Intranasal introduction of Fc-fused interleukin-7 provides long-lasting prophylaxis against lethal influenza virus infection

Journal of Virology

Volumn 90, Issue 5, 2016, Pages 2273-2284

  Kang, Moon Cheol ^a   Choi, Dong Hoon ^a   Choi, Young Woo ^a   Park, Seong Jeong ^a   Namkoong, Hong ^a   Park, Ki Seok ^a   Ahn, So Shin ^a   Surh, Charles D ^a   Yoon, Sun Woo ^b   Kim, Doo Jin ^b   Choi, Jung ah ^c   Park, Yunji ^a   Sung, Young Chul ^a   Lee, Seung Woo ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^c International Vaccine Institute   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

FC FUSED INTERLEUKIN 7; INTERLEUKIN 7; UNCLASSIFIED DRUG; HYBRID PROTEIN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOLOGIC FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; FEMALE; IMMUNOPATHOLOGY; INFLUENZA; MEMORY T LYMPHOCYTE; MORTALITY; MOUSE; NONHUMAN; OPTIMAL DRUG DOSE; PRIORITY JOURNAL; SINGLE DRUG DOSE; TRANSCYTOSIS; VIRAL CLEARANCE; VIRUS INHIBITION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS; INTRANASAL DRUG ADMINISTRATION; LUNG; LYMPHOCYTE DEPLETION; ORTHOMYXOVIRIDAE INFECTIONS; T LYMPHOCYTE;

ADMINISTRATION, INTRANASAL; ANIMALS; FEMALE; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOLOGIC FACTORS; INFLUENZA A VIRUS; INTERLEUKIN-7; LUNG; LYMPHOCYTE DEPLETION; MICE, INBRED BALB C; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE INFECTIONS; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES;

EID: 84961147501     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02768-15     Document Type: Article

References (47)

