Targeting the HA2 subunit of influenza A virus hemagglutinin via CD40L provides universal protection against diverse subtypes

Mucosal Immunology

Volumn 8, Issue 1, 2015, Pages 211-220

  Fan, X ^a,b   Hashem, A M ^c,d,e,f   Chen, Z ^g   Li, C ^a   Doyle, T ^c,f   Zhang, Y ^b   Yi, Y ^g   Farnsworth, A ^c   Xu, K ^a   Li, Z ^a   He, R ^h   Li, X ^c,f   Wang, J ^a  

^a NATIONAL INSTITUTES FOR FOOD AND DRUG CONTROL   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c Health Canada and World Health Organization Collaborating Center for Standardization and Evaluation of Biologicals   (Canada)

^d Aziz University   (Saudi Arabia)

^e KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^f UNIVERSITY OF OTTAWA   (Canada)

^g Shanghai Institute of Biological Products   (China)

^h PUBLIC HEALTH AGENCY OF CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CD40 LIGAND; GAMMA INTERFERON; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; INFLUENZA VIRUS HEMAGGLUTININ SUBUNIT HA2; INTERLEUKIN 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; H1N1 VIRUS HEMAGGLUTININ; HYBRID PROTEIN; NEUTRALIZING ANTIBODY; PROTEIN SUBUNIT;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CELLULAR IMMUNITY; CODON; CONTROLLED STUDY; FEMALE; IMMUNOGENICITY; IN VITRO STUDY; INFLUENZA A; INFLUENZA A CALIFORNIA 7 2009 H1N1 VIRUS; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H9N2; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; VIRUS NEUTRALIZATION; VIRUS RECOMBINANT; ADENOVIRIDAE; ANIMAL; ANTIGENIC VARIATION; BAGG ALBINO MOUSE; CHEMISTRY; DOG; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HUMAN; IMMUNIZATION; IMMUNOLOGY; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MDCK CELL LINE; METABOLISM; MOLECULARLY TARGETED THERAPY; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; SPECIES DIFFERENCE;

ADENOVIRIDAE; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIGENIC VARIATION; CD40 LIGAND; DOGS; FEMALE; HEK293 CELLS; HELA CELLS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNIZATION; INFLUENZA A VIRUS; INFLUENZA VACCINES; INFLUENZA, HUMAN; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICE, INBRED BALB C; MOLECULAR TARGETED THERAPY; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RECOMBINANT FUSION PROTEINS; SPECIES SPECIFICITY;

EID: 84921462503     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.59     Document Type: Article

References (51)

