TLR7 and 9 agonists are highly effective mucosal adjuvants for norovirus virus-like particle vaccines

Human Vaccines and Immunotherapeutics

Volumn 10, Issue 2, 2014, Pages 410-416

  Hjelm, Brooke E ^a,b   Kilbourne, Jacquelyn ^a   Herbst Kralovetz, Melissa M ^c  

^a Arizona State University   (United States)

^b TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Antibody production; Mucosal adjuvants; Mucosal immunology; Nasal vaccination; Norovirus; Oral vaccination; TLR agonists; Virus like particles

Indexed keywords

CL 097; CPG OLIGODEOXYNUCLEOTIDE; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOLOGICAL ADJUVANT; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 8; UNCLASSIFIED DRUG; VIRUS LIKE PARTICLE VACCINE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MEMBRANE PROTEIN; TLR7 PROTEIN, MOUSE; TLR9 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; VIRUS ANTIBODY;

ADJUVANT THERAPY; ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; DRUG EFFECT; DRUG POTENCY; FEMALE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOMODULATION; MOUSE; NONHUMAN; NOROVIRUS; VIRUS PARTICLE; AGONISTS; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CALICIVIRIDAE INFECTIONS; CHEMISTRY; FECES; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; MUCOSAL ADMINISTRATION; MUCOSAL IMMUNITY; ORAL DRUG ADMINISTRATION; VAGINA;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ADMINISTRATION, MUCOSAL; ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES, VIRAL; CALICIVIRIDAE INFECTIONS; FECES; FEMALE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MEMBRANE GLYCOPROTEINS; MICE, INBRED BALB C; NORWALK VIRUS; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 9; VACCINES, VIRUS-LIKE PARTICLE; VAGINA;

EID: 84896903153     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.27147     Document Type: Article

References (33)

