Type III interferon-mediated signaling is critical for controlling live attenuated yellow fever virus infection in vivo

mBio

Volumn 8, Issue 4, 2017, Pages

  Douam, Florian ^a   Soto Albrecht, Yentli E ^a   Hrebikova, Gabriela ^a   Sadimin, Evita ^b   Davidson, Christian ^b   Kotenko, Sergei V ^c   Ploss, Alexander ^a  

^a PRINCETON UNIVERSITY   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Flavivirus; Innate immunity; Interferons; Live vector vaccines; Yellow fever virus

Indexed keywords

ALPHA INTERFERON; ALPHA INTERFERON RECEPTOR; BETA INTERFERON; BETA INTERFERON RECEPTOR; INTERFERON; INTERFERON RECEPTOR; INTERFERON RECEPTOR LAMBDA; INTERFERON TYPE III; UNCLASSIFIED DRUG; CYTOKINE; INTERFERON RECEPTOR, TYPE II; LIVE VACCINE; YELLOW FEVER VACCINE;

ADAPTIVE IMMUNITY; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; IMMUNE EVASION; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; IMMUNOMODULATION; IN VIVO STUDY; INFECTION CONTROL; INFECTION PREVENTION; KNOCKOUT MOUSE; MALE; MORTALITY; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; VIRUS LOAD; VIRUS REPLICATION; WILD TYPE MOUSE; YELLOW FEVER; ANIMAL; DEFICIENCY; DISEASE MODEL; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; VIROLOGY; YELLOW FEVER VIRUS;

ANIMALS; BLOOD-BRAIN BARRIER; CYTOKINES; DISEASE MODELS, ANIMAL; IMMUNITY, INNATE; INTERFERONS; MICE; RECEPTORS, INTERFERON; SIGNAL TRANSDUCTION; VACCINES, ATTENUATED; YELLOW FEVER; YELLOW FEVER VACCINE; YELLOW FEVER VIRUS;

EID: 85029171391     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00819-17     Document Type: Article

References (56)

