2 activation by nonstructural proteins,” Journal of Virology, vol. 79, no. 3, pp. 1934–1942, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Falgout, M. Pethel, Y.-M. Zhang, and C.-J. Lai, “Both nonstructural proteins NS2B and NS3 are required for the proteolytic processing of dengue virus nonstructural proteins,” Journal of Virology, vol. 65, no. 5, pp. 2467–2475, 1991. View at Google Scholar · View at Scopus
  44. S. Aguirre, A. M. Maestre, S. Pagni et al., “DENV Inhibits Type I IFN Production in Infected Cells by Cleaving Human STING,” PLoS Pathogens, vol. 8, no. 10, Article ID e1002934, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Aguilera-Pesantes and M. A. Méndez, “Structure and sequence based functional annotation of Zika virus NS2b protein: Computational insights,” Biochemical and Biophysical Research Communications, 2016. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Zmurko, J. Neyts, and K. Dallmeier, “Flaviviral NS4b, chameleon and jack-in-the-box roles in viral replication and pathogenesis, and a molecular target for antiviral intervention,” Reviews in Medical Virology, vol. 25, no. 4, pp. 205–223, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Lu and P. Gong, “Crystal Structure of the Full-Length Japanese Encephalitis Virus NS5 Reveals a Conserved Methyltransferase-Polymerase Interface,” PLoS Pathogens, vol. 9, no. 8, Article ID e1003549, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. X.-D. Li, C. Shan, C.-L. Deng et al., “The Interface between Methyltransferase and Polymerase of NS5 Is Essential for Flavivirus Replication,” PLOS Neglected Tropical Diseases, vol. 8, no. 5, Article ID e2891, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. V. J. Klema, M. Ye, A. Hindupur et al., “Dengue Virus Nonstructural Protein 5 (NS5) Assembles into a Dimer with a Unique Methyltransferase and Polymerase Interface,” PLoS Pathogens, vol. 12, no. 2, Article ID e1005451, 2016. View at Publisher · View at Google Scholar · View at Scopus
  50. B. Zhao, G. Yi, F. Du et al., “Structure and function of the Zika virus full-length NS5 protein,” Nature Communications, vol. 8, Article ID 14762, 2017. View at Publisher · View at Google Scholar · View at Scopus
  51. D. C. Chang, L. T. Hoang, A. N. Mohamed Naim et al., “Evasion of early innate immune response by 2-O-methylation of dengue genomic RNA,” Virology, vol. 499, pp. 259–266, 2016. View at Publisher · View at Google Scholar · View at Scopus
  52. A. D. Davidson, “Chapter 2 New Insights into Flavivirus Nonstructural Protein 5,” Advances in Virus Research, vol. 74, pp. 41–101, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. X. Xu, K. Vaughan, D. Weiskopf et al., “Identifying candidate targets of immune responses in Zika Virus based on homology to Epitopes in other Flavivirus Species,” PLoS Currents, 2016. View at Publisher · View at Google Scholar
  54. Y. Shi and G. F. Gao, “Structural Biology of the Zika Virus,” Trends in Biochemical Sciences, vol. 42, no. 6, pp. 443–456, 2017. View at Publisher · View at Google Scholar · View at Scopus
  55. E. D. Coelho, J. P. Arrais, S. Matos et al., “Computational prediction of the human-microbial oral interactome,” BMC Systems Biology, vol. 8, no. 1, article no. 24, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Tang, C. Hammack, S. C. Ogden et al., “Zika virus infects human cortical neural progenitors and attenuates their growth,” Cell Stem Cell, vol. 18, no. 5, pp. 587–590, 2016. View at Publisher · View at Google Scholar · View at Scopus
  57. J. P. Arrais, N. Rosa, J. Melo et al., “OralCard: A bioinformatic tool for the study of oral proteome,” Archives of Oral Biolog, vol. 58, no. 7, pp. 762–772, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. N. Rosa, M. J. Correia, J. P. Arrais et al., “From the salivary proteome to the OralOme: Comprehensive molecular oral biology,” Archives of Oral Biolog, vol. 57, no. 7, pp. 853–864, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. P. Shannon, A. Markiel, O. Ozier et al., “Cytoscape: a software Environment for integrated models of biomolecular interaction networks,” Genome Research, vol. 13, no. 11, pp. 2498–2504, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Kanehisa, Y. Sato, M. Kawashima, M. Furumichi, and M. Tanabe, “KEGG as a reference resource for gene and protein annotation,” Nucleic Acids Research, vol. 44, no. 1, pp. D457–D462, 2016. View at Publisher · View at Google Scholar
