Synthetic toll-like receptor 4 (TLR4) and TLR7 ligands work additively via Myd88 to induce protective antiviral immunity in mice

Journal of Virology

Volumn 91, Issue 19, 2017, Pages

  Goff, Peter H ^a   Hayashi, Tomoko ^a   He, Wenqian ^a   Yao, Shiyin ^a   Cottam, Howard B ^a   Tan, Gene S ^a   Crain, Brian ^a   Krammer, Florian ^a   Messer, Karen ^a   Pu, Minya ^a   Carson, Dennis A ^a   Palese, Peter ^a,b   Corr, Maripat ^c  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Adjuvant; Influenza virus; TLR4; TLR7; Toll like receptor; vaccine

Indexed keywords

IMMUNOLOGICAL ADJUVANT; INFLUENZA VACCINE; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; INFLUENZA VIRUS HEMAGGLUTININ; MEMBRANE PROTEIN; MYD88 PROTEIN, MOUSE; TICAM-1 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; TLR7 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN; VIRUS ANTIBODY; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFECT; FEMALE; HUMORAL IMMUNITY; IMMUNOGENICITY; INFECTION PREVENTION; INFLUENZA A (H1N1); INFLUENZA VACCINATION; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T CELL DEPLETION; VIRUS TITRATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); KNOCKOUT MOUSE; LUNG; ORTHOMYXOVIRIDAE INFECTIONS; TH1 CELL; TH2 CELL; VACCINATION; VIROLOGY;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; FEMALE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; LUNG; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; ORTHOMYXOVIRIDAE INFECTIONS; TH1 CELLS; TH2 CELLS; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 7; VACCINATION;

EID: 85029227796     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01050-17     Document Type: Article

References (49)