1. Gerhard, W., Mozdzanowska, K. & Zharikova, D. Prospects for universal influenza virus vaccine. Emerging Infect. Dis 12, 569-574 (2006)
2. Hashem, A. M. et al. Recent developments in bioinformatics analyses of influenza A virus surface glycoproteins and their biological relevance. Curr. Bioinform. 6, 415-426 (2011)
3. Subbarao, K. et al. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279, 393-396 (1998)
4. Lin, Y. P. et al. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc. Natl. Acad. Sci. USA 97, 9654-9658 (2000)
5. Fouchier, R. A. M. et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc. Natl. Acad. Sci. USA 101, 1356-1361 (2004)
6. Dai, C. & Jiang, M. Understanding H7N9 avian flu. B. M. J. 346, f2755 (2013)
7. Skehel, J. J. & Wiley, D. C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69, 531-569 (2000)
8. Gerhard,W., Yewdell, J., Frankel,M. E. & Webster, R. G. Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature 290, 713-717 (1981)
9. Wiley, D. C. & Skehel, J. J. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56, 365-394 (1987)
10. Chen, J. et al. A soluble domain of the membrane-anchoring chain of influenza virus hemagglutinin (HA2) folds in Escherichia coli into the low-pHinduced conformation. Proc. Natl. Acad. Sci. USA 92, 12205-12209 (1995)
11. Chun, S. et al. Universal antibodies and their applications to the quantitative determination of virtually all subtypes of the influenza A viral hemagglutinins. Vaccine 26, 6068-6076 (2008)
12. Hashem, A. M. et al. Universal antibodies against the highly conserved influenza fusion peptide cross-neutralize several subtypes of influenza A virus. Biochem. Biophy. Res. Commun 403, 247-251 (2010)
13. Throsby, M. et al. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM memory B cells. PLoS ONE 3, e3942 (2008)
14. Ekiert, D. C. et al. Antibody recognition of a highly conserved influenza virus epitope. Science 324, 246-251 (2009)
15. Sui, J. et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16, 265-273 (2009)
16. Corti, D. et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333, 850-856 (2011)
17. Ekiert, D. C. et al. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333, 843-850 (2011)
18. Bommakanti, G. et al. Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge. Proc. Natl. Acad. Sci. USA 107, 13701-13706 (2010)
19. Steel, J. et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio 1, e00018-10 (2010)
20. Wang, T. T. et al. Vaccination with a synthetic peptide from the influenza virus hemagglutinin provides protection against distinct viral subtypes. Proc. Natl. Acad. Sci. USA 107, 18979-18984 (2010)
21. van Kooten, C. & Banchereau, J. CD40-CD40 ligand. J. Leukoc. Biol. 67, 2-17 (2000)
22. Bishop, G. A. & Hostager, B. S. The CD40-CD154 interaction in B cell-Tcell liaisons. Cytokine Growth Factor Rev. 14, 297-309 (2003)
23. Quezada, S. A., Jarvinen, L. Z., Lind, E. F. & Noelle, R. J. CD40/CD154 interactions at the interface of tolerance and immunity. Annu. Rev. Immunol. 22, 307-328 (2004)
24. Oxenius, A. et al. CD40-CD40 ligand interactions are critical in T-B cooperation but not for other anti-viral CD4 Tcell functions. J. Exp. Med. 183, 2209-2218 (1996)
25. Schultze, J. L. et al. CD40-activated human B cells: an alternative source of highly efficient antigen presenting cells to generate autologous antigen-specific T cells for adoptive immunotherapy. J. Clin. Invest. 100, 2757-2765 (1997)
26. Bennett, S. R., Carbone, F. R., Karamalis, F., Flavell, R. A., Miller, J. F. & Heath, W. R. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393, 478-480 (1998)
27. Schoenberger, S. P., Toes, R. E., van der Voort, E. I., Offringa, R. & Melief, C. J. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393, 480-483 (1998)
28. Bergwelt-Baildon von, M. et al. CD40-stimulated B lymphocytes pulsed with tumor antigens are effective antigen-presenting cells that can generate specific T cells. Cancer Res 2003;63:2836-43
29. Cancer Res 64, 4055-4056. author reply 4056-7 (2004)
30. Tripp, R. A., Jones, L., Anderson, L. J. & Brown, M. P. CD40 ligand (CD154) enhances the Th1 and antibody responses to respiratory syncytial virus in the Balb/c mouse. J. Immunol. 164, 5913-5921 (2000)
