Dengue viruses cleave STING in humans but not in nonhuman primates, their presumed natural reservoir

eLife

Volumn 7, Issue , 2018, Pages

  Stabell, Alex C ^a   Meyerson, Nicholas R ^a   Gullberg, Rebekah C ^b   Gilchrist, Alison R ^a   Webb, Kristofor J ^a   Old, William M ^a   Perera, Rushika ^b   Sawyer, Sara L ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; MEMBRANE PROTEIN; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 3; PROTEINASE; STING PROTEIN; UNCLASSIFIED DRUG; MPYS PROTEIN, HUMAN; PEPTIDE HYDROLASE; VIRAL PROTEIN;

ANIMAL CELL; ANTIBODY DETECTION; ARTICLE; CONTROLLED STUDY; CRISPR-CAS9 SYSTEM; DENGUE VIRUS 2; ESCHERICHIA COLI; GENE MUTATION; GENE SEQUENCE; GENETIC TRANSFECTION; HAPLORHINI; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INFECTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLAQUE ASSAY; PLASMID; PROTEIN CLEAVAGE; RNA EXTRACTION; SANGER SEQUENCING; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING; A-549 CELL LINE; AMINO ACID SEQUENCE; ANIMAL; CLASSIFICATION; DENGUE; DENGUE VIRUS; ENZYMOLOGY; GENETICS; HOST RANGE; METABOLISM; PHYSIOLOGY; PRIMATE; SEQUENCE HOMOLOGY; VIROLOGY;

A549 CELLS; AMINO ACID SEQUENCE; ANIMALS; DENGUE; DENGUE VIRUS; HOST SPECIFICITY; HUMANS; MEMBRANE PROTEINS; MICE; PEPTIDE HYDROLASES; PRIMATES; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

EID: 85045690360     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.31919     Document Type: Article

References (102)

1. Aguirre S, Fernandez-Sesma A. 2017. Collateral Damage during Dengue Virus Infection: Making Sense of DNA by cGAS. Journal of Virology 91:e01081-16. DOI: https://doi.org/10.1128/JVI.01081-16, PMID: 28446670
2. Aguirre S, Luthra P, Sanchez-Aparicio MT, Maestre AM, Patel J, Lamothe F, Fredericks AC, Tripathi S, Zhu T, Pintado-Silva J, Webb LG, Bernal-Rubio D, Solovyov A, Greenbaum B, Simon V, Basler CF, Mulder LC, García-Sastre A, Fernandez-Sesma A. 2017. Dengue virus NS2B protein targets cGAS for degradation and prevents mitochondrial DNA sensing during infection. Nature Microbiology 2:17037. DOI: https://doi.org/10.1038/nmicrobiol.2017.37, PMID: 28346446
3. Aguirre S, Maestre AM, Pagni S, Patel JR, Savage T, Gutman D, Maringer K, Bernal-Rubio D, Shabman RS, Simon V, Rodriguez-Madoz JR, Mulder LC, Barber GN, Fernandez-Sesma A. 2012. DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathogens 8:e1002934. DOI: https://doi.org/10. 1371/journal.ppat.1002934, PMID: 23055924
4. Althouse BM, Durbin AP, Hanley KA, Halstead SB, Weaver SC, Cummings DA. 2014. Viral kinetics of primary dengue virus infection in non-human primates: a systematic review and individual pooled analysis. Virology 452-453:237–246. DOI: https://doi.org/10.1016/j.virol.2014.01.015, PMID: 24606701
5. Ashour J, Laurent-Rolle M, Shi PY, García-Sastre A. 2009. NS5 of dengue virus mediates STAT2 binding and degradation. Journal of Virology 83:5408–5418. DOI: https://doi.org/10.1128/JVI.02188-08, PMID: 19279106
6. Ashour J, Morrison J, Laurent-Rolle M, Belicha-Villanueva A, Plumlee CR, Bernal-Rubio D, Williams KL, Harris E, Fernandez-Sesma A, Schindler C, García-Sastre A. 2010. Mouse STAT2 restricts early dengue virus replication. Cell Host & Microbe 8:410–421. DOI: https://doi.org/10.1016/j.chom.2010.10.007, PMID: 21075352
7. Bera AK, Kuhn RJ, Smith JL. 2007. Functional characterization of cis and trans activity of the Flavivirus NS2B-NS3 protease. Journal of Biological Chemistry 282:12883–12892. DOI: https://doi.org/10.1074/jbc.M611318200, PMID: 17337448
