Use of the microparticle nanoscale silicon dioxide as an adjuvant to boost vaccine immune responses against influenza virus in neonatal mice

Journal of Virology

Volumn 90, Issue 9, 2016, Pages 4735-4744

  Russell, Ryan F ^a   McDonald, Jacqueline U ^a   Lambert, Laura ^a   Tregoning, John S ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM PYROPHOSPHATE; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; INFLAMMASOME; INFLUENZA VACCINE; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MURAMYL TRIPEPTIDE; SILICA NANOPARTICLE; AUTACOID; BIOLOGICAL MARKER; CYTOKINE; IMMUNOLOGICAL ADJUVANT; NANOPARTICLE; SILICON DIOXIDE; VIRUS ANTIBODY; VIRUS ANTIGEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME ACTIVATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A (H1N1); INFLUENZA A VIRUS (A/ENGLAND/195/2009(H1N1)); INFLUENZA A VIRUS (H1N1); INNATE IMMUNITY; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; VACCINATION; ANIMAL; CELL LINE; DISEASE MODEL; HUMAN; IMMUNIZATION; IMMUNOLOGY; MACROPHAGE; METABOLISM; ORTHOMYXOVIRIDAE INFECTIONS;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; BIOMARKERS; CELL LINE; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNIZATION; INFLAMMASOMES; INFLAMMATION MEDIATORS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; MACROPHAGES; MICE; NANOPARTICLES; ORTHOMYXOVIRIDAE INFECTIONS; SILICON DIOXIDE;

EID: 84964988242     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03159-15     Document Type: Article

References (41)

1. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Barker-Collo S, Bartels DH, Bell ML, Benjamin EJ, Bennett D, Bhalla K, Bikbov B, Bin Abdulhak A, Birbeck G, Blyth F, Bolliger I, Boufous S, Bucello C, Burch M, Burney P, Carapetis J, Chen H, Chou D, Chugh SS, Coffeng LE, Colan SD, Colquhoun S, Colson KE, Condon J, Connor MD, Cooper LT, Corriere M, Cortinovis M, de Vaccaro KC, Couser W, Cowie BC, Criqui MH, Cross M, et al. 2012. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2095-2128. http://dx.doi.org/10.1016/S0140-6736(12)61728-0.
2. Tregoning JS, Schwarze J. 2010. Respiratory viral infections in infants: causes, clinical symptoms, virology, and immunology. Clin Microbiol Rev 23:74-98. http://dx.doi.org/10.1128/CMR.00032-09.
3. Wood N, Siegrist CA. 2011. Neonatal immunization: where do we stand? Curr Opin Infect Dis 24:190-195. http://dx.doi.org/10.1097/QCO.0b013e328345d563.
4. de Brito CA, Goldoni AL, Sato MN. 2009. Immune adjuvants in early life: targeting the innateimmunesystem to overcome impaired adaptive response. Immunotherapy 1:883-895. http://dx.doi.org/10.2217/imt.09.38.
5. Rappuoli R, Mandl CW, Black S, De Gregorio E. 2011. Vaccines for the twenty-first century society. Nat Rev Immunol 11:865-872.
6. Arias MA, Van Roey GA, Tregoning JS, Moutaftsi M, Coler RN, Windish HP, Reed SG, Carter D, Shattock RJ. 2012. Glucopyranosyl lipid adjuvant (GLA), a synthetic TLR4 agonist, promotes potent systemic and mucosal responses to intranasal immunization with HIVgp140. PLoS One 7:e41144. http://dx.doi.org/10.1371/journal.pone.0041144.
7. Sadeghi K, Berger A, Langgartner M, Prusa AR, Hayde M, Herkner K, Pollak A, Spittler A, Forster-Waldl E. 2007. Immaturity of infection control in preterm and term newborns is associated with impaired tolllike receptor signaling. J Infect Dis 195:296-302. http://dx.doi.org/10.1086/509892.
8. Burl S, Townend J, Njie-Jobe J, Cox M, Adetifa UJ, Touray E, Philbin VJ, Mancuso C, Kampmann B, Whittle H, Jaye A, Flanagan KL, Levy O. 2011. Age-dependent maturation of Toll-like receptor-mediated cytokine responses in Gambian infants. PLoS One 6:e18185. http://dx.doi.org/10.1371/journal.pone.0018185.
9. Levy O, Zarember KA, Roy RM, Cywes C, Godowski PJ, Wessels MR. 2004. Selective impairment of TLR-mediated innate immunity in human newborns: neonatal blood plasma reduces monocyte TNF-alpha induction by bacterial lipopeptides, lipopolysaccharide, and imiquimod, but preserves the response to R-848. J Immunol 173:4627-4634. http://dx.doi.org/10.4049/jimmunol.173.7.4627.
10. H1 potency of neonatal dendritic cells. J Allergy Clin Immunol 136:1355-1368. http://dx.doi.org/10.1016/j.jaci.2015.02.030.
11. Schroder K, Tschopp J. 2010. The inflammasomes. Cell 140:821-832. http://dx.doi.org/10.1016/j.cell.2010.01.040.
12. Oleszycka E, Moran HB, Tynan GA, Hearnden CH, Coutts G, Campbell M, Allan SM, Scott CJ, Lavelle EC. 2015. IL-1alpha and inflammasome-independent IL-1beta promote neutrophil infiltration following alum vaccination. FEBS J 283:9-24. http://dx.doi.org/10.1111/febs.13546.
13. Nakae S, Asano M, Horai R, Iwakura Y. 2001. Interleukin-1α, but not interleukin-1α, is required for T-cell-dependent antibody production. Immunology 104:402-409. http://dx.doi.org/10.1046/j.1365-2567.2001.01337.x.
14. Staats HF, Ennis FA. 1999. IL-1 is an effective adjuvant for mucosal and systemic immune responses when coadministered with protein immunogens. J Immunol 162:6141-6147.
15. Fadeel B. 2012. Clear and present danger? Engineered nanoparticles and the immune system. Swiss Med Wkly 142:w13609.
16. Baron L, Gombault A, Fanny M, Villeret B, Savigny F, Guillou N, Panek C, Le Bert M, Lagente V, Rassendren F, Riteau N, Couillin I. 2015. The NLRP3 inflammasome is activated by nanoparticles through ATP, ADP and adenosine. Cell Death Dis 6:e1629. http://dx.doi.org/10.1038/cddis.2014.576.
17. Rosenthal AK. 2011. Crystals, inflammation, and osteoarthritis. Curr Opin Rheumatol 23:170-173. http://dx.doi.org/10.1097/BOR.0b013e3283432d1f.
18. Mulla MJ, Myrtolli K, Potter J, Boeras C, Kavathas PB, Sfakianaki AK, Tadesse S, Norwitz ER, Guller S, Abrahams VM. 2011. Uric acid induces trophoblast IL-1beta production via the inflammasome: implications for the pathogenesis of preeclampsia. Am J Reprod Immunol 65:542-548. http://dx.doi.org/10.1111/j.1600-0897.2010.00960.x.
19. Li H, Nookala S, Re F. 2007. Aluminum hydroxide adjuvants activate caspase-1 and induce IL-1beta and IL-18 release. J Immunol 178:5271-5276. http://dx.doi.org/10.4049/jimmunol.178.8.5271.
20. Wischke C, Mathew S, Roch T, Frentsch M, Lendlein A. 2012. Potential of NOD receptor ligands as immunomodulators in particulate vaccine carriers. J Control Release 164:299-306. http://dx.doi.org/10.1016/j.jconrel.2012.06.034.
21. Park EK, Jung HS, Yang HI, Yoo MC, Kim C, Kim KS. 2007. Optimized THP-1 differentiation is required for the detection of responses to weak stimuli. Inflamm Res 56:45-50. http://dx.doi.org/10.1007/s00011-007-6115-5.
22. Baillie GJ, Galiano M, Agapow PM, Myers R, Chiam R, Gall A, Palser AL, Watson SJ, Hedge J, Underwood A, Platt S, McLean E, Pebody RG, Rambaut A, Green J, Daniels R, Pybus OG, Kellam P, Zambon M. 2012. Evolutionary dynamics of local pandemic H1N1/2009 influenza virus lineages revealed by whole-genome analysis. J Virol 86:11-18. http://dx.doi.org/10.1128/JVI.05347-11.