1. Ohmit SE, Petrie JG, Malosh RE, Cowling BJ, Thompson MG, Shay DK, Monto AS. 2013. Influenza vaccine effectiveness in the community and the household. Clin Infect Dis 56:1363-1369. https://doi.org/10.1093/ cid/cit060.
2. Thompson WW, Comanor L, Shay DK. 2006. Epidemiology of seasonal influenza: use of surveillance data and statistical models to estimate the burden of disease. J Infect Dis 194:S82-S91. https://doi.org/10.1086/ 507558.
3. Hannoun C. 2013. The evolving history of influenza viruses and influenza vaccines. Expert Rev Vaccines 12:1085-1094. https://doi.org/10.1586/ 14760584.2013.824709.
4. Smith GJ, Bahl J, Vijaykrishna D, Zhang J, Poon LL, Chen H, Webster RG, Peiris JS, Guan Y. 2009. Dating the emergence of pandemic influenza viruses. Proc Natl Acad Sci U S A 106:11709-11712. https://doi.org/10 .1073/pnas.0904991106.
5. Cox RJ. 2013. Correlates of protection to influenza virus, where do we go from here? Hum Vaccin Immunother 9:405-408. https://doi.org/ 10.4161/hv.22908.
6. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC, de Jong JC, Kelso A, Klimov AI, Kageyama T, Komadina N, Lapedes AS, Lin YP, Mosterin A, Obuchi M, Odagiri T, Osterhaus ADME, Rimmelzwaan GF, Shaw MW, Skepner E, Stohr K, Tashiro M, Fouchier RAM, Smith DJ. 2008. Influenza vaccine strain selection and recent studies on the global migration of seasonal influenza viruses. Vaccine 26:D31-D34. https://doi.org/10.1016/j.vaccine.2008.07 .078.
7. Steel J, Lowen AC, Wang TT, Yondola M, Gao Q, Haye K, Garcia-Sastre A, Palese P. 2010. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio 1:e00018-10. https://doi.org/10.1128/mBio .00018-10.
8. Wang TT, Tan GS, Hai R, Pica N, Ngai L, Ekiert DC, Wilson IA, Garcia-Sastre A, Moran TM, Palese P. 2010. Vaccination with a synthetic peptide from the influenza virus hemagglutinin provides protection against distinct viral subtypes. Proc Natl Acad Sci U S A 107:18979-18984. https://doi .org/10.1073/pnas.1013387107.
9. Krammer F, Margine I, Hai R, Flood A, Hirsh A, Tsvetnitsky V, Chen D, Palese P. 2014. H3 stalk-based chimeric hemagglutinin influenza virus constructs protect mice from H7N9 challenge. J Virol 88:2340-2343. https://doi.org/10.1128/JVI.03183-13.
10. Krammer F, Palese P. 2014. Universal influenza virus vaccines: need for clinical trials. Nat Immunol 15:3-5. https://doi.org/10.1038/nri3797.
11. Krammer F, Palese P. 2013. Influenza virus hemagglutinin stalk-based antibodies and vaccines. Curr Opin Virol 3:521-530. https://doi.org/10 .1016/j.coviro.2013.07.007.
12. Krammer F, Palese P, Steel J. 2015. Advances in universal influenza virus vaccine design and antibody mediated therapies based on conserved regions of the hemagglutinin. Curr Top Microbiol Immunol 386:301-321. https://doi.org/10.1007/82_2014_408.
13. Krammer F, Pica N, Hai R, Margine I, Palese P. 2013. Chimeric hemagglutinin influenza virus vaccine constructs elicit broadly protective stalk-specific antibodies. J Virol 87:6542-6550. https://doi.org/10 .1128/JVI.00641-13.
14. Clegg CH, Roque R, Hoeven NV, Perrone L, Baldwin SL, Rininger JA, Bowen RA, Reed SG. 2012. Adjuvant solution for pandemic influenza vaccine production. Proc Natl Acad Sci U S A 109:17585-17590. https:// doi.org/10.1073/pnas.1207308109.
15. Martinez-Gil L, Goff PH, Hai R, Garcia-Sastre A, Shaw ML, Palese P. 2013. A Sendai virus-derived RNA agonist of RIG-I as a virus vaccine adjuvant. J Virol 87:1290-1300. https://doi.org/10.1128/JVI.02338-12.
16. Reed SG, Orr MT, Fox CB. 2013. Key roles of adjuvants in modern vaccines. Nat Med 19:1597-1608. https://doi.org/10.1038/nm.3409.
17. Goff PH, Eggink D, Seibert CW, Hai R, Martinez-Gil L, Krammer F, Palese P. 2013. Adjuvants and immunization strategies to induce influenza virus hemagglutinin stalk antibodies. PLoS One 8:e79194. https://doi.org/10 .1371/journal.pone.0079194.
18. Goff PH, Hayashi T, Martinez-Gil L, Corr M, Crain B, Yao S, Cottam HB, Chan M, Ramos I, Eggink D, Heshmati M, Krammer F, Messer K, Pu M, Fernandez-Sesma A, Palese P, Carson DA. 2015. Synthetic Toll-like receptor 4 (TLR4) and TLR7 ligands as influenza virus vaccine adjuvants induce rapid, sustained, and broadly protective responses. J Virol 89: 3221-3235. https://doi.org/10.1128/JVI.03337-14.
19. O'Hagan DT, Rappuoli R, De Gregorio E, Tsai T, Del Giudice G. 2011. MF59 adjuvant: the best insurance against influenza strain diversity. Expert Rev Vaccines 10:447-462. https://doi.org/10.1586/erv.11.23.