8. Best SM. 2016. Flaviviruses. Current Biology 26:R1258–R1260. DOI: https://doi.org/10.1016/j.cub.2016.09.029, PMID: 27997831
9. Best SM. 2017. The Many Faces of the Flavivirus NS5 Protein in Antagonism of Type I Interferon Signaling. Journal of Virology 91:e01970-16. DOI: https://doi.org/10.1128/JVI.01970-16, PMID: 27881649
10. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI. 2013. The global distribution and burden of dengue. Nature 496:504–507. DOI: https://doi.org/10.1038/nature12060, PMID: 23563266
11. Burdette DL, Vance RE. 2013. STING and the innate immune response to nucleic acids in the cytosol. Nature Immunology 14:19–26. DOI: https://doi.org/10.1038/ni.2491, PMID: 23238760
12. Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS, Westaway EG, Brandt WE. 1989. Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. Journal of General Virology 70:37–43. DOI: https://doi.org/10.1099/0022-1317-70-1-37, PMID: 2543738
13. Campbell M, Oakeson KF, Yandell M, Halpert JR, Dearing D. 2016. The draft genome sequence and annotation of the desert woodrat Neotoma lepida. Genomics Data 9:58–59. DOI: https://doi.org/10.1016/j.gdata.2016.06. 008, PMID: 27408812
14. Cardosa J, Ooi MH, Tio PH, Perera D, Holmes EC, Bibi K, Abdul Manap Z. 2009. Dengue virus serotype 2 from a sylvatic lineage isolated from a patient with dengue hemorrhagic fever. PLoS Neglected Tropical Diseases 3: e423. DOI: https://doi.org/10.1371/journal.pntd.0000423, PMID: 19399166
15. Cassetti MC, Durbin A, Harris E, Rico-Hesse R, Roehrig J, Rothman A, Whitehead S, Natarajan R, Laughlin C. 2010. Report of an NIAID workshop on dengue animal models. Vaccine 28:4229–4234. DOI: https://doi.org/10. 1016/j.vaccine.2010.04.045, PMID: 20434551
16. Chambers TJ, McCourt DW, Rice CM. 1990. Production of yellow fever virus proteins in infected cells: identification of discrete polyprotein species and analysis of cleavage kinetics using region-specific polyclonal antisera. Virology 177:159–174. DOI: https://doi.org/10.1016/0042-6822(90)90470-C, PMID: 2353452
17. Demogines A, Abraham J, Choe H, Farzan M, Sawyer SL. 2013. Dual host-virus arms races shape an essential housekeeping protein. PLoS Biology 11:e1001571. DOI: https://doi.org/10.1371/journal.pbio.1001571, PMID: 23723737
18. Demogines A, Farzan M, Sawyer SL. 2012. Evidence for ACE2-utilizing coronaviruses (CoVs) related to severe acute respiratory syndrome CoV in bats. Journal of Virology 86:6350–6353. DOI: https://doi.org/10.1128/JVI. 00311-12, PMID: 22438550
19. Desmyter J, Melnick JL, Rawls WE. 1968. Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). Journal of Virology 2:955–961. PMID: 4302013
20. Diallo M, Ba Y, Sall AA, Diop OM, Ndione JA, Mondo M, Girault L, Mathiot C. 2003. Amplification of the sylvatic cycle of dengue virus type 2, Senegal, 1999-2000: entomologic findings and epidemiologic considerations. Emerging Infectious Diseases 9:362–367. DOI: https://doi.org/10.3201/eid0903.020219, PMID: 12643833
21. Diamond MS, Pierson TC. 2015. Molecular Insight into Dengue Virus Pathogenesis and Its Implications for Disease Control. Cell 162:488–492. DOI: https://doi.org/10.1016/j.cell.2015.07.005, PMID: 26232221
22. Ding Q, Cao X, Lu J, Huang B, Liu YJ, Kato N, Shu HB, Zhong J. 2013. Hepatitis C virus NS4B blocks the interaction of STING and TBK1 to evade host innate immunity. Journal of Hepatology 59:52–58. DOI: https://doi.org/10.1016/j.jhep.2013.03.019, PMID: 23542348