1. Sharp TM, Tomashek KM, Read JS, Margolis HS, Waterman SH. 2017. A new look at an old disease: recent insights into the global epidemiology of dengue. Curr Epidemiol Rep 4:11–21. https://doi.org/10.1007/s40471-017-0095-y.
2. Monath TP, Vasconcelos PFC. 2015. Yellow fever. J Clin Virol 64:160–173. https://doi.org/10.1016/j.jcv.2014.08.030.
3. Calvet GA, Santos FB, Sequeira PC. 2016. Zika virus infection: epidemiology, clinical manifestations and diagnosis. Curr Opin Infect Dis 29: 459–466. https://doi.org/10.1097/QCO.0000000000000301.
4. Monath TP. 2013. 17D yellow fever virus vaccine. Am J Trop Med Hyg 89:1225. https://doi.org/10.4269/ajtmh.13-0443a.
5. Woodall JP, Yuill TM. 2016. Why is the yellow fever outbreak in Angola a “threat to the entire world”? Int J Infect Dis 48:96–97. https://doi.org/10.1016/j.ijid.2016.05.001.
6. Hahn CS, Dalrymple JM, Strauss JH, Rice CM. 1987. Comparison of the virulent Asibi strain of yellow-fever virus with the 17d vaccine strain derived from it. Proc Natl Acad Sci U S A 84:2019–2023. https://doi.org/10.1073/pnas.84.7.2019.
7. Erickson AK, Pfeiffer JK. 2015. Spectrum of disease outcomes in mice infected with YFV-17D. J Gen Virol 96:1328–1339. https://doi.org/10.1099/vir.0.000075.
8. Julander JG. 2016. Animal models of yellow fever and their application in clinical research. Curr Opin Virol 18:64–69. https://doi.org/10.1016/j.coviro.2016.03.010.
9. Platanias LC. 2005. Mechanisms of type-I- and type-II-interferonmediated signalling. Nat Rev Immunol 5:375–386. https://doi.org/10.1038/nri1604.
10. McNab F, Mayer-Barber K, Sher A, Wack A, O’Garra A. 2015. Type I interferons in infectious disease. Nat Rev Immunol 15:87-103. https://doi.org/10.1038/nri3787.
11. van den Broek MF, Müller U, Huang S, Zinkernagel RM, Aguet M. 1995. Immune defence in mice lacking type I and/or type II interferon receptors. Immunol Rev 148:5-18. https://doi.org/10.1111/j.1600-065X.1995.tb00090.x.
12. Meier KC, Gardner CL, Khoretonenko MV, Klimstra WB, Ryman KD. 2009. A mouse model for studying viscerotropic disease caused by yellow fever virus infection. PLoS Pathog 5:e1000614. https://doi.org/10.1371/journal.ppat.1000614.
13. Thibodeaux BA, Garbino NC, Liss NM, Piper J, Blair CD, Roehrig JT. 2012. A small animal peripheral challenge model of yellow fever using interferon-receptor deficient mice and the 17D-204 vaccine strain. Vaccine 30:3180–3187. https://doi.org/10.1016/j.vaccine.2012.03.003.
14. Muñoz-Jordán JL, Laurent-Rolle M, Ashour J, Martínez-Sobrido L, Ashok M, Lipkin WI, García-Sastre A. 2005. Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses. J Virol 79:8004–8013. https://doi.org/10.1128/JVI.79.13.8004-8013.2005.
15. Laurent-Rolle M, Morrison J, Rajsbaum R, Macleod JM, Pisanelli G, Pham A, Ayllon J, Miorin L, Martínez-Romero C, tenOever BR, García-Sastre A. 2014. The interferon signaling antagonist function of yellow fever virus NS5 protein is activated by type I interferon. Cell Host Microbe 16: 314–327. https://doi.org/10.1016/j.chom.2014.07.015.
16. Watson AM, Lam LK, Klimstra WB, Ryman KD. 2016. The 17D-204 vaccine strain-induced protection against virulent yellow fever virus is mediated by humoral immunity and CD4+ but not CD8+ T Cells. PLoS Pathog 12:e1005786. https://doi.org/10.1371/journal.ppat.1005786.
17. Teixeira LK, Fonseca BP, Barboza BA, Viola JP. 2005. The role of interferongamma on immune and allergic responses. Mem Inst Oswaldo Cruz 100(Suppl 1):137–144. https://doi.org/10.1590/S0074-02762005000900024.
18. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP. 2003. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4:69–77. https://doi.org/10.1038/ni875.
19. Wack A, Terczyńska-Dyla E, Hartmann R. 2015. Guarding the frontiers: the biology of type III interferons. Nat Immunol 16:802–809. https://doi.org/10.1038/ni.3212.
20. Lazear HM, Nice TJ, Diamond MS. 2015. Interferon-lambda: immune functions at barrier surfaces and beyond. Immunity 43:15–28. https://doi.org/10.1016/j.immuni.2015.07.001.
21. Kotenko SV, Durbin JE. 2017. Contribution of type III interferons to antiviral immunity: location, location, location. J Biol Chem 292: 7295–7303. https://doi.org/10.1074/jbc.R117.777102.
22. Lazear HM, Daniels BP, Pinto AK, Huang AC, Vick SC, Doyle SE, Gale M, Jr., Klein RS, Diamond MS. 2015. Interferon-lambda restricts West Nile virus neuroinvasion by tightening the blood-brain barrier. Sci Transl Med 7:284ra59. https://doi.org/10.1126/scitranslmed.aaa4304.