  61. M. Kanehisa and S. Goto, “KEGG: kyoto encyclopedia of genes and genomes,” Nucleic Acids Research, vol. 28, no. 1, pp. 27–30, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Amara and J. Mercer, “Viral apoptotic mimicry,” Nature Reviews Microbiology, vol. 13, no. 8, pp. 461–469, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. T. Guirimand, S. Delmotte, and V. Navratil, “VirHostNet 2.0: Surfing on the web of virus/host molecular interactions data,” Nucleic Acids Research, vol. 43, no. 1, pp. D583–D587, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. C. Hulo, E. De Castro, P. Masson et al., “ViralZone: A knowledge resource to understand virus diversity,” Nucleic Acids Research, vol. 39, no. 1, pp. D576–D582, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. UniProt Consortium, “Uniprot: the universal protein knowledgebase,” Nucleic Acids Research, vol. 45, no. D1, pp. D158–D169, 2017. View at Publisher · View at Google Scholar
  66. F. Sievers, A. Wilm, D. Dineen et al., “Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega,” Molecular Systems Biology, vol. 7, article 539, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. K. Yoon, G. Song, X. Qian et al., “Zika-Virus-Encoded NS2A Disrupts Mammalian Cortical Neurogenesis by Degrading Adherens Junction Proteins,” Cell Stem Cell, vol. 21, no. 3, pp. 349–358.e6, 2017. View at Publisher · View at Google Scholar
  68. D. Szklarczyk, A. Franceschini, S. Wyder et al., “STRING v10: protein-protein interaction networks, integrated over the tree of life,” Nucleic Acids Research, vol. 43, pp. D447–D452, 2015. View at Publisher · View at Google Scholar
  69. S. Bhattacharyya, A. Zagórska, E. D. Lew et al., “Enveloped viruses disable innate immune responses in dendritic cells by direct activation of TAM receptors,” Cell Host & Microbe, vol. 14, no. 2, pp. 136–147, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. A. L. C. Valadão, R. S. Aguiar, and L. B. de Arruda, “Interplay between inflammation and cellular stress triggered by Flaviviridae viruses,” Frontiers in Microbiology, vol. 7, article no. 1233, 2016. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Bayer, N. J. Lennemann, Y. Ouyang et al., “Type III Interferons Produced by Human Placental Trophoblasts Confer Protection against Zika Virus Infection,” Cell Host & Microbe, vol. 19, no. 5, pp. 705–712, 2016. View at Publisher · View at Google Scholar · View at Scopus
  72. L. de Noronha, C. Zanluca, M. L. V. Azevedo, K. G. Luz, and C. N. D. dos Santos, “Zika virus damages the human placental barrier and presents marked fetal neurotropism,” Memórias do Instituto Oswaldo Cruz, vol. 111, no. 5, pp. 287–293, 2016. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Tabata, M. Petitt, H. Puerta-Guardo et al., “Zika Virus Targets Different Primary Human Placental Cells, Suggesting Two Routes for Vertical Transmission,” Cell Host & Microbe, vol. 20, no. 2, pp. 155–166, 2016. View at Publisher · View at Google Scholar · View at Scopus
  74. J. J. Miner and M. S. Diamond, “Understanding how zika virus enters and infects neural target cells,” Cell Stem Cell, vol. 18, no. 5, pp. 559-560, 2016. View at Publisher · View at Google Scholar · View at Scopus
  75. G. Savidis, W. M. McDougall, P. Meraner et al., “Identification of Zika Virus and Dengue Virus Dependency Factors using Functional Genomics,” Cell Reports, vol. 16, no. 1, pp. 232–246, 2016. View at Publisher · View at Google Scholar · View at Scopus
  76. T. J. Nowakowski, A. A. Pollen, E. Di Lullo, C. Sandoval-Espinosa, M. Bershteyn, and A. R. Kriegstein, “Expression analysis highlights AXL as a candidate zika virus entry receptor in neural stem cells,” Cell Stem Cell, vol. 18, no. 5, pp. 591–596, 2016. View at Publisher · View at Google Scholar