31. Pereboev, A. V. et al. Enhanced gene transfer to mouse dendritic cells using adenoviral vectors coated with a novel adapter molecule. Mol. Ther. 9, 712-720 (2004)
32. Zheng, M. et al. CD4 T cell-independent DNA vaccination against opportunistic infections. J. Clin. Invest. 115, 3536-3544 (2005)
33. Huang, D. et al. Significant alterations of biodistribution and immune responses in Balb/c mice administered with adenovirus targeted to CD40() cells. Gene Ther 15, 298-308 (2008)
34. Liu, J. et al. CD40L expressed from the canarypox vector, ALVAC, can boost immunogenicity of HIV-1 canarypox vaccine in mice and enhance the in vitro expansion of viral specific CD8 Tcell memory responses from HIV-1-infected and HIV-1-uninfected individuals. Vaccine 26, 4062-4072 (2008)
35. Gómez, C. E., Nájera, J. L., Sánchez, R., Jiménez, V. & Esteban, M. Multimeric soluble CD40 ligand (sCD40L) efficiently enhances HIV specific cellular immune responses during DNA prime and boost with attenuated poxvirus vectors MVA and NYVAC expressing HIV antigens. Vaccine 27, 3165-3174 (2009)
36. Lin, F. C., Peng, Y., Jones, L. A., Verardi, P. H. & Yilma, T. D. Incorporation of CD40 ligand into the envelope of pseudotyped single-cycle simian immunodeficiency viruses enhances immunogenicity. J. Virol. 83, 1216-1227 (2009)
37. Cao, J.,Wang, X., Du,Y., Li,Y.,Wang, X. &Jiang,P. CD40 ligand expressed in adenovirus can improve the immunogenicity of the GP3 and GP5 of porcine reproductive and respiratory syndrome virus in swine. Vaccine 28, 7514-7522 (2010)
38. Hangalapura, B. N. et al. Selective transduction of dendritic cells in human lymph nodes and superior induction of high-avidity melanoma-reactive cytotoxic T cells by a CD40-targeted adenovirus. J. Immunother. 33, 706-715 (2010)
39. Kim, Y.-S. et al. CD40-targeted recombinant adenovirus significantly enhances the efficacy of antitumor vaccines based on dendritic cells and B cells. Hum. Gene Ther. 21, 1697-1706 (2010)
40. Franco, D., Liu, W., Gardiner, D. F., Hahn, B. H. & Ho, D. D. CD40Lcontaining virus-like particle as a candidate HIV-1 vaccine targeting dendritic cells. J. Acquir. Immune Defic. Syndr. 56, 393-400 (2011)
41. Yao, Q. et al. Immunogenicity and protective efficacy of a DNA vaccine encoding a chimeric protein of avian influenza hemagglutinin subtype H5 fused to CD154 (CD40L) in Pekin ducks. Vaccine 28, 8147-8156 (2010)
42. Sánchez Ramos, O. et al. Avian CD154 enhances humoral and cellular immune responses induced by an adenovirus vector-based vaccine in chickens. Comp. Immunol. Microbiol. Infect. Dis. 34, 259-265 (2011)
43. Epstein, S. L. Prior H1N1 influenza infection and susceptibility of Cleveland Family Study participants during the H2N2 pandemic of 1957: an experiment of nature. J. Infect. Dis. 193, 49-53 (2006)
44. Gerhard, W. The role of the antibody response in influenza virus infection. Curr. Top. Microbiol. Immunol. 260, 171-190 (2001)
45. Stanekova, Z. et al. Epitope specificity of anti-HA2 antibodies induced in humans during influenza infection. Influenza Resp. Vir 6, 389-395 (2012)
46. Varec ková, E. et al. HA2 glycopolypeptide of influenza A virus and antiviral immunity. Acta Virol 57, 247 V 256 (2013)
47. Carragher, D. M., Kaminski, D. A., Moquin, A., Hartson, L. & Randall, T. D. A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to influenza virus. J. Immunol. 181, 4168-4176 (2008)
48. Flaman, A. S., Gravel, C., Hashem, A. M., Tocchi, M. & Li, X. The effect of interferon-a on the expression of cytochrome P450 3A4 in human hepatoma cells. Toxicol. Appl. Pharmacol. 253, 130-136 (2011)
49. Reed, J. & Muench, H. A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 27, 493-497 (1938)
50. Hauser, H., Shen, L., Gu, Q.-L., Krueger, S. & Chen, S.-Y. Secretory heatshock protein as a dendritic cell-targeting molecule: a new strategy to enhance the potency of genetic vaccines. Gene Ther 11, 924-932 (2004)
51. Hashem, A. M. et al. Subcutaneous immunization with recombinant adenovirus expressing influenza A nucleoprotein protects mice against lethal viral challenge. Hum. Vaccin. Immunother 8, 425-430 (2012).