20. Camilloni B, Basileo M, Valente S, Nunzi E, Iorio AM. 2015. Immunogenicity of intramuscular MF59-adjuvanted and intradermal administered influenza enhanced vaccines in subjects aged over 60: a literature review. Hum Vaccin Immunother 11:553-563. https://doi.org/10.1080/ 21645515.2015.1011562.
21. Van Buynder PG, Konrad S, Van Buynder JL, Brodkin E, Krajden M, Ramler G, Bigham M. 2013. The comparative effectiveness of adjuvanted and unadjuvanted trivalent inactivated influenza vaccine (TIV) in the elderly. Vaccine 31:6122-6128. https://doi.org/10.1016/j.vaccine.2013.07.059.
22. Chan M, Hayashi T, Mathewson RD, Nour A, Hayashi Y, Yao S, Tawatao RI, Crain B, Tsigelny IF, Kouznetsova VL, Messer K, Pu M, Corr M, Carson DA, Cottam HB. 2013. Identification of substituted pyrimido[5,4-b]indoles as selective Toll-like receptor 4 ligands. J Med Chem 56:4206-4223. https:// doi.org/10.1021/jm301694x.
23. Chan M, Hayashi T, Kuy CS, Gray CS, Wu CC, Corr M, Wrasidlo W, Cottam HB, Carson DA. 2009. Synthesis and immunological characterization of toll-like receptor 7 agonistic conjugates. Bioconjug Chem 20:1194-1200. https://doi.org/10.1021/bc900054q.
24. Chan M, Hayashi T, Mathewson RD, Yao S, Gray C, Tawatao RI, Kalenian K, Zhang Y, Hayashi Y, Lao FS, Cottam HB, Carson DA. 2011. Synthesis and characterization of PEGylated toll like receptor 7 ligands. Bioconjug Chem 22:445-454. https://doi.org/10.1021/bc1004813.
25. Krammer F, Pica N, Hai R, Tan GS, Palese P. 2012. Hemagglutinin stalkreactive antibodies are boosted following sequential infection with seasonal and pandemic H1N1 influenza virus in mice. J Virol 86: 10302-10307. https://doi.org/10.1128/JVI.01336-12.
26. Margine I, Hai R, Albrecht RA, Obermoser G, Harrod AC, Banchereau J, Palucka K, Garcia-Sastre A, Palese P, Treanor JJ, Krammer F. 2013. H3N2 influenza virus infection induces broadly reactive hemagglutinin stalk antibodies in humans and mice. J Virol 87:4728-4737. https://doi.org/ 10.1128/JVI.03509-12.
27. Margine I, Krammer F, Hai R, Heaton NS, Tan GS, Andrews SA, Runstadler JA, Wilson PC, Albrecht RA, Garcia-Sastre A, Palese P. 2013. Hemagglutinin stalk-based universal vaccine constructs protect against group 2 influenza A viruses. J Virol 87:10435-10446. https://doi.org/10.1128/JVI .01715-13.
28. Pica N, Hai R, Krammer F, Wang TT, Maamary J, Eggink D, Tan GS, Krause JC, Moran T, Stein CR, Banach D, Wrammert J, Belshe RB, Garcia-Sastre A, Palese P. 2012. Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses. Proc Natl Acad Sci U S A 109:2573-2578. https://doi.org/ 10.1073/pnas.1200039109.
29. Martin ME, Dieter JA, Luo Z, Baumgarth N, Solnick JV. 2012. Predicting the outcome of infectious diseases: variability among inbred mice as a new and powerful tool for biomarker discovery. mBio 3:e00199-12. https://doi.org/10.1128/mBio.00199-12.
30. Aoshi T, Koyama S, Kobiyama K, Akira S, Ishii KJ. 2011. Innate and adaptive immune responses to viral infection and vaccination. Curr Opin Virol 1:226-232. https://doi.org/10.1016/j.coviro.2011.07.002.
31. Akira S. 2011. Innate immunity and adjuvants. Philos Trans R Soc Lond B Biol Sci 366:2748-2755. https://doi.org/10.1098/rstb.2011.0106.
32. Wheeler CM, Skinner SR, Del Rosario-Raymundo MR, Garland SM, Chatterjee A, Lazcano-Ponce E, Salmerón J, McNeil S, Stapleton JT, Bouchard C, Martens MG, Money DM, Quek SC, Romanowski B, Vallejos CS, ter Harmsel B, Prilepskaya V, Fong KL, Kitchener H, Minkina G, Lim YKT, Stoney T, Chakhtoura N, Cruickshank ME, Savicheva A, da Silva DP, Ferguson M, Molijn AC, Quint WGV, Hardt K, Descamps D, Suryakiran PV, Karkada N, Geeraerts B, Dubin G, Struyf F. 2016. Efficacy, safety, and immunogenicity of the human papillomavirus 16/18 AS04-adjuvanted vaccine in women older than 25 years: 7-year follow-up of the phase 3, double-blind, randomised controlled VIVIANE study. Lancet Infect Dis 16:1154-1168. https://doi.org/10.1016/S1473-3099(16)30120-7.
33. Kasturi SP, Kozlowski PA, Nakaya HI, Burger MC, Russo P, Pham M, Kovalenkov Y, Silveira EL, Havenar-Daughton C, Burton SL, Kilgore KM, Johnson MJ, Nabi R, Legere T, Sher ZJ, Chen X, Amara RR, Hunter E, Bosinger SE, Spearman P, Crotty S, Villinger F, Derdeyn CA, Wrammert J, Pulendran B. 2017. Adjuvanting a simian immunodeficiency virus vaccine with Toll-like receptor ligands encapsulated in nanoparticles induces persistent antibody responses and enhanced protection in TRIM5α restrictive macaques. J Virol 91:e01844-16. https://doi.org/10 .1128/JVI.01844-16.
34. Kasturi SP, Skountzou I, Albrecht RA, Koutsonanos D, Hua T, Nakaya HI, Ravindran R, Stewart S, Alam M, Kwissa M, Villinger F, Murthy N, Steel J, Jacob J, Hogan RJ, Garcia-Sastre A, Compans R, Pulendran B. 2011. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 470:543-547. https://doi.org/10.1038/ nature09737.