23. Elde NC, Child SJ, Geballe AP, Malik HS. 2009. Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457:485–489. DOI: https://doi.org/10.1038/nature07529, PMID: 19043403
24. Falgout B, Pethel M, Zhang YM, Lai CJ. 1991. Both nonstructural proteins NS2B and NS3 are required for the proteolytic processing of dengue virus nonstructural proteins. Journal of Virology 65:2467–2475. PMID: 201676 8
25. Ferreira MS, de Castro PH, Silva GA, Casseb SM, Dias Júnior AG, Rodrigues SG, Azevedo RS, Costa e Silva MF, Zauli DA, Araújo MS, Béla SR, Teixeira-Carvalho A, Martins-Filho OA, Vasconcelos PF. 2014. Callithrix penicillata: a feasible experimental model for dengue virus infection. Immunology Letters 158:126–133. DOI: https://doi.org/10.1016/j.imlet.2013.12.008, PMID: 24361035
26. Franco L, Palacios G, Martinez JA, Vázquez A, Savji N, De Ory F, Sanchez-Seco MP, Martín D, Lipkin WI, Tenorio A. 2011. First report of sylvatic DENV-2-associated dengue hemorrhagic fever in West Africa. PLoS Neglected Tropical Diseases 5:e1251. DOI: https://doi.org/10.1371/journal.pntd.0001251, PMID: 21829739
27. Freifeld CC, Mandl KD, Reis BY, Brownstein JS. 2008. HealthMap: global infectious disease monitoring through automated classification and visualization of Internet media reports. Journal of the American Medical Informatics Association 15:150–157. DOI: https://doi.org/10.1197/jamia.M2544, PMID: 18096908
28. Geissmann T. 2007. Status reassessment of the gibbons: Results of the Asian primate red list workshop 2006. Gibbon Journal 3:5–77.
29. Green AM, Beatty PR, Hadjilaou A, Harris E. 2014. Innate immunity to dengue virus infection and subversion of antiviral responses. Journal of Molecular Biology 426:1148–1160. DOI: https://doi.org/10.1016/j.jmb.2013.11. 023, PMID: 24316047
30. Halstead SB, Shotwell H, Casals J. 1973. Studies on the pathogenesis of dengue infection in monkeys. I. Clinical laboratory responses to primary infection. Journal of Infectious Diseases 128:7–14. DOI: https://doi.org/10. 1093/infdis/128.1.7, PMID: 4198027
31. Hanley KA, Monath TP, Weaver SC, Rossi SL, Richman RL, Vasilakis N. 2013. Fever versus fever: the role of host and vector susceptibility and interspecific competition in shaping the current and future distributions of the sylvatic cycles of dengue virus and yellow fever virus. Infection, Genetics and Evolution 19:292–311. DOI: https://doi.org/10.1016/j.meegid.2013.03.008, PMID: 23523817
32. Heaton NS, Perera R, Berger KL, Khadka S, Lacount DJ, Kuhn RJ, Randall G. 2010. Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis. PNAS 107:17345–17350. DOI: https://doi.org/10.1073/pnas.1010811107, PMID: 20855599
33. Hickey AC, Koster JA, Thalmann CM, Hardcastle K, Tio PH, Cardosa MJ, Bossart KN. 2013. Serotype-specific host responses in rhesus macaques after primary dengue challenge. The American Journal of Tropical Medicine and Hygiene 89:1043–1057. DOI: https://doi.org/10.4269/ajtmh.13-0145, PMID: 24062475
34. Holm CK, Rahbek SH, Gad HH, Bak RO, Jakobsen MR, Jiang Z, Hansen AL, Jensen SK, Sun C, Thomsen MK, Laustsen A, Nielsen CG, Severinsen K, Xiong Y, Burdette DL, Hornung V, Lebbink RJ, Duch M, Fitzgerald KA, Bahrami S, et al. 2016. Influenza A virus targets a cGAS-independent STING pathway that controls enveloped RNA viruses. Nature Communications 7:10680. DOI: https://doi.org/10.1038/ncomms10680, PMID: 26893169
