Adjuvant-carrying synthetic vaccine particles augment the immune response to encapsulated antigen and exhibit strong local immune activation without inducing systemic cytokine release

Vaccine

Volumn 32, Issue 24, 2014, Pages 2882-2895

  Ilyinskii, Petr O ^a   Roy, Christopher J ^a   O'Neil, Conlin P ^a   Browning, Erica A ^a   Pittet, Lynnelle A ^a   Altreuter, David H ^a   Alexis, Frank ^b,f   Tonti, Elena ^c,g   Shi, Jinjun ^b   Basto, Pamela A ^d,e   Iannacone, Matteo ^c   Radovic Moreno, Aleksandar F ^d,e   Langer, Robert S ^d,e   Farokhzad, Omid C ^b   von Andrian, Ulrich H ^c   Johnston, Lloyd P M ^a   Kishimoto, Takashi Kei ^a  

^a Selecta Biosciences   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d David H Koch Institute for Integrative Cancer Research   (United States)

^e HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^f CLEMSON UNIVERSITY   (United States)

^g SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Adjuvant; CpG; R848; Resiquimod; Synthetic nanoparticle vaccine; TLR agonist

Indexed keywords

ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; CYTOKINE; EPITOPE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIGAND; MONOCYTE CHEMOTACTIC PROTEIN 1; NANOPARTICLE; OVALBUMIN; POLYGLACTIN; POLYMER; RANTES; RESIQUIMOD; SYNTHETIC VACCINE PARTICLE; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CELL INFILTRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG FORMULATION; FEMALE; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOSTIMULATION; INJECTION; INOCULATION; LYMPH NODE; MOUSE; NANOENCAPSULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STABLE EXPRESSION; VACCINATION;

ADJUVANT; CPG; R848; RESIQUIMOD; SYNTHETIC NANOPARTICLE VACCINE; TLR AGONIST;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODY FORMATION; ANTIGENS; CELLS, CULTURED; CYTOKINES; FEMALE; IMIDAZOLES; IMMUNITY, CELLULAR; MICE, INBRED C57BL; NANOPARTICLES; OLIGODEOXYRIBONUCLEOTIDES; SPLEEN; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 8; TOLL-LIKE RECEPTOR 9; VACCINES, SYNTHETIC;

EID: 84899912149     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2014.02.027     Document Type: Article

References (73)

