Toll-like receptor 8 agonist nanoparticles mimic immunomodulating effects of the live BCG vaccine and enhance neonatal innate and adaptive immune responses

Journal of Allergy and Clinical Immunology

Volumn 140, Issue 5, 2017, Pages 1339-1350

  Dowling, David J ^a,b   Scott, Evan A ^c   Scheid, Annette ^a,b,d,i   Bergelson, Ilana ^a   Joshi, Sweta ^a   Pietrasanta, Carlo ^a,b,e   Brightman, Spencer ^a   Sanchez Schmitz, Guzman ^a,b   Van Haren, Simon D ^a,b   Ninković, Jana ^a,b   Kats, Dina ^c   Guiducci, Cristiana ^f   de Titta, Alexandre ^g   Bonner, Daniel K ^g   Hirosue, Sachiko ^g   Swartz, Melody A ^g,h   Hubbell, Jeffrey A ^g,h   Levy, Ofer ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Northwestern University   (United States)

^d TUFTS MEDICAL CENTER   (United States)

^e UNIVERSITY OF MILAN   (Italy)

^f Dynavax Technologies Corporation   (United States)

^g EPFL   (Switzerland)

^h UNIVERSITY OF CHICAGO   (United States)

ⁱ BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

BCG; dendritic cells; nanoparticle; Newborn; polymersome; Toll like receptor 8; vaccine

Indexed keywords

ALUMINUM PHOSPHATE; AMPHOPHILE; BCG VACCINE; CD4 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; COPOLYMER; DIPHTHERIA TOXOID CRM197; HERMES ANTIGEN; IMIDAZOQUINOLINE DERIVATIVE; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NANOCARRIER; NANOPARTICLE; PNEUMOCOCCUS VACCINE; PROSTAGLANDIN E2; RECOMBINANT HEPATITIS B VACCINE; TOLL LIKE RECEPTOR 8 AGONIST; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CYTOKINE; IMIDAZOLE DERIVATIVE; POLYMER; QUINOLINE; QUINOLINE DERIVATIVE; TLR8 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 8;

ADAPTIVE IMMUNITY; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; CD4+ T LYMPHOCYTE; CELL DEATH; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG FORMULATION; DRUG RELEASE; HELPER CELL; HUMAN; HUMAN CELL; IMMUNIZATION; IMMUNOGENICITY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MALE; MONOCYTE; MOUSE; NANOENCAPSULATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; AGONISTS; ANIMAL; BIOMIMETICS; C57BL MOUSE; CELL CULTURE; CHEMISTRY; COMPARATIVE STUDY; IMMUNOLOGY; METABOLISM; SCID MOUSE; VACCINATION;

ADAPTIVE IMMUNITY; ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANIMALS, NEWBORN; BCG VACCINE; BIOMIMETICS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; HUMANS; IMIDAZOLES; IMMUNITY, INNATE; IMMUNOMODULATION; INFANT, NEWBORN; MICE; MICE, INBRED C57BL; MICE, SCID; MONOCYTES; NANOPARTICLES; POLYMERS; QUINOLINES; TOLL-LIKE RECEPTOR 8; VACCINATION;

EID: 85016072384     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.12.985     Document Type: Article

References (49)