23. Elleman CJ, Barclay WS. 2004. The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology 321:144-153. http://dx.doi.org/10.1016/j.virol.2003.12.009.
24. Siggins MK, Gill SK, Langford PR, Li Y, Ladhani SN, Tregoning JS. 26 July 2015. PHiD-CV induces anti-protein D antibodies but does not augment pulmonary clearance of nontypeable Haemophilus influenzae in mice. Vaccine http://dx.doi.org/10.1016/j.vaccine.2015.07.034.
25. Calabro S, Tortoli M, Baudner BC, Pacitto A, Cortese M, O'Hagan DT, De Gregorio E, Seubert A, Wack A. 2011. Vaccine adjuvants alum and MF59 induce rapid recruitment of neutrophils and monocytes that participate in antigen transport to draining lymph nodes. Vaccine 29:1812-1823. http://dx.doi.org/10.1016/j.vaccine.2010.12.090.
26. Awate S, Babiuk LA, Mutwiri G. 2013. Mechanisms of action of adjuvants. Front Immunol 4:114. http://dx.doi.org/10.3389/fimmu.2013.00114.
27. Seubert A, Calabro S, Santini L, Galli B, Genovese A, Valentini S, Aprea S, Colaprico A, D'Oro U, Giuliani MM, Pallaoro M, Pizza M, O'Hagan DT, Wack A, Rappuoli R, De Gregorio E. 2011. Adjuvanticity of the oil-in-water emulsion MF59 is independent of Nlrp3 inflammasome but requires the adaptor protein MyD88. Proc Natl Acad SciUSA108:11169-11174 http://dx.doi.org/10.1073/pnas.1107941108.
28. Cheng C, Jain P, Bettahi I, Pal S, Tifrea D, de la Maza LM. 2011. A TLR2 agonist is a more effective adjuvant for a Chlamydia major outer membrane protein vaccine than ligands to other TLR and NOD receptors. Vaccine 29:6641-6649. http://dx.doi.org/10.1016/j.vaccine.2011.06.105.
29. Fu C, Liu T, Li L, Liu H, Chen D, Tang F. 2013. The absorption, distribution, excretion and toxicity of mesoporous silica nanoparticles in mice following different exposure routes. Biomaterials 34:2565-2575. http://dx.doi.org/10.1016/j.biomaterials.2012.12.043.
30. Mastelic Gavillet B, Eberhardt CS, Auderset F, Castellino F, Seubert A, Tregoning JS, Lambert PH, de Gregorio E, Del Giudice G, Siegrist CA. 2015. MF59 mediates its B cell adjuvanticity by promoting T follicular helper cells and thus germinal center responses in adult and early life. J Immunol 194:4836-4845. http://dx.doi.org/10.4049/jimmunol.1402071.
31. Honda-Okubo Y, Kolpe A, Li L, Petrovsky N. 2014. A single immunization with inactivated H1N1 influenza vaccine formulated with delta inulin adjuvant (Advax) overcomes pregnancy-associated immune suppression and enhances passive neonatal protection. Vaccine 32:4651-4659. http://dx.doi.org/10.1016/j.vaccine.2014.06.057.
32. Khalil SM, Tonkin DR, Snead AT, Parks GD, Johnston RE, White LJ. 2014. An alphavirus-based adjuvant enhances serum and mucosal antibodies, T cells, and protective immunity to influenza virus in neonatal mice. J Virol 88:9182-9196. http://dx.doi.org/10.1128/JVI.00327-14.
33. Sharma AA, Jen R, Kan B, Sharma A, Marchant E, Tang A, Gadawski I, Senger C, Skoll A, Turvey SE, Sly LM, Cote HC, Lavoie PM. 2015. Impaired NLRP3 inflammasome activity during fetal development regulates IL-1beta production in human monocytes. Eur J Immunol 45:238-249. http://dx.doi.org/10.1002/eji.201444707.
34. Philbin VJ, Dowling DJ, Gallington LC, Cortes G, Tan Z, Suter EE, Chi KW, Shuckett A, Stoler-Barak L, Tomai M, Miller RL, Mansfield K, Levy O. 2012. Imidazoquinoline Toll-like receptor 8 agonists activate human newborn monocytes and dendritic cells through adenosinerefractory and caspase-1-dependent pathways. J Allergy Clin Immunol 130:195-204.e199. http://dx.doi.org/10.1016/j.jaci.2012.02.042.
35. Russell RF, McDonald JU, Ivanova M, Zhong Z, Bukreyev A, Tregoning JS. 2015. Partial attenuation of respiratory syncytial virus with a deletion of a small hydrophobic gene is associated with elevated interleukin-1beta responses. J Virol 89:8974-8981. http://dx.doi.org/10.1128/JVI.01070-15.
36. Suzuki H, Sozen T, Hasegawa Y, Chen W, Zhang JH. 2009. Caspase-1 inhibitor prevents neurogenic pulmonary edema after subarachnoid hemorrhage in mice. Stroke 40:3872-3875. http://dx.doi.org/10.1161/STROKEAHA.109.566109.
37. Duan J, Yu Y, Yu Y, Li Y, Wang J, Geng W, Jiang L, Li Q, Zhou X, Sun Z. 2014. Silica nanoparticles induce autophagy and endothelial dysfunction via the PI3K/Akt/mTOR signaling pathway. Int J Nanomedicine 9:5131-5141. http://dx.doi.org/10.2147/IJN.S71074.
38. Lewis DJ, Lythgoe MP. 2015. Application of "systems vaccinology" to evaluate inflammation and reactogenicity of adjuvanted preventative vaccines. J Immunol Res 2015:909406.
39. Partinen M, Saarenpaa-Heikkila O, Ilveskoski I, Hublin C, Linna M, Olsen P, Nokelainen P, Alen R, Wallden T, Espo M, Rusanen H, Olme J, Satila H, Arikka H, Kaipainen P, Julkunen I, Kirjavainen T. 2012. Increased incidence and clinical picture of childhood narcolepsy following the 2009 H1N1 pandemic vaccination campaign in Finland. PLoS One 7:e33723. http://dx.doi.org/10.1371/journal.pone.0033723.
40. Armstrong PK, Dowse GK, Effler PV, Carcione D, Blyth CC, Richmond PC, Geelhoed GC, Mascaro F, Scully M, Weeramanthri TS. 2011. Epidemiological study of severe febrile reactions in young children in Western Australia caused by a 2010 trivalent inactivated influenza vaccine. BMJ Open 1:e000016.
41. Leeb A, Carcione D, Richmond PC, Jacoby P, Effler PV. 2011. Reactogenicity of two 2010 trivalent inactivated influenza vaccine formulations in adults. Vaccine 29:7920-7924. http://dx.doi.org/10.1016/j.vaccine.2011.08.073.