1. Alving C.R., Peachman K.K., Rao M., Reed S.G. Adjuvants for human vaccines. Curr Opin Immunol 2012, 24:310-315.
2. Pulendran B., Ahmed R. Immunological mechanisms of vaccination. Nat Immunol 2011, 12:509-517.
3. Leroux-Roels G. Unmet needs in modern vaccinology. Adjuvants to improve the immune response. Vaccine 2010, 28S:C25-C36.
4. Wang W., Singh M. Selection of adjuvants for enhanced vaccine potency. World J Vaccines 2011, 1:33-78.
5. Evans T.G., McElrath M.J., Matthews T., Montefiori D., Weinhold K., Wolff M., et al. QS-21 promotes an adjuvant effect allowing for reduced antigen dose during HIV-1 envelope subunit immunization in humans. Vaccine 2001, 19:2080-2091.
6. Buge S.L., Ma H.L., Amara R.R., Wyatt L.S., Earl P.L., Villinger F., et al. Gp120-alum boosting of a Gag-Pol-Env DNA/MVA AIDS vaccine: poorer control of a pathogenic viral challenge. AIDS Res Hum Retroviruses 2003, 19:891-900.
7. Patel J., Galey D., Jones J., Ray P., Woodward J.G., Nath A., et al. HIV-1 Tat-coated nanoparticles result in enhanced humoral immune responses and neutralizing antibodies compared to alum adjuvant. Vaccine 2006, 24:3564-3573.
8. Vajdy M., Selby M., Medina-Selby A., Coit D., Hall J., Tandeske L., et al. Hepatitis C virus polyprotein vaccine formulations capable of inducing broad antibody and cellular immune responses. J Gen Virol 2006, 87:2253-2262.
9. Huleatt J.W., Nakaar V., Desai P., Huang Y., Hewitt D., Jacobs A., et al. Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin. Vaccine 2008, 26:201-214.
10. Sokolovska A., Hem S.L., HogenEsch H. Activation of dendritic cells and induction of CD4(+) T cell differentiation by aluminum-containing adjuvants. Vaccine 2007, 25:4575-4585.
11. Castilow E.M., Olson M.R., Varga S.M. Understanding respiratory syncytial virus (RSV) vaccine-enhanced disease. Immunol Res 2007, 39:225-239.
12. Tomai M.A., Vasilakos J.P. TLR-7 and -8 agonists as vaccine adjuvants. Expert Rev Vaccines 2011, 10:405-407.
13. Aguilar J.C., Rodríguez E.G. Vaccine adjuvants revisited. Vaccine 2007, 25:3752-3762.
14. Krieg A.M., Yi A.K., Matson S., Waldschmidt T.J., Bishop G.A., Teasdale R., et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995, 374:546-549.
15. Suzuki K., Mori A., Ishii K.J., Saito J., Singer D.S., Klinman D.M., et al. Activation of target-tissue immune-recognition molecules by double-stranded polynucleotides. Proc Natl Acad Sci U S A 1999, 96:2285-2290.
16. Schenten D., Medzhitov R. The control of adaptive immune responses by the innate immune system. Adv Immunol 2011, 109:87-124.
17. Kawai T., Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2010, 34:637-650.
18. Akira S. Innate immunity and adjuvants. Phil Trans R Soc B 2011, 366:2748-2755.
19. Hemmi H., Kaisho T., Takeuchi O., Sato S., Sanjo H., Hoshino K., et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002, 3:196-200.
20. Jurk M., Heil F., Vollmer J., Schetter C., Krieg A.M., Wagner H., et al. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat Immunol 2002, 3:499.
21. Edwards A.D., Diebold S.S., Slack E.M., Tomizawa H., Hemmi H., Kaisho T., et al. Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8 alpha+ DC correlates with unresponsiveness to imidazoquinolines. Eur J Immunol 2003, 33:827-833.
22. Diebold S.S., Kaisho T., Hemmi H., Akira S., Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004, 303:1529-1531.
23. 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 2004, 303:1526-1529.
24. Diebold S.S. Recognition of viral single-stranded RNA by Toll-like receptors. Adv Drug Deliv Rev 2008, 60:813-823.
25. Sato Y., Roman M., Tighe H., Lee D., Corr M., Nguyen M.D., et al. Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science 1996, 273:352-354.
26. Roman M., Martin-Orozco E., Goodman J.S., Nguyen M.D., Sato Y., Ronaghy A., et al. Immunostimulatory DNA sequences function as T helper-1-promoting adjuvants. Nat Med 1997, 3:849-854.
27. Sparwasser T., Miethke T., Lipford G., Borschert K., Häcker H., Heeg K., et al. Bacterial DNA causes septic shock. Nature 1997, 386:336-337.
28. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000, 408:740-745.
29. Harper D.M. Currently approved prophylactic HPV vaccines. Expert Rev Vaccines 2009, 8:1663-1679.
30. Johnson D.A. Synthetic TLR4-active glycolipids as vaccine adjuvants and stand-alone immunotherapeutics. Curr Top Med Chem 2008, 8:64-79.
31. Basith S., Manavalan B., Lee G., Kim S.G., Choi S. Toll-like receptor modulators: a patent review (2006-2010). Expert Opin Ther Pat 2011, 21:927-944.
32. Wang Y., Abel K., Lantz K., Krieg A.M., McChesney M.B., Miller C.J. The Toll-like receptor 7 (TLR7) agonist, imiquimod, and the TLR9 agonist, CpG ODN, induce antiviral cytokines and chemokines but do not prevent vaginal transmission of simian immunodeficiency virus when applied intravaginally to rhesus macaques. J Virol 2005, 79:14355-14370.
33. Krieg A.M. Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 2006, 5:471-484.
34. Wille-Reece U., Flynn B.J., Loré K., Koup R.A., Miles A.P., Saul A., et al. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J Exp Med 2006, 203:1249-1258.
35. Karan D., Krieg A.M., Lubaroff D.M. Paradoxical enhancement of CD8 T cell-dependent anti-tumor protection despite reduced CD8 T cell responses with addition of a TLR9 agonist to a tumor vaccine. Int J Cancer 2007, 121:1520-1528.
36. Krieg A.M. Antiinfective applications of Toll-like receptor 9 agonists. Proc Am Thorac Soc 2007, 4:289-294.
37. Vasilakos J.P., Smith R.M.A., Gibson S.J., Lindh J.M., Pederson L.K., Reiter M.J., et al. Adjuvant activities of immune response modifier R-848: comparison with CpG ODN. Cell Immunol 2000, 204:64-74.
38. Doxsee C.L., Riter T.R., Reiter M.J., Gibson S.J., Vasilakos J.P., Kedl R.M. The immune response modifier and Toll-like receptor 7 agonist S-27609 selectively induces IL-12 and TNF-alpha production in CD11c+CD11b+CD8- dendritic cells. J Immunol 2003, 171:1156-1163.
39. Pockros P.J., Guyader D., Patton H., Tong M.J., Wright T., McHutchison J.G., et al. Oral resiquimod in chronic HCV infection: safety and efficacy in 2 placebo-controlled, double-blind phase IIa studies. J Hepatol 2007, 47:174-182.
40. Malyala P., O'Hagan D.T., Singh M. Enhancing the therapeutic efficacy of CpG oligonucleotides using biodegradable microparticles. Adv Drug Deliv Rev 2009, 61:218-225.
41. Bachmann M.F., Jennings G.T. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 2010, 10:787-796.
42. Kasturi S.P., Skountzou I., Albrecht R.A., Koutsonanos D., Hua T., Nakaya H.I., et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 2011, 470:543-547.
43. Junt T., Moseman E.A., Iannacone M., Massberg S., Lang P.A., Boes M., et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007, 450:110-114.
44. Manolova V., Flace A., Bauer M., Schwarz K., Saudan P., Bachmann M.F. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 2008, 38:1404-1413.
45. Singh M., Kazzaz J., Ugozzoli M., Malyala P., Chesko J., O'Hagan D.T. Polylactide-co-glycolide microparticles with surface adsorbed antigens