1. PrabhuDas, M., Adkins, B., Gans, H., King, C., Levy, O., Ramilo, O., et al. Challenges in infant immunity: implications for responses to infection and vaccines. Nat Immunol 12 (2011), 189–194.
2. Dowling, D.J., Levy, O., Ontogeny of early life immunity. Trends Immunol 35 (2014), 299–310.
3. Kollmann, T.R., Levy, O., Montgomery, R.R., Goriely, S., Innate immune function by Toll-like receptors: distinct responses in newborns and the elderly. Immunity 37 (2012), 771–783.
4. Levy, O., Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat Rev Immunol 7 (2007), 379–390.
5. Adkins, B., Leclerc, C., Marshall-Clarke, S., Neonatal adaptive immunity comes of age. Nat Rev Immunol 4 (2004), 553–564.
6. Sanchez-Schmitz, G., Levy, O., Development of newborn and infant vaccines. Sci Transl Med, 3, 2011, 90ps27.
7. Levy, O., Goriely, S., Kollmann, T.R., Immune response to vaccine adjuvants during the first year of life. Vaccine 31 (2013), 2500–2505.
8. van den Biggelaar, A.H., Pomat, W.S., Immunization of newborns with bacterial conjugate vaccines. Vaccine 31 (2013), 2525–2530.
9. Dowling, D., Hamilton, C.M., O'Neill, S.M., A comparative analysis of cytokine responses, cell surface marker expression and MAPKs in DCs matured with LPS compared with a panel of TLR ligands. Cytokine 41 (2008), 254–262.
10. Coffman, R.L., Sher, A., Seder, R.A., Vaccine adjuvants: putting innate immunity to work. Immunity 33 (2010), 492–503.
11. Dowling, D.J., Levy, O., Pediatric vaccine adjuvants: components of the modern vaccinologist's toolbox. Pediatr Infect Dis J 34 (2015), 1395–1398.
12. Tanji, H., Ohto, U., Shibata, T., Miyake, K., Shimizu, T., Structural reorganization of the Toll-like receptor 8 dimer induced by agonistic ligands. Science 339 (2013), 1426–1429.
13. Philbin, V.J., Dowling, D.J., Gallington, L.C., Cortes, G., Tan, Z., Suter, E.E., et al. Imidazoquinoline Toll-like receptor 8 agonists activate human newborn monocytes and dendritic cells through adenosine-refractory and caspase-1-dependent pathways. J Allergy Clin Immunol 130 (2012), 195–204.e9.
14. Dowling, D.J., Tan, Z., Prokopowicz, Z.M., Palmer, C.D., Matthews, M.A., Dietsch, G.N., et al. The ultra-potent and selective TLR8 agonist VTX-294 activates human newborn and adult leukocytes. PLoS One, 8, 2013, e58164.
15. Hubbell, J.A., Thomas, S.N., Swartz, M.A., Materials engineering for immunomodulation. Nature 462 (2009), 449–460.
16. Swartz, M.A., Hirosue, S., Hubbell, J.A., Engineering approaches to immunotherapy. Sci Transl Med, 4, 2012, 148rv9.
17. Reddy, S.T., Swartz, M.A., Hubbell, J.A., Targeting dendritic cells with biomaterials: developing the next generation of vaccines. Trends Immunol 27 (2006), 573–579.
18. Bachmann, M.F., Jennings, G.T., Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 10 (2010), 787–796.
19. Cerritelli, S., Velluto, D., Hubbell, J.A., PEG-SS-PPS: reduction-sensitive disulfide block copolymer vesicles for intracellular drug delivery. Biomacromolecules 8 (2007), 1966–1972.
20. Cerritelli, S., O'Neil, C.P., Velluto, D., Fontana, A., Adrian, M., Dubochet, J., et al. Aggregation behavior of poly(ethylene glycol-bl-propylene sulfide) di- and triblock copolymers in aqueous solution. Langmuir 25 (2009), 11328–11335.
21. Scott, E.A., Stano, A., Gillard, M., Maio-Liu, A.C., Swartz, M.A., Hubbell, J.A., Dendritic cell activation and T cell priming with adjuvant- and antigen-loaded oxidation-sensitive polymersomes. Biomaterials 33 (2012), 6211–6219.
22. Stano, A., Scott, E.A., Dane, K.Y., Swartz, M.A., Hubbell, J.A., Tunable T cell immunity towards a protein antigen using polymersomes vs. solid-core nanoparticles. Biomaterials 34 (2013), 4339–4346.
23. Trumpfheller, C., Longhi, M.P., Caskey, M., Idoyaga, J., Bozzacco, L., Keler, T., et al. Dendritic cell-targeted protein vaccines: a novel approach to induce T-cell immunity. J Intern Med 271 (2012), 183–192.
24. Rappuoli, R., Aderem, A.A., 2020 vision for vaccines against HIV, tuberculosis and malaria. Nature 473 (2011), 463–469.
25. D'Argenio, D.A., Wilson, C.B., A decade of vaccines: Integrating immunology and vaccinology for rational vaccine design. Immunity 33 (2010), 437–440.
26. Vekemans, J., Amedei, A., Ota, M.O., D'Elios, M.M., Goetghebuer, T., Ismaili, J., et al. Neonatal bacillus Calmette-Guerin vaccination induces adult-like IFN-gamma production by CD4+ T lymphocytes. Eur J Immunol 31 (2001), 1531–1535.