  77. O. L. Gervásio, W. D. Phillips, L. Cole, and D. G. Allen, “Caveolae respond to cell stretch and contribute to stretch-induced signaling,” Journal of Cell Science, vol. 124, no. 21, pp. 3581–3590, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. G. Fibriansah, K. D. Ibarra, T.-S. Ng et al., “Cryo-EM structure of an antibody that neutralizes dengue virus type 2 by locking E protein dimers,” Science, vol. 349, no. 6243, pp. 88–91, 2015. View at Publisher · View at Google Scholar · View at Scopus
  79. M. V. Cherrier, B. Kaufmann, G. E. Nybakken et al., “Structural basis for the preferential recognition of immature flaviviruses by a fusion-loop antibody,” EMBO Journal, vol. 28, no. 20, pp. 3269–3276, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. A. S. Richard, B.-S. Shim, Y.-C. Kwon et al., “AXL-dependent infection of human fetal endothelial cells distinguishes Zika virus from other pathogenic flaviviruses,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 114, no. 8, pp. 2024–2029, 2017. View at Publisher · View at Google Scholar · View at Scopus
  81. W. Dejnirattisai, A. I. Webb, V. Chan et al., “Lectin switching during dengue virus infection,” The Journal of Infectious Diseases, vol. 203, no. 12, pp. 1775–1783, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. W. M. Schneider, M. D. Chevillotte, and C. M. Rice, “Interferon-stimulated genes: a complex web of host defenses,” Annual Review of Immunology, vol. 32, pp. 513–545, 2014. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Thiemmeca, C. Tamdet, N. Punyadee et al., “Secreted NS1 protects dengue virus from mannose-binding lectin-mediated neutralization,” The Journal of Immunology, vol. 197, no. 10, pp. 4053–4065, 2016. View at Publisher · View at Google Scholar · View at Scopus
  84. M. S. Suthar, S. Aguirre, and A. Fernandez-Sesma, “Innate Immune Sensing of Flaviviruses,” PLoS Pathogens, vol. 9, no. 9, Article ID e1003541, 2013. View at Publisher · View at Google Scholar · View at Scopus
  85. T. Matsumiya and D. M. Stafforini, “Function and Regulation of Retinoic Acid-Inducible Gene-I,” Critical Reviews™ in Immunology, vol. 30, no. 6, pp. 489–513, 2010. View at Publisher · View at Google Scholar
  86. H. Kato, O. Takeuchi, S. Sato et al., “Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses,” Nature, vol. 441, no. 7089, pp. 101–105, 2006. View at Publisher · View at Google Scholar
  87. M. U. Gack, “Mechanisms of RIG-I-Like receptor activation and manipulation by viral pathogens,” Journal of Virology, vol. 88, no. 10, pp. 5213–5216, 2014. View at Publisher · View at Google Scholar · View at Scopus
  88. A. M. A. Nasirudeen, H. H. Wong, P. Thien, S. Xu, K.-P. Lam, and D. X. Liu, “RIG-I, MDA5 and TLR3 synergistically play an important role in restriction of dengue virus infection,” PLOS Neglected Tropical Diseases, vol. 5, no. 1, article e926, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. K. M. Quicke, J. R. Bowen, E. L. Johnson et al., “Zika Virus Infects Human Placental Macrophages,” Cell Host & Microbe, vol. 20, no. 1, pp. 83–90, 2016. View at Publisher · View at Google Scholar · View at Scopus
  90. S. M. Best, “The many faces of the flavivirus NS5 protein in antagonism of type I interferon signaling,” Journal of Virology, vol. 91, no. 3, Article ID e01970-16, 2017. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Ashour, M. Laurent-Rolle, P.-Y. Shi, and A. García-Sastre, “NS5 of dengue virus mediates STAT2 binding and degradation,” Journal of Virology, vol. 83, no. 11, pp. 5408–5418, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Grant, S. S. Ponia, S. Tripathi et al., “Zika Virus Targets Human STAT2 to Inhibit Type i Interferon Signaling,” Cell Host & Microbe, vol. 19, no. 6, pp. 882–890, 2016. View at Publisher · View at Google Scholar · View at Scopus
  93. H. A. Dar, T. Zaheer, R. Z. Paracha, and A. Ali, “Structural analysis and insight into Zika virus NS5 mediated interferon inhibition,” Infection, Genetics and Evolution, vol. 51, pp. 143–152, 2017. View at Publisher · View at Google Scholar · View at Scopus
  94. G. A. Versteeg, R. Rajsbaum, M. T. Sánchez-Aparicio et al., “The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern-recognition receptors,” Immunity, vol. 38, no. 2, pp. 384–398, 2013. View at Publisher · View at Google Scholar · View at Scopus