23. Douam F, Hrebikova G, Albrecht YE, Sellau J, Sharon Y, Ding Q, Ploss A. 2017. Single-cell tracking of flavivirus RNA uncovers species-specific interactions with the immune system dictating disease outcome. Nat Commun 8:14781. https://doi.org/10.1038/ncomms14781.
24. Marchevsky RS, Freire MS, Coutinho ES, Galler R. 2003. Neurovirulence of yellow fever 17DD vaccine virus to rhesus monkeys. Virology 316:55–63. https://doi.org/10.1016/S0042-6822(03)00583-X.
25. Kitchener S. 2004. Viscerotropic and neurotropic disease following vaccination with the 17D yellow fever vaccine, ARILVAX. Vaccine 22: 2103–2105. https://doi.org/10.1016/j.vaccine.2004.01.026.
26. McMahon AW, Eidex RB, Marfin AA, Russell M, Sejvar JJ, Markoff L, Hayes EB, Chen RT, Ball R, Braun MM, Cetron M, Yellow Fever Working Group. 2007. Neurologic disease associated with 17D-204 yellow fever vaccination: a report of 15 cases. Vaccine 25:1727–1734. https://doi.org/10.1016/j.vaccine.2006.11.027.
27. Garcia-Tapia D, Hassett DE, Mitchell WJ, Jr., Johnson GC, Kleiboeker SB. 2007. West Nile virus encephalitis: sequential histopathological and immunological events in a murine model of infection. J Neurovirol 13:130–138. https://doi.org/10.1080/13550280601187185.
28. Donadieu E, Lowenski S, Servely JL, Laloy E, Lilin T, Nowotny N, Richardson J, Zientara S, Lecollinet S, Coulpier M. 2013. Comparison of the neuropathology induced by two West Nile virus strains. PLoS One 8:e84473. https://doi.org/10.1371/journal.pone.0084473.
29. Fu TL, Ong KC, Tran YD, McLean CA, Wong KT. 2016. Viral neuronotropism is important in the pathogenesis of Murray Valley encephalitis. Neuropathol Appl Neurobiol 42:307–310. https://doi.org/10.1111/nan.12285.
30. Daniels BP, Holman DW, Cruz-Orengo L, Jujjavarapu H, Durrant DM, Klein RS. 2014. Viral pathogen-associated molecular patterns regulate bloodbrain barrier integrity via competing innate cytokine signals. mBio 5:e01476-14. https://doi.org/10.1128/mBio.01476-14.
31. Winkelmann ER, Luo H, Wang T. 26 January 2016. West Nile virus infection in the central nervous system. F 1000 Res https://f1000research.com/articles/5-105/v1.
32. Egli A, Santer DM, O’Shea D, Tyrrell DL, Houghton M. 2014. The impact of the interferon-lambda family on the innate and adaptive immune response to viral infections. Emerg Microbes Infect 3:e51. https://doi.org/10.1038/emi.2014.51.
33. Misumi I, Whitmire JK. 2014. IFN-lambda exerts opposing effects on T cell responses depending on the chronicity of the virus infection. J Immunol 192:3596–3606. https://doi.org/10.4049/jimmunol.1301705.
34. Nolz JC, Starbeck-Miller GR, Harty JT. 2011. Naive, effector and memory CD8 T-cell trafficking: parallels and distinctions. Immunotherapy 3:1223–1233. https://doi.org/10.2217/imt.11.100.
35. Pennock ND, White JT, Cross EW, Cheney EE, Tamburini BA, Kedl RM. 2013. T cell responses: naive to memory and everything in between. Adv Physiol Educ 37:273–283. https://doi.org/10.1152/advan.00066.2013.
36. Berard M, Tough DF. 2002. Qualitative differences between naive and memory T cells. Immunology 106:127–138. https://doi.org/10.1046/j.1365-2567.2002.01447.x.
37. Carrette F, Surh CD. 2012. IL-7 signaling and CD127 receptor regulation in the control of T cell homeostasis. Semin Immunol 24:209–217. https://doi.org/10.1016/j.smim.2012.04.010.
38. Mahnke YD, Brodie TM, Sallusto F, Roederer M, Lugli E. 2013. The who’s who of T-cell differentiation: human memory T-cell subsets. Eur J Immunol 43:2797–2809. https://doi.org/10.1002/eji.201343751.
39. Baaten BJG, Tinoco R, Chen AT, Bradley LM. 2012. Regulation of antigenexperienced T cells: lessons from the quintessential memory marker CD44. Front Immunol 3:23. https://doi.org/10.3389/fimmu.2012.00023.
40. Chai Q, He WQ, Zhou M, Lu H, Fu ZF. 2014. Enhancement of blood-brain barrier permeability and reduction of tight junction protein expression are modulated by chemokines/cytokines induced by rabies virus infection. J Virol 88:4698–4710. https://doi.org/10.1128/JVI.03149-13.
41. Querec TD, Akondy RS, Lee EK, Cao W, Nakaya HI, Teuwen D, Pirani A, Gernert K, Deng J, Marzolf B, Kennedy K, Wu H, Bennouna S, Oluoch H, Miller J, Vencio RZ, Mulligan M, Aderem A, Ahmed R, Pulendran B. 2009. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol 10:116–125. https://doi.org/10.1038/ni.1688.