35. Hueffer K, Parker JS, Weichert WS, Geisel RE, Sgro JY, Parrish CR. 2003. The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. Journal of Virology 77:1718–1726. DOI: https://doi.org/10.1128/JVI.77.3.1718-1726.2003, PMID: 12525605
36. Ishikawa H, Barber GN. 2008. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455:674–678. DOI: https://doi.org/10.1038/nature07317, PMID: 18724357
37. Ishikawa H, Ma Z, Barber GN. 2009. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461:788–792. DOI: https://doi.org/10.1038/nature08476, PMID: 19776740
38. Jin L, Waterman PM, Jonscher KR, Short CM, Reisdorph NA, Cambier JC. 2008. MPYS, a novel membrane tetraspanner, is associated with major histocompatibility complex class II and mediates transduction of apoptotic signals. Molecular and Cellular Biology 28:5014–5026. DOI: https://doi.org/10.1128/MCB.00640-08, PMID: 18559423
39. Jones M, Davidson A, Hibbert L, Gruenwald P, Schlaak J, Ball S, Foster GR, Jacobs M. 2005. Dengue virus inhibits alpha interferon signaling by reducing STAT2 expression. Journal of Virology 79:5414–5420. DOI: https://doi.org/10.1128/JVI.79.9.5414-5420.2005, PMID: 15827155
40. Keane M, Craig T, Alföldi J, Berlin AM, Johnson J, Seluanov A, Gorbunova V, Di Palma F, Lindblad-Toh K, Church GM, de Magalhães JP. 2014. The Naked Mole Rat Genome Resource: facilitating analyses of cancer and longevity-related adaptations. Bioinformatics 30:3558–3560. DOI: https://doi.org/10.1093/bioinformatics/btu579, PMID: 25172923
41. Kerr SA, Jackson EL, Lungu OI, Meyer AG, Demogines A, Ellington AD, Georgiou G, Wilke CO, Sawyer SL. 2015. Computational and Functional Analysis of the Virus-Receptor Interface Reveals Host Range Trade-Offs in New World Arenaviruses. Journal of Virology 89:11643–11653. DOI: https://doi.org/10.1128/JVI.01408-15, PMID: 26355089
42. Li J, Lim SP, Beer D, Patel V, Wen D, Tumanut C, Tully DC, Williams JA, Jiricek J, Priestle JP, Harris JL, Vasudevan SG. 2005a. Functional profiling of recombinant NS3 proteases from all four serotypes of dengue virus using tetrapeptide and octapeptide substrate libraries. Journal of Biological Chemistry 280:28766–28774. DOI: https://doi.org/10.1074/jbc.M500588200, PMID: 15932883
43. Li XD, Sun L, Seth RB, Pineda G, Chen ZJ. 2005b. Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. PNAS 102:17717–17722. DOI: https://doi.org/10.1073/pnas.0508531102, PMID: 16301520
44. Lou DI, Kim ET, Meyerson NR, Pancholi NJ, Mohni KN, Enard D, Petrov DA, Weller SK, Weitzman MD, Sawyer SL. 2016. An Intrinsically Disordered Region of the DNA Repair Protein Nbs1 Is a Species-Specific Barrier to Herpes Simplex Virus 1 in Primates. Cell Host & Microbe 20:178–188. DOI: https://doi.org/10.1016/j.chom. 2016.07.003, PMID: 27512903
45. Mansfield KL, Horton DL, Johnson N, Li L, Barrett AD, Smith DJ, Galbraith SE, Solomon T, Fooks AR. 2011. Flavivirus-induced antibody cross-reactivity. Journal of General Virology 92:2821–2829. DOI: https://doi.org/10. 1099/vir.0.031641-0, PMID: 21900425
46. Martin C, Buckler-White A, Wollenberg K, Kozak CA. 2013. The avian XPR1 gammaretrovirus receptor is under positive selection and is disabled in bird species in contact with virus-infected wild mice. Journal of Virology 87: 10094–10104. DOI: https://doi.org/10.1128/JVI.01327-13, PMID: 23843647
47. Mayer SV, Tesh RB, Vasilakis N. 2017. The emergence of arthropod-borne viral diseases: A global prospective on dengue, chikungunya and zika fevers. Acta Tropica 166:155–163. DOI: https://doi.org/10.1016/j.actatropica. 2016.11.020, PMID: 27876643