1. Atmar RL, Bernstein DI, Harro CD, Al-Ibrahim MS, Chen WH, Ferreira J, Estes MK, Graham DY, Opekun AR, Richardson C, et al. Norovirus vaccine against experimental human Norwalk Virus illness. N Engl J Med 2011; 365:2178-87; PMID:22150036; http://dx.doi.org/10.1056/NEJMoa1101245
2. Deschuyteneer M, Elouahabi A, Plainchamp D, Plisnier M, Soete D, Corazza Y, Lockman L, Giannini S, Deschamps M. Molecular and structural characterization of the L1 virus-like particles that are used as vaccine antigens in Cervarix, the AS04-adjuvanted HPV-16 and -18 cervical cancer vaccine. Hum Vaccin 2010; 6:407-19; PMID:20953154; http://dx.doi.org/10.4161/hv.6.5.11023
3. El-Kamary SS, Pasetti MF, Mendelman PM, Frey SE, Bernstein DI, Treanor JJ, Ferreira J, Chen WH, Sublett R, Richardson C, et al. Adjuvanted intranasal Norwalk virus-like particle vaccine elicits antibodies and antibody-secreting cells that express homing receptors for mucosal and peripheral lymphoid tissues. J Infect Dis 2010; 202:1649-58; PMID:20979455; http://dx.doi.org/10.1086/657087
4. Giannini SL, Hanon E, Moris P, Van Mechelen M, Morel S, Dessy F, Fourneau MA, Colau B, Suzich J, Losonksy G, et al. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine 2006; 24:5937-49; PMID:16828940; http://dx.doi.org/10.1016/j.vaccine.2006.06.005 (Pubitemid 44080367)
5. Herbst-Kralovetz M, Mason HS, Chen Q. Norwalk virus-like particles as vaccines. Expert Rev Vaccines 2010; 9:299-307; PMID:20218858; http://dx.doi. org/10.1586/erv.09.163
6. Landry N, Ward BJ, Trépanier S, Montomoli E, Dargis M, Lapini G, Vézina LP. Preclinical and clinical development of plant-made virus-like particle vaccine against avian H5N1 influenza. PLoS One 2010; 5:e15559; PMID:21203523; http://dx.doi. org/10.1371/journal.pone.0015559
7. López-Macías C. Virus-like particle (VLP)-based vaccines for pandemic influenza: performance of a VLP vaccine during the 2009 influenza pandemic. Hum Vaccin Immunother 2012; 8:411-4; PMID:22330956; http://dx.doi.org/10.4161/ hv.18757
8. Ludwig C, Wagner R. Virus-like particles-universal molecular toolboxes. Curr Opin Biotechnol 2007; 18:537-45; PMID:18083549; http://dx.doi. org/10.1016/j.copbio.2007.10.013
9. Paavonen J, Jenkins D, Bosch FX, Naud P, Salmerón J, Wheeler CM, Chow SN, Apter DL, Kitchener HC, Castellsague X, et al.; HPV PATRICIA study group. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III doubleblind, randomised controlled trial. Lancet 2007; 369:2161-70; PMID:17602732; http://dx.doi. org/10.1016/S0140-6736(07)60946-5 (Pubitemid 46977438)
10. Roy P, Noad R. Virus-like particles as a vaccine delivery system: myths and facts. Hum Vaccin 2008; 4:5-12; PMID:18438104; http://dx.doi.org/10.4161/ hv.4.1.5559 (Pubitemid 351785255)
11. Tacket CO, Sztein MB, Losonsky GA, Wasserman SS, Estes MK. Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin Immunol 2003; 108:241-7; PMID:14499247; http://dx.doi.org/10. 1016/ S1521-6616(03)00120-7 (Pubitemid 37117370)
12. Wheeler CM, Bautista OM, Tomassini JE, Nelson M, Sattler CA, Barr E; Protocol 11 study Investigators. Safety and immunogenicity of co-administered quadrivalent human papillomavirus (HPV)-6/11/16/18 L1 virus-like particle (VLP) and hepatitis B (HBV) vaccines. Vaccine 2008; 26:686-96; PMID:18164106; http://dx.doi.org/10.1016/j. vaccine.2007.11.043
13. Jackson EM, Herbst-Kralovetz MM. Intranasal vaccination with murabutide enhances humoral and mucosal immune responses to a virus-like particle vaccine. PLoS One 2012; 7:e41529; PMID:22855691; http://dx.doi.org/10.1371/journal.pone. 0041529
14. Velasquez LS, Hjelm BE, Arntzen CJ, Herbst-Kralovetz MM. An intranasally delivered Toll-like receptor 7 agonist elicits robust systemic and mucosal responses to Norwalk virus-like particles. Clin Vaccine Immunol 2010; 17:1850-8; PMID:20962211; http:// dx.doi.org/10.1128/CVI.00230-10
15. Harandi AM, Davies G, Olesen OF. Vaccine adjuvants: scientific challenges and strategic initiatives. Expert Rev Vaccines 2009; 8:293-8; PMID:19249971; http://dx.doi.org/10.1586/14760584.8.3.293