42. Crotta S, Davidson S, Mahlakoiv T, Desmet CJ, Buckwalter MR, Albert ML, Staeheli P, Wack A. 2013. Type I and type III interferons drive redundant amplification loops to induce a transcriptional signature in influenzainfected airway epithelia. PLoS Pathog 9:e1003773. https://doi.org/10.1371/journal.ppat.1003773.
43. Mahlakõiv T, Ritz D, Mordstein M, DeDiego ML, Enjuanes L, Müller MA, Drosten C, Staeheli P. 2012. Combined action of type I and type III interferon restricts initial replication of severe acute respiratory syndrome coronavirus in the lung but fails to inhibit systemic virus spread. J Gen Virol 93:2601–2605. https://doi.org/10.1099/vir.0.046284-0.
44. Pott J, Mahlakõiv T, Mordstein M, Duerr CU, Michiels T, Stockinger S, Staeheli P, Hornef MW. 2011. IFN-lambda determines the intestinal epithelial antiviral host defense. Proc Natl Acad Sci U S A 108:7944–7949. https://doi.org/10.1073/pnas.1100552108.
45. Nice TJ, Baldridge MT, McCune BT, Norman JM, Lazear HM, Artyomov M, Diamond MS, Virgin HW. 2015. Interferon-lambda cures persistent murine norovirus infection in the absence of adaptive immunity. Science 347:269–273. https://doi.org/10.1126/science.1258100.
46. Hermant P, Michiels T. 2014. Interferon-lambda in the context of viral infections: production, response and therapeutic implications. J Innate Immun 6:563–574. https://doi.org/10.1159/000360084.
47. Yin Z, Dai J, Deng J, Sheikh F, Natalia M, Shih T, Lewis-Antes A, Amrute SB, Garrigues U, Doyle S, Donnelly RP, Kotenko SV, Fitzgerald-Bocarsly P. 2012. Type III IFNs are produced by and stimulate human plasmacytoid dendritic cells. J Immunol 189:2735–2745. https://doi.org/10.4049/jimmunol.1102038.
48. Bruewer M, Utech M, Ivanov AI, Hopkins AM, Parkos CA, Nusrat A. 2005. Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J 19:923–933. https://doi.org/10.1096/fj.04-3260com.
49. Srinivas S, Dai J, Eskdale J, Gallagher GE, Megjugorac NJ, Gallagher G. 2008. Interferon-lambda1 (interleukin-29) preferentially down-regulates interleukin-13 over other T helper type 2 cytokine responses in vitro. Immunology 125:492–502. https://doi.org/10.1111/j.1365-2567.2008.02862.x.
50. Dai J, Megjugorac NJ, Gallagher GE, Yu RY, Gallagher G. 2009. IFNlambda1 (IL-29) inhibits GATA3 expression and suppresses Th2 responses in human naive and memory T cells. Blood 113:5829–5838. https://doi.org/10.1182/blood-2008-09-179507.
51. Douam F, Gaska JM, Winer BY, Ding Q, von Schaewen M, Ploss A. 2015. Genetic dissection of the host tropism of human-tropic pathogens. Annu Rev Genet 49:21–45. https://doi.org/10.1146/annurev-genet-112414-054823.
52. Beck A, Tesh RB, Wood TG, Widen SG, Ryman KD, Barrett AD. 2014. Comparison of the live attenuated yellow fever vaccine 17D-204 strain to its virulent parental strain Asibi by deep sequencing. J Infect Dis 209:334–344. https://doi.org/10.1093/infdis/jit546.
53. Belsher JL, Gay P, Brinton M, DellaValla J, Ridenour R, Lanciotti R, Perelygin A, Zaki S, Paddock C, Querec T, Zhu T, Pulendran B, Eidex RB, Hayes E. 2007. Fatal multiorgan failure due to yellow fever vaccineassociated viscerotropic disease. Vaccine 25:8480–8485. https://doi.org/10.1016/j.vaccine.2007.08.061.
54. Pulendran B, Miller J, Querec TD, Akondy R, Moseley N, Laur O, Glidewell J, Monson N, Zhu T, Zhu H, Staprans S, Lee D, Brinton MA, Perelygin AA, Vellozzi C, Brachman P, Lalor S, Teuwen D, Eidex RB, Cetron M, Priddy F, del Rio C, Altman J, Ahmed R. 2008. Case of yellow fever vaccineassociated viscerotropic disease with prolonged viremia, robust adaptive immune responses, and polymorphisms in CCR5 and RANTES genes. J Infect Dis 198:500–507. https://doi.org/10.1086/590187.
55. Lin JD, Feng N, Sen A, Balan M, Tseng HC, McElrath C, Smirnov SV, Peng J, Yasukawa LL, Durbin RK, Durbin JE, Greenberg HB, Kotenko SV. 2016. Distinct roles of type I and type III interferons in intestinal immunity to homologous and heterologous Rotavirus infections. PLoS Pathog 12: e1005600. https://doi.org/10.1371/journal.ppat.1005600.
56. Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, Heinzen EL, Qiu P, Bertelsen AH, Muir AJ, Sulkowski M, McHutchison JG, Goldstein DB. 2009. Genetic variation in IL28B predicts hepatitis C treatmentinduced viral clearance. Nature 461:399–401.