1. Tumpey TM, Belser JA. 2009. Resurrected pandemic influenza viruses. Annu Rev Microbiol 63:79-98. http://dx.doi.org/10.1146/annurev.micro.091208.073359.
2. Cowling BJ, Jin L, Lau EH, Liao Q, Wu P, Jiang H, Tsang TK, Zheng J, Fang VJ, Chang Z, Ni MY, Zhang Q, Ip DK, Yu J, Li Y, Wang L, Tu W, Meng L, Wu JT, Luo H, Li Q, Shu Y, Li Z, Feng Z, Yang W, Wang Y, Leung GM, Yu H. 2013. Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: a population-based study of laboratory-confirmed cases. Lancet 382:129-137. http://dx.doi.org/10.1016/S0140-6736(13)61171-X.
3. Taubenberger JK, Morens DM. 2010. Influenza: the once and future pandemic. Public Health Rep 125(Suppl 3):S16-S26.
4. Kramer SC, Bansal S. 2015. Assessing the use of antiviral treatment to control influenza. Epidemiol Infect 143:1621-1631. http://dx.doi.org/10.1017/S0950268814002520.
5. Dunning J, Baillie JK, Cao B, Hayden FG. 2014. Antiviral combinations for severe influenza. Lancet Infect Dis 14:1259-1270. http://dx.doi.org/10.1016/S1473-3099(14)70821-7.
6. Hurt AC, Holien JK, Parker M, Kelso A, Barr IG. 2009. Zanamivirresistant influenza viruses with a novel neuraminidase mutation. J Virol 83:10366-10373. http://dx.doi.org/10.1128/JVI.01200-09.
7. Damjanovic D, Small CL, Jeyanathan M, McCormick S, Xing Z. 2012. Immunopathology in influenza virus infection: uncoupling the friend from foe. Clin Immunol 144:57-69. http://dx.doi.org/10.1016/j.clim.2012.05.005.
8. Kuiken T, Riteau B, Fouchier RA, Rimmelzwaan GF. 2012. Pathogenesis of influenza virus infections: the good, the bad and the ugly. Curr Opin Virol 2:276-286. http://dx.doi.org/10.1016/j.coviro.2012.02.013.
9. To KK, Hung IF, Li IW, Lee KL, Koo CK, Yan WW, Liu R, Ho KY, Chu KH, Watt CL, Luk WK, Lai KY, Chow FL, Mok T, Buckley T, Chan JF, Wong SS, Zheng B, Chen H, Lau CC, Tse H, Cheng VC, Chan KH, Yuen KY. 2010. Delayed clearance of viral load and marked cytokine activation in severe cases of pandemic H1N1 2009 influenza virus infection. Clin Infect Dis 50:850-859. http://dx.doi.org/10.1086/650581.
10. Perrone LA, Plowden JK, Garcia-Sastre A, Katz JM, Tumpey TM. 2008. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 4:e1000115. http://dx.doi.org/10.1371/journal.ppat.1000115.
11. Shirey KA, Lai W, Scott AJ, Lipsky M, Mistry P, Pletneva LM, Karp CL, McAlees J, Gioannini TL, Weiss J, Chen WH, Ernst RK, Rossignol DP, Gusovsky F, Blanco JC, Vogel SN. 2013. The TLR4 antagonist Eritoran protects mice from lethal influenza infection. Nature 497:498-502. http://dx.doi.org/10.1038/nature12118.
12. Marsolais D, Hahm B, Walsh KB, Edelmann KH, McGavern D, Hatta Y, Kawaoka Y, Rosen H, Oldstone MB. 2009. A critical role for the sphingosine analog AAL-R in dampening the cytokine response during influenza virus infection. Proc Natl Acad Sci U S A 106:1560-1565. http://dx.doi.org/10.1073/pnas.0812689106.
13. Coulombe F, Jaworska J, Verway M, Tzelepis F, Massoud A, Gillard J, Wong G, Kobinger G, Xing Z, Couture C, Joubert P, Fritz JH, Powell WS, Divangahi M. 2014. Targeted prostaglandin E2 inhibition enhances antiviral immunity through induction of type I interferon and apoptosis in macrophages. Immunity 40:554-568. http://dx.doi.org/10.1016/j.immuni.2014.02.013.
14. Darwish I, Mubareka S, Liles WC. 2011. Immunomodulatory therapy for severe influenza. Expert Rev Anti Infect Ther 9:807-822. http://dx.doi.org/10.1586/eri.11.56.
15. Maines TR, Szretter KJ, Perrone L, Belser JA, Bright RA, Zeng H, Tumpey TM, Katz JM. 2008. Pathogenesis of emerging avian influenza viruses in mammals and the host innate immune response. Immunol Rev 225:68-84. http://dx.doi.org/10.1111/j.1600-065X.2008.00690.x.