48. Mazzon M, Jones M, Davidson A, Chain B, Jacobs M. 2009. Dengue virus NS5 inhibits interferon-alpha signaling by blocking signal transducer and activator of transcription 2 phosphorylation. The Journal of Infectious Diseases 200:1261–1270. DOI: https://doi.org/10.1086/605847, PMID: 19754307
49. Messina JP, Brady OJ, Pigott DM, Brownstein JS, Hoen AG, Hay SI. 2014. A global compendium of human dengue virus occurrence. Scientific Data 1:140004. DOI: https://doi.org/10.1038/sdata.2014.4, PMID: 25977762
50. Meyerson NR, Sharma A, Wilkerson GK, Overbaugh J, Sawyer SL. 2015. Identification of Owl Monkey CD4 Receptors Broadly Compatible with Early-Stage HIV-1 Isolates. Journal of Virology 89:8611–8622. DOI: https://doi.org/10.1128/JVI.00890-15, PMID: 26063421
51. Meyerson NR, Zhou L, Guo YR, Zhao C, Tao YJ, Krug RM, Sawyer SL. 2017. Nuclear TRIM25 Specifically Targets Influenza Virus Ribonucleoproteins to Block the Onset of RNA Chain Elongation. Cell Host & Microbe 22:627– 638. DOI: https://doi.org/10.1016/j.chom.2017.10.003
52. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167–1172. DOI: https://doi.org/10.1038/nature04193, PMID: 16177806
53. Miller EH, Obernosterer G, Raaben M, Herbert AS, Deffieu MS, Krishnan A, Ndungo E, Sandesara RG, Carette JE, Kuehne AI, Ruthel G, Pfeffer SR, Dye JM, Whelan SP, Brummelkamp TR, Chandran K. 2012. Ebola virus entry requires the host-programmed recognition of an intracellular receptor. The EMBO Journal 31:1947–1960. DOI: https://doi.org/10.1038/emboj.2012.53, PMID: 22395071
54. Moi ML, Omatsu T, Hirayama T, Nakamura S, Katakai Y, Yoshida T, Saito A, Tajima S, Ito M, Takasaki T, Akari H, Kurane I. 2013. Presence of Viral Genome in Urine and Development of Hematuria and Pathological Changes in Kidneys in Common Marmoset (Callithrix jacchus) after Inoculation with Dengue Virus. Pathogens 2:357–363. DOI: https://doi.org/10.3390/pathogens2020357, PMID: 25437039
55. Morrison J, Aguirre S, Fernandez-Sesma A. 2012. Innate immunity evasion by Dengue virus. Viruses 4:397–413. DOI: https://doi.org/10.3390/v4030397, PMID: 22590678
56. Mozzi A, Pontremoli C, Forni D, Clerici M, Pozzoli U, Bresolin N, Cagliani R, Sironi M. 2015. OASes and STING: adaptive evolution in concert. Genome Biology and Evolution 7:1016–1032. DOI: https://doi.org/10.1093/gbe/evv046, PMID: 25752600
57. Nathaniel TI, Otukonyong EE, Okon M, Chaves J, Cochran T, Nathaniel AI. 2013. Metabolic regulatory clues from the naked mole rat: toward brain regulatory functions during stroke. Brain Research Bulletin 98:44–52. DOI: https://doi.org/10.1016/j.brainresbull.2013.07.008, PMID: 23886571
58. Ng M, Ndungo E, Kaczmarek ME, Herbert AS, Binger T, Kuehne AI, Jangra RK, Hawkins JA, Gifford RJ, Biswas R, Demogines A, James RM, Yu M, Brummelkamp TR, Drosten C, Wang LF, Kuhn JH, Müller MA, Dye JM, Sawyer SL, et al. 2015. Filovirus receptor NPC1 contributes to species-specific patterns of ebolavirus susceptibility in bats. eLife 4:e11785. DOI: https://doi.org/10.7554/eLife.11785, PMID: 26698106
59. Nitta S, Sakamoto N, Nakagawa M, Kakinuma S, Mishima K, Kusano-Kitazume A, Kiyohashi K, Murakawa M, Nishimura-Sakurai Y, Azuma S, Tasaka-Fujita M, Asahina Y, Yoneyama M, Fujita T, Watanabe M. 2013. Hepatitis C virus NS4B protein targets STING and abrogates RIG-I-mediated type I interferon-dependent innate immunity. Hepatology 57:46–58. DOI: https://doi.org/10.1002/hep.26017, PMID: 22911572