35. Iyer SS, Gangadhara S, Victor B, Shen X, Chen X, Nabi R, Kasturi SP, Sabula MJ, Labranche CC, Reddy PB, Tomaras GD, Montefiori DC, Moss B, Spearman P, Pulendran B, Kozlowski PA, Amara RR. 2016. Virus-like particles displaying trimeric simian immunodeficiency virus (SIV) envelope gp160 enhance the breadth of DNA/modified vaccinia virus Ankara SIV vaccine-induced antibody responses in rhesus macaques. J Virol 90:8842-8854. https://doi.org/10.1128/JVI.01163-16.
36. Zens KD, Farber DL. 2015. Memory CD4 T cells in influenza. Curr Top Microbiol Immunol 386:399-421. https://doi.org/10.1007/82_2014_401.
37. Wilkinson TM, Li CK, Chui CS, Huang AK, Perkins M, Liebner JC, Lambkin-Williams R, Gilbert A, Oxford J, Nicholas B, Staples KJ, Dong T, Douek DC, McMichael AJ, Xu XN. 2012. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat Med 18:274-280. https://doi.org/10.1038/nm.2612.
38. Nakaya HI, Clutterbuck E, Kazmin D, Wang L, Cortese M, Bosinger SE, Patel NB, Zak DE, Aderem A, Dong T, Del Giudice G, Rappuoli R, Cerundolo V, Pollard AJ, Pulendran B, Siegrist CA. 2016. Systems biology of immunity to MF59-adjuvanted versus nonadjuvanted trivalent seasonal influenza vaccines in early childhood. Proc Natl Acad Sci U S A 113: 1853-1858. https://doi.org/10.1073/pnas.1519690113.
39. Garcia-Sicilia J, Aristegui J, Omenaca F, Carmona A, Tejedor JC, Merino JM, Garcia-Corbeira P, Walravens K, Bambure V, Moris P, Caplanusi A, Gillard P, Dieussaert I. 2015. Safety and persistence of the humoral and cellular immune responses induced by 2 doses of an AS03-adjuvanted A(H1N1)pdm09 pandemic influenza vaccine administered to infants, children and adolescents: two open, uncontrolled studies. Hum Vaccin Immunother 11:2359-2369. https://doi.org/10 .1080/21645515.2015.1063754.
40. Pedersen GK, Sjursen H, Nostbakken JK, Jul-Larsen A, Hoschler K, Cox RJ. 2014. Matrix M(TM) adjuvanted virosomal H5N1 vaccine induces balanced Th1/Th2 CD4+ T cell responses in man. Hum Vaccin Immunother 10:2408-2416. https://doi.org/10.4161/hv.29583.
41. Spensieri F, Siena E, Borgogni E, Zedda L, Cantisani R, Chiappini N, Schiavetti F, Rosa D, Castellino F, Montomoli E, Bodinham CL, Lewis DJ, Medini D, Bertholet S, Del Giudice G. 2016. Early rise of blood T follicular helper cell subsets and baseline immunity as predictors of persisting late functional antibody responses to vaccination in humans. PLoS One 11:e0157066. https://doi.org/10.1371/journal.pone.0157066.
42. Pedersen GK, Madhun AS, Breakwell L, Hoschler K, Sjursen H, Pathirana RD, Goudsmit J, Cox RJ. 2012. T-helper 1 cells elicited by H5N1 vaccination predict seroprotection. J Infect Dis 206:158-166. https://doi.org/10 .1093/infdis/jis330.
43. Cox F, Baart M, Huizingh J, Tolboom J, Dekking L, Goudsmit J, Saeland E, Radošević K. 2015. Protection against H5N1 influenza virus induced by matrix-M adjuvanted seasonal virosomal vaccine in mice requires both antibodies and T cells. PLoS One 10:e0145243. https://doi.org/10.1371/ journal.pone.0145243.
44. Ahmed SS, Schur PH, MacDonald NE, Steinman L. 2014. Narcolepsy, 2009 A(H1N1) pandemic influenza, and pandemic influenza vaccinations: what is known and unknown about the neurological disorder, the role for autoimmunity, and vaccine adjuvants. J Autoimmun 50:1-11. https:// doi.org/10.1016/j.jaut.2014.01.033.
45. Fox CB, Haensler J. 2013. An update on safety and immunogenicity of vaccines containing emulsion-based adjuvants. Expert Rev Vaccines 12: 747-758. https://doi.org/10.1586/14760584.2013.811188.
46. Hayashi T, Gray CS, Chan M, Tawatao RI, Ronacher L, McGargill MA, Datta SK, Carson DA, Corr M. 2009. Prevention of autoimmune disease by induction of tolerance to Toll-like receptor 7. Proc Natl Acad Sci U S A 106:2764-2769. https://doi.org/10.1073/pnas.0813037106.
47. Krammer F, Grabherr R. 2010. Alternative influenza vaccines made by insect cells. Trends Mol Med 16:313-320. https://doi.org/10.1016/j .molmed.2010.05.002.
48. Krammer F, Margine I, Tan GS, Pica N, Krause JC, Palese P. 2012. A carboxy-terminal trimerization domain stabilizes conformational epitopes on the stalk domain of soluble recombinant hemagglutinin substrates. PLoS One 7:e43603. https://doi.org/10.1371/journal.pone .0043603.
49. Hai R, Martinez-Sobrido L, Fraser KA, Ayllon J, Garcia-Sastre A, Palese P. 2008. Influenza B virus NS1-truncated mutants: live-attenuated vaccine approach. J Virol 82:10580-10590. https://doi.org/10.1128/JVI.01213-08.