27. Demirjian, A., Levy, O., Safety and efficacy of neonatal vaccination. Eur J Immunol 39 (2009), 36–46.
28. Dobrovolskaia, M.A., McNeil, S.E., Immunological properties of engineered nanomaterials. Nat Nanotechnol 2 (2007), 469–478.
29. O'Garra, A., Murphy, K.M., From IL-10 to IL-12: how pathogens and their products stimulate APCs to induce T(H)1 development. Nat Immunol 10 (2009), 929–932.
30. Levitz, S.M., Golenbock, D.T., Beyond empiricism: informing vaccine development through innate immunity research. Cell 148 (2012), 1284–1292.
31. Palmer, C.D., Ninkovic, J., Prokopowicz, Z.M., Mancuso, C.J., Marin, A., Andrianov, A.K., et al. The effect of stable macromolecular complexes of ionic polyphosphazene on HIV Gag antigen and on activation of human dendritic cells and presentation to T-cells. Biomaterials 35 (2014), 8876–8886.
32. Ganapathi, L., Van Haren, S., Dowling, D.J., Bergelson, I., Shukla, N.M., Malladi, S.S., et al. The imidazoquinoline toll-like receptor-7/8 agonist hybrid-2 potently induces cytokine production by human newborn and adult leukocytes. PLoS One, 10, 2015, e0134640.
33. Guiducci, C., Gong, M., Cepika, A.M., Xu, Z., Tripodo, C., Bennett, L., et al. RNA recognition by human TLR8 can lead to autoimmune inflammation. J Exp Med 210 (2013), 2903–2919.
34. Prota, G., Christensen, D., Andersen, P., Medaglini, D., Ciabattini, A., Peptide-specific T helper cells identified by MHC class II tetramers differentiate into several subtypes upon immunization with CAF01 adjuvanted H56 tuberculosis vaccine formulation. Vaccine 33 (2015), 6823–6830.
35. Pettengill, M.A., van Haren, S.D., Levy, O., Soluble mediators regulating immunity in early life. Front Immunol, 5, 2014, 457.
36. Zaitseva, M., Romantseva, T., Blinova, K., Beren, J., Sirota, L., Drane, D., et al. Use of human MonoMac6 cells for development of in vitro assay predictive of adjuvant safety in vivo. Vaccine 30 (2012), 4859–4865.
37. Heil, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303 (2004), 1526–1529.
38. Nabel, G.J., Designing tomorrow's vaccines. N Engl J Med 368 (2013), 551–560.
39. Geng, Y., Dalhaimer, P., Cai, S., Tsai, R., Tewari, M., Minko, T., et al. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat Nanotechnol 2 (2007), 249–255.
40. Walkey, C.D., Olsen, J.B., Guo, H., Emili, A., Chan, W.C., Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J Am Chem Soc 134 (2012), 2139–2147.
41. Levy, O., Suter, E.E., Miller, R.L., Wessels, M.R., Unique efficacy of Toll-like receptor 8 agonists in activating human neonatal antigen-presenting cells. Blood 108 (2006), 1284–1290.
42. Tacken, P.J., Zeelenberg, I.S., Cruz, L.J., van Hout-Kuijer, M.A., van de Glind, G., Fokkink, R.G., et al. Targeted delivery of TLR ligands to human and mouse dendritic cells strongly enhances adjuvanticity. Blood 118 (2011), 6836–6844.
43. Wu, T.Y., Singh, M., Miller, A.T., De Gregorio, E., Doro, F., D'Oro, U., et al. Rational design of small molecules as vaccine adjuvants. Sci Transl Med, 6, 2014, 263ra160.
44. van Haren, S.D., Ganapathi, L., Bergelson, I., Dowling, D.J., Banks, M., Samuels, R.C., et al. In vitro cytokine induction by TLR-activating vaccine adjuvants in human blood varies by age and adjuvant. Cytokine 83 (2016), 99–109.
45. Schreibelt, G., Benitez-Ribas, D., Schuurhuis, D., Lambeck, A.J., van Hout-Kuijer, M., Schaft, N., et al. Commonly used prophylactic vaccines as an alternative for synthetically produced TLR ligands to mature monocyte-derived dendritic cells. Blood 116 (2010), 564–574.
46. Mastelic, B., Garcon, N., Del Giudice, G., Golding, H., Gruber, M., Neels, P., et al. Predictive markers of safety and immunogenicity of adjuvanted vaccines. Biologicals 41 (2013), 458–468.
47. Oh, D.Y., Dowling, D.J., Ahmed, S., Choi, H., Brightman, S., Bergelson, I., et al. Adjuvant-induced human monocyte secretome profiles reveal adjuvant- and age-specific protein signatures. Mol Cell Proteomics 15 (2016), 1877–1894.
48. Shann, F., Editorial commentary: different strains of Bacillus Calmette-Guerin vaccine have very different effects on tuberculosis and on unrelated infections. Clin Infect Dis 61 (2015), 960–962.
49. Marciano, B.E., Huang, C.Y., Joshi, G., Rezaei, N., Carvalho, B.C., Allwood, Z., et al. BCG vaccination in patients with severe combined immunodeficiency: complications, risks, and vaccination policies. J Allergy Clin Immunol 133 (2014), 1134–1141.