60. Osada N, Kohara A, Yamaji T, Hirayama N, Kasai F, Sekizuka T, Kuroda M, Hanada K. 2014. The genome landscape of the african green monkey kidney-derived vero cell line. DNA Research 21:673–683. DOI: https://doi.org/10.1093/dnares/dsu029, PMID: 25267831
61. Patel MR, Loo YM, Horner SM, Gale M, Malik HS. 2012. Convergent evolution of escape from hepaciviral antagonism in primates. PLoS Biology 10:e1001282. DOI: https://doi.org/10.1371/journal.pbio.1001282, PMID: 22427742
62. Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE, Moreira MA, Kessing B, Pontius J, Roelke M, Rumpler Y, Schneider MP, Silva A, O’Brien SJ, Pecon-Slattery J. 2011. A molecular phylogeny of living primates. PLoS Genetics 7:e1001342. DOI: https://doi.org/10.1371/journal.pgen.1001342, PMID: 21436896
63. Perera R, Kuhn RJ. 2008. Structural proteomics of dengue virus. Current Opinion in Microbiology 11:369–377. DOI: https://doi.org/10.1016/j.mib.2008.06.004, PMID: 18644250
64. Perry ST, Buck MD, Lada SM, Schindler C, Shresta S. 2011. STAT2 mediates innate immunity to Dengue virus in the absence of STAT1 via the type I interferon receptor. PLoS Pathogens 7:e1001297. DOI: https://doi.org/10. 1371/journal.ppat.1001297, PMID: 21379341
65. Preugschat F, Yao CW, Strauss JH. 1990. In vitro processing of dengue virus type 2 nonstructural proteins NS2A, NS2B, and NS3. Journal of Virology 64:4364–4374. PMID: 2143543
66. Pyke AT, Moore PR, Taylor CT, Hall-Mendelin S, Cameron JN, Hewitson GR, Pukallus DS, Huang B, Warrilow D, van den Hurk AF. 2016. Highly divergent dengue virus type 1 genotype sets a new distance record. Scientific Reports 6:22356. DOI: https://doi.org/10.1038/srep22356, PMID: 26924208
67. Radoshitzky SR, Kuhn JH, Spiropoulou CF, Albariño CG, Nguyen DP, Salazar-Bravo J, Dorfman T, Lee AS, Wang E, Ross SR, Choe H, Farzan M. 2008. Receptor determinants of zoonotic transmission of New World hemorrhagic fever arenaviruses. PNAS 105:2664–2669. DOI: https://doi.org/10.1073/pnas.0709254105, PMID: 18268337
68. Microbiology and Infectious Disease
69. Rico-Hesse R. 1990. Molecular evolution and distribution of dengue viruses type 1 and 2 in nature. Virology 174: 479–493. DOI: https://doi.org/10.1016/0042-6822(90)90102-W, PMID: 2129562
70. Rodhain F. 1991. The role of monkeys in the biology of dengue and yellow fever. Comparative Immunology, Microbiology and Infectious Diseases 14:9–19. DOI: https://doi.org/10.1016/0147-9571(91)90036-D, PMID: 1 905605
71. Rodriguez-Madoz JR, Belicha-Villanueva A, Bernal-Rubio D, Ashour J, Ayllon J, Fernandez-Sesma A. 2010. Inhibition of the type I interferon response in human dendritic cells by dengue virus infection requires a catalytically active NS2B3 complex. Journal of Virology 84:9760–9774. DOI: https://doi.org/10.1128/JVI.01051-10, PMID: 20660196
72. Rossi SL, Nasar F, Cardosa J, Mayer SV, Tesh RB, Hanley KA, Weaver SC, Vasilakis N. 2012. Genetic and phenotypic characterization of sylvatic dengue virus type 4 strains. Virology 423:58–67. DOI: https://doi.org/10. 1016/j.virol.2011.11.018, PMID: 22178263
73. Rowley PA, Ho B, Bushong S, Johnson A, Sawyer SL. 2016. XRN1 Is a Species-Specific Virus Restriction Factor in Yeasts. PLOS Pathogens 12:e1005890. DOI: https://doi.org/10.1371/journal.ppat.1005890, PMID: 27711183
74. Rudnick A. 1965. Studies of the ecology of dengue in Malaysia: a preliminary report. Journal of Medical Entomology 2:203–208. DOI: https://doi.org/10.1093/jmedent/2.2.203, PMID: 5827577