16. Ji H, Gu Q, Chen LL, Xu K, Ling X, Bao CJ, Tang FY, Qi X, Wu YQ, Ai J, Shen GY, Dong DJ, Yu HY, Huang M, Cao Q, Xu Y, Zhao W, Xu YT, Xia Y, Chen SH, Yang GL, Gu CL, Xie GX, Zhu YF, Zhu FC, Zhou MH. 2014. Epidemiological and clinical characteristics and risk factors for death of patients with avian influenza A H7N9 virus infection from Jiangsu Province, Eastern China. PLoS One 9:e89581. http://dx.doi.org/10.1371/journal.pone.0089581.
17. Kim TS, Sun J, Braciale TJ. 2011. T cell responses during influenza infection: getting and keeping control. Trends Immunol 32:225-231. http://dx.doi.org/10.1016/j.it.2011.02.006.
18. Teijaro JR, Turner D, Pham Q, Wherry EJ, Lefrancois L, Farber DL. 2011. Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J Immunol 187:5510-5514. http://dx.doi.org/10.4049/jimmunol.1102243.
19. Wu T, Hu Y, Lee YT, Bouchard KR, Benechet A, Khanna K, Cauley LS. 2014. Lung-resident memory CD8 T cells (TRM) are indispensable for optimal cross-protection against pulmonary virus infection. J Leukoc Biol 95:215-224. http://dx.doi.org/10.1189/jlb.0313180.
20. 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 influenzaspecific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat Med 18:274-280. http://dx.doi.org/10.1038/nm.2612.
21. McMaster SR, Gabbard JD, Koutsonanos DG, Compans RW, Tripp RA, Tompkins SM, Kohlmeier JE. 2015. Memory T cells generated by prior exposure to influenza cross react with the novel H7N9 influenza virus and confer protective heterosubtypic immunity. PLoS One 10:e0115725. http://dx.doi.org/10.1371/journal.pone.0115725.
22. Strutt TM, McKinstry KK, Dibble JP, Winchell C, Kuang Y, Curtis JD, Huston G, Dutton RW, Swain SL. 2010. Memory CD4+ T cells induce innate responses independently of pathogen. Nat Med 16:558-564. http://dx.doi.org/10.1038/nm.2142.
23. Swain SL, McKinstry KK, Strutt TM. 2012. Expanding roles for CD4(+) T cells in immunity to viruses. Nat Rev Immunol 12:136-148. http://dx.doi.org/10.1038/nri3152.
24. Mackall CL, Fry TJ, Gress RE. 2011. Harnessing the biology of IL-7 for therapeutic application. Nat Rev Immunol 11:330-342. http://dx.doi.org/10.1038/nri2970.
25. Park SH, Song MY, Nam HJ, Im SJ, Sung YC. 2010. Codelivery of IL-7 augments multigenic HCV DNA vaccine-induced antibody as well as broad T cell responses in cynomolgus monkeys. Immune Netw 10:198-205. http://dx.doi.org/10.4110/in.2010.10.6.198.
26. Nam HJ, Song MY, Choi DH, Yang SH, Jin HT, Sung YC. 2010. Marked enhancement of antigen-specific T-cell responses by IL-7-fused nonlytic, but not lytic, Fc as a genetic adjuvant. Eur J Immunol 40:351-358. http://dx.doi.org/10.1002/eji.200939271.
27. Seo YB, Im SJ, Namkoong H, Kim SW, Choi YW, Kang MC, Lim HS, Jin HT, Yang SH, Cho ML, Kim YM, Lee SW, Choi YK, Surh CD, Sung YC. 2014. Crucial roles of interleukin-7 in the development of T follicular helper cells and in the induction of humoral immunity. J Virol 88:8998-9009. http://dx.doi.org/10.1128/JVI.00534-14.
28. Kim ES, Jang do S, Yang SY, Lee MN, Jin KS, Cha HJ, Kim JK, Sung YC, Choi KY. 2013. Controlled release of human growth hormone fused with a human hybrid Fc fragment through a nanoporous polymer membrane. Nanoscale 5:4262-4269. http://dx.doi.org/10.1039/c3nr00474k.
29. Song MS, Pascua PN, Lee JH, Baek YH, Lee OJ, Kim CJ, Kim H, Webby RJ, Webster RG, Choi YK. 2009. The polymerase acidic protein gene of influenza A virus contributes to pathogenicity in a mouse model. J Virol 83:12325-12335. http://dx.doi.org/10.1128/JVI.01373-09.
30. Kim EH, Lee JH, Pascua PN, Song MS, Baek YH, Kwon HI, Park SJ, Lim GJ, Decano A, Chowdhury MY, Seo SK, Song MK, Kim CJ, Choi YK. 2013. Prokaryote-expressed M2e protein improves H9N2 influenza vaccine efficacy and protection against lethal influenza A virus in mice. Virol J 10:104. http://dx.doi.org/10.1186/1743-422X-10-104.