16. Kanzler H, Barrat FJ, Hessel EM, Coffman RL. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat Med 2007; 13:552-9; PMID:17479101; http://dx.doi. org/10.1038/nm1589 (Pubitemid 46830615)
17. Knuschke T, Epple M, Westendorf AM. The type of adjuvant strongly influences the T-cell response during nanoparticle-based immunization. Hum Vaccin Immunother 2013; 10:10; PMID:23982325
18. Phoolcharoen W, Dye JM, Kilbourne J, Piensook K, Pratt WD, Arntzen CJ, Chen Q, Mason HS, Herbst-Kralovetz MM. A nonreplicating subunit vaccine protects mice against lethal Ebola virus challenge. Proc Natl Acad Sci U S A 2011; 108:20695-700; PMID:22143779; http://dx.doi.org/10.1073/ pnas.1117715108
19. Rhee JH, Lee SE, Kim SY. Mucosal vaccine adjuvants update. Clin Exp Vaccine Res 2012; 1:50-63; PMID:23596577; http://dx.doi.org/10.7774/ cevr.2012.1.1.50
20. Holmgren J, Czerkinsky C. Mucosal immunity and vaccines. Nat Med 2005; 11(Suppl):S45-53; PMID:15812489; http://dx.doi.org/10.1038/ nm1213 (Pubitemid 40562303)
21. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004; 4:499-511; PMID:15229469; http://dx.doi.org/10.1038/nri1391 (Pubitemid 38931765)
22. Beutler BA. TLRs and innate immunity. Blood 2009; 113:1399-407; PMID:18757776; http://dx.doi. org/10.1182/blood-2008-07-019307
23. Chilton PM, Embry CA, Mitchell TC. Effects of Differences in Lipid A Structure on TLR4 Pro-Inflammatory Signaling and Inflammasome Activation. Front Immunol 2012; 3:154; PMID:22707952; http://dx.doi.org/10.3389/ fimmu.2012.00154
24. Pulendran B, Ahmed R. Translating innate immunity into immunological memory: implications for vaccine development. Cell 2006; 124:849-63; PMID:16497593; http://dx.doi.org/10.1016/j. cell.2006.02.019 (Pubitemid 43261457)
25. Ball JM, Hardy ME, Atmar RL, Conner ME, Estes MK. Oral immunization with recombinant Norwalk virus-like particles induces a systemic and mucosal immune response in mice. J Virol 1998; 72:1345-53; PMID:9445035 (Pubitemid 28116920)
26. Santi L, Batchelor L, Huang Z, Hjelm B, Kilbourne J, Arntzen CJ, Chen Q, Mason HS. An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles. Vaccine 2008; 26:1846-54; PMID:18325641; http://dx.doi. org/10.1016/j.vaccine.2008.01.053
27. Velasquez LS, Shira S, Berta AN, Kilbourne J, Medi BM, Tizard I, Ni Y, Arntzen CJ, Herbst-Kralovetz MM. Intranasal delivery of Norwalk virus-like particles formulated in an in situ gelling, dry powder vaccine. Vaccine 2011; 29:5221-31; PMID:21640778; http://dx.doi.org/10.1016/j.vaccine.2011.05.027
28. Mutsch M, Zhou W, Rhodes P, Bopp M, Chen RT, Linder T, Spyr C, Steffen R. Use of the inactivated intranasal influenza vaccine and the risk of Bell's palsy in Switzerland. N Engl J Med 2004; 350:896-903; PMID:14985487; http://dx.doi.org/10.1056/ NEJMoa030595 (Pubitemid 38252537)
29. Pedersen GK, Cox RJ. The mucosal vaccine quandary: intranasal vs. sublingual immunization against influenza. Hum Vaccin Immunother 2012; 8:689-93; PMID:22495121; http://dx.doi.org/10.4161/ hv.19568
30. van Ginkel FW, Jackson RJ, Yuki Y, McGhee JR. Cutting edge: the mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. J Immunol 2000; 165:4778-82; PMID:11045998
31. Reeck A, Kavanagh O, Estes MK, Opekun AR, Gilger MA, Graham DY, Atmar RL. Serological correlate of protection against norovirus-induced gastroenteritis. J Infect Dis 2010; 202:1212-8; PMID:20815703; http://dx.doi.org/10.1086/656364
32. Harrington PR, Lindesmith L, Yount B, Moe CL, Baric RS. Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J Virol 2002; 76:12335-43; PMID:12414974; http://dx.doi. org/10.1128/JVI.76.23. 12335-12343.2002 (Pubitemid 35304332)
33. Cong Y, Jupelli M, Guentzel MN, Zhong G, Murthy AK, Arulanandam BP. Intranasal immunization with chlamydial protease-like activity factor and CpG deoxynucleotides enhances protective immunity against genital Chlamydia muridarum infection. Vaccine 2007; 25:3773-80; PMID:17349723; http:// dx.doi.org/10.1016/j.vaccine.2007.02.010 (Pubitemid 46589760)