75. Rudnick A. 1986. Dengue VIrus Ecology in Malasia. Inst Med Res Malays Bull 23:51–152.
76. Sawyer SL, Elde NC. 2012. A cross-species view on viruses. Current Opinion in Virology 2:561–568. DOI: https://doi.org/10.1016/j.coviro.2012.07.003, PMID: 22835485
77. Scherer WF, Russell PK, Rosen L, Casals J, Dickerman RW. 1978. Experimental infection of chimpanzees with dengue viruses. The American Journal of Tropical Medicine and Hygiene 27:590–599. DOI: https://doi.org/10. 4269/ajtmh.1978.27.590, PMID: 677372
78. Scherwitzl I, Mongkolsapaja J, Screaton G. 2017. Recent advances in human flavivirus vaccines. Current Opinion in Virology 23:95–101. DOI: https://doi.org/10.1016/j.coviro.2017.04.002, PMID: 28486135
79. Shimoyama M, Smith JR, De Pons J, Tutaj M, Khampang P, Hong W, Erbe CB, Ehrlich GD, Bakaletz LO, Kerschner JE. 2016. The Chinchilla Research Resource Database: resource for an otolaryngology disease model. Database 2016:baw073. DOI: https://doi.org/10.1093/database/baw073, PMID: 27173523
80. Shresta S, Kyle JL, Snider HM, Basavapatna M, Beatty PR, Harris E. 2004. Interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas T- and B-cell-dependent immunity are less critical. Journal of Virology 78:2701–2710. DOI: https://doi.org/10.1128/JVI.78.6.2701-2710.2004, PMID: 14990690
81. Skopec MM, Malenke JR, Halpert JR, Denise Dearing M. 2013. An in vivo assay for elucidating the importance of cytochromes P450 for the ability of a wild mammalian herbivore (Neotoma lepida) to consume toxic plants. Physiological and Biochemical Zoology 86:593–601. DOI: https://doi.org/10.1086/672212, PMID: 23995490
82. Stabell AC, Hawkins J, Li M, Gao X, David M, Press WH, Sawyer SL. 2016. Non-human Primate Schlafen11 Inhibits Production of Both Host and Viral Proteins. PLOS Pathogens 12:e1006066. DOI: https://doi.org/10. 1371/journal.ppat.1006066, PMID: 28027315
83. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. 2004. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427:848–853. DOI: https://doi.org/10. 1038/nature02343, PMID: 14985764
84. Sun L, Xing Y, Chen X, Zheng Y, Yang Y, Nichols DB, Clementz MA, Banach BS, Li K, Baker SC, Chen Z. 2012. Coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of STING-mediated signaling. PLoS One 7:e30802. DOI: https://doi.org/10.1371/journal.pone.0030802, PMID: 22312431
85. Sun W, Li Y, Chen L, Chen H, You F, Zhou X, Zhou Y, Zhai Z, Chen D, Jiang Z. 2009. ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. PNAS 106:8653–8658. DOI: https://doi.org/10.1073/pnas.0900850106, PMID: 19433799
86. Tesh RB, Travassos da Rosa AP, Guzman H, Araujo TP, Xiao SY. 2002. Immunization with heterologous flaviviruses protective against fatal West Nile encephalitis. Emerging Infectious Diseases 8:245–251. DOI: https://doi.org/10.3201/eid0803.010238, PMID: 11927020
87. Vasilakis N, Cardosa J, Hanley KA, Holmes EC, Weaver SC. 2011. Fever from the forest: prospects for the continued emergence of sylvatic dengue virus and its impact on public health. Nature Reviews Microbiology 9: 532–541. DOI: https://doi.org/10.1038/nrmicro2595, PMID: 21666708
88. Vasilakis N, Deardorff ER, Kenney JL, Rossi SL, Hanley KA, Weaver SC. 2009. Mosquitoes put the brake on arbovirus evolution: experimental evolution reveals slower mutation accumulation in mosquito than vertebrate cells. PLoS Pathogens 5:e1000467. DOI: https://doi.org/10.1371/journal.ppat.1000467, PMID: 19503824