31. Anderson KG, Mayer-Barber K, Sung H, Beura L, James BR, Taylor JJ, Qunaj L, Griffith TS, Vezys V, Barber DL, Masopust D. 2014. Intravascular staining for discrimination of vascular and tissue leukocytes. Nature Protoc 9:209-222. http://dx.doi.org/10.1038/nprot.2014.005.
32. Choi JP, Kim YS, Tae YM, Choi EJ, Hong BS, Jeon SG, Gho YS, Zhu Z, Kim YK. 2010. A viral PAMP double-stranded RNA induces allergenspecific Th17 cell response in the airways which is dependent on VEGF and IL-6. Allergy 65:1322-1330. http://dx.doi.org/10.1111/j.1398-9995.2010.02369.x.
33. Ye L, Zeng R, Bai Y, Roopenian DC, Zhu X. 2011. Efficient mucosal vaccination mediated by the neonatal Fc receptor. Nat Biotechnol 29:158-163. http://dx.doi.org/10.1038/nbt.1742.
34. Woodland DL, Kohlmeier JE. 2009. Migration, maintenance and recall of memory T cells in peripheral tissues. Nat Rev Immunol 9:153-161. http://dx.doi.org/10.1038/nri2496.
35. Turner DL, Bickham KL, Thome JJ, Kim CY, D'Ovidio F, Wherry EJ, Farber DL. 2014. Lung niches for the generation and maintenance of tissue-resident memory T cells. Mucosal Immunol 7:501-510. http://dx.doi.org/10.1038/mi.2013.67.
36. Rutigliano JA, Sharma S, Morris MY, Oguin TH 3rd, McClaren JL, Doherty PC, Thomas PG. 2014. Highly pathological influenza A virus infection is associated with augmented expression of PD-1 by functionally compromised virus-specific CD8+ T cells. J Virol 88:1636-1651. http://dx.doi.org/10.1128/JVI.02851-13.
37. Brandes M, Klauschen F, Kuchen S, Germain RN. 2013. A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 154:197-212. http://dx.doi.org/10.1016/j.cell.2013.06.013.
38. La Gruta NL, Turner SJ. 2014. T cell mediated immunity to influenza: mechanisms of viral control. Trends Immunol 35:396-402. http://dx.doi.org/10.1016/j.it.2014.06.004.
39. Jaleco S, Swainson L, Dardalhon V, Burjanadze M, Kinet S, Taylor N. 2003. Homeostasis of naive and memory CD4+ T cells: IL-2 and IL-7 differentially regulate the balance between proliferation and Fas-mediated apoptosis. J Immunol 171:61-68. http://dx.doi.org/10.4049/jimmunol.171.1.61.
40. Geginat J, Lanzavecchia A, Sallusto F. 2003. Proliferation and differentiation potential of human CD8+ memory T-cell subsets in response to antigen or homeostatic cytokines. Blood 101:4260-4266. http://dx.doi.org/10.1182/blood-2002-11-3577.
41. Thomas PG, Keating R, Hulse-Post DJ, Doherty PC. 2006. Cellmediated protection in influenza infection. Emerg Infect Dis 12:48-54. http://dx.doi.org/10.3201/eid1201.051237.
42. Turner DL, Farber DL. 2014. Mucosal resident memory CD4 T cells in protection and immunopathology. Front Immunol 5:331. http://dx.doi.org/10.3389/fimmu.2014.00331.
43. McKinstry KK, Strutt TM, Kuang Y, Brown DM, Sell S, Dutton RW, Swain SL. 2012. Memory CD4+ T cells protect against influenza through multiple synergizing mechanisms. J Clin Invest 122:2847-2856. http://dx.doi.org/10.1172/JCI63689.
44. Teijaro JR, Verhoeven D, Page CA, Turner D, Farber DL. 2010. Memory CD4 T cells direct protective responses to influenza virus in the lungs through helper-independent mechanisms. J Virol 84:9217-9226. http://dx.doi.org/10.1128/JVI.01069-10.
45. Rice JC, Bucy RP. 1995. Differences in the degree of depletion, rate of recovery, and the preferential elimination of naive CD4+ T cells by anti-CD4 monoclonal antibody (GK1.5) in young and aged mice. J Immunol 154:6644-6654.
46. Czajkowsky DM, Hu J, Shao Z, Pleass RJ. 2012. Fc-fusion proteins: new developments and future perspectives. EMBO Mol Med 4:1015-1028. http://dx.doi.org/10.1002/emmm.201201379.
47. Dumont JA, Bitonti AJ, Clark D, Evans S, Pickford M, Newman SP. 2005. Delivery of an erythropoietin-Fc fusion protein by inhalation in humans through an immunoglobulin transport pathway. J Aerosol Med 18:294-303. http://dx.doi.org/10.1089/jam.2005.18.294.