89. Vasilakis N, Fokam EB, Hanson CT, Weinberg E, Sall AA, Whitehead SS, Hanley KA, Weaver SC. 2008. Genetic and phenotypic characterization of sylvatic dengue virus type 2 strains. Virology 377:296–307. DOI: https://doi. org/10.1016/j.virol.2008.04.044, PMID: 18570968
90. Vasilakis N, Shell EJ, Fokam EB, Mason PW, Hanley KA, Estes DM, Weaver SC. 2007. Potential of ancestral sylvatic dengue-2 viruses to re-emerge. Virology 358:402–412. DOI: https://doi.org/10.1016/j.virol.2006.08. 049, PMID: 17014880
91. Vasilakis N, Weaver SC. 2008. The history and evolution of human dengue emergence. Advances in Virus Research 72:1–76. DOI: https://doi.org/10.1016/S0065-3527(08)00401-6, PMID: 19081488
92. Walsh PD, Abernethy KA, Bermejo M, Beyers R, De Wachter P, Akou ME, Huijbregts B, Mambounga DI, Toham AK, Kilbourn AM, Lahm SA, Latour S, Maisels F, Mbina C, Mihindou Y, Obiang SN, Effa EN, Starkey MP, Telfer P, Thibault M, et al. 2003. Catastrophic ape decline in western equatorial Africa. Nature 422:611–614. DOI: https://doi.org/10.1038/nature01566, PMID: 12679788
93. Wang E, Ni H, Xu R, Barrett AD, Watowich SJ, Gubler DJ, Weaver SC. 2000. Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. Journal of Virology 74:3227–3234. DOI: https://doi.org/10. 1128/JVI.74.7.3227-3234.2000, PMID: 10708439
94. Weaver SC, Vasilakis N. 2009. Molecular evolution of dengue viruses: contributions of phylogenetics to understanding the history and epidemiology of the preeminent arboviral disease. Infection, Genetics and Evolution 9:523–540. DOI: https://doi.org/10.1016/j.meegid.2009.02.003, PMID: 19460319
95. Wolfe ND, Kilbourn AM, Karesh WB, Rahman HA, Bosi EJ, Cropp BC, Andau M, Spielman A, Gubler DJ. 2001. Sylvatic transmission of arboviruses among Bornean orangutans. The American Journal of Tropical Medicine and Hygiene 64:310–316. DOI: https://doi.org/10.4269/ajtmh.2001.64.310, PMID: 11463123
96. Wu X, Wu FH, Wang X, Wang L, Siedow JN, Zhang W, Pei ZM. 2014. Molecular evolutionary and structural analysis of the cytosolic DNA sensor cGAS and STING. Nucleic Acids Research 42:8243–8257. DOI: https://doi. org/10.1093/nar/gku569, PMID: 24981511
97. Yu CY, Chang TH, Liang JJ, Chiang RL, Lee YL, Liao CL, Lin YL. 2012. Dengue virus targets the adaptor protein MITA to subvert host innate immunity. PLoS Pathogens 8:e1002780. DOI: https://doi.org/10.1371/journal.ppat. 1002780, PMID: 22761576
98. Yusof R, Clum S, Wetzel M, Murthy HM, Padmanabhan R. 2000. Purified NS2B/NS3 serine protease of dengue virus type 2 exhibits cofactor NS2B dependence for cleavage of substrates with dibasic amino acids in vitro. Journal of Biological Chemistry 275:9963–9969. DOI: https://doi.org/10.1074/jbc.275.14.9963, PMID: 10744671
99. Zhang L, Mohan PM, Padmanabhan R. 1992. Processing and localization of Dengue virus type 2 polyprotein precursor NS3-NS4A-NS4B-NS5. Journal of Virology 66:7549–7554. PMID: 1433530
100. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ. 2011. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nature Immunology 12:959–965. DOI: https://doi.org/10.1038/ni.2091, PMID: 21892174
101. Zhong B, Yang Y, Li S, Wang YY, Li Y, Diao F, Lei C, He X, Zhang L, Tien P, Shu HB. 2008. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29:538–550. DOI: https://doi.org/10.1016/j.immuni.2008.09.003, PMID: 18818105
102. Zompi S, Harris E. 2012. Animal models of dengue virus infection. Viruses 4:62–82. DOI: https://doi.org/10.3390/v4010062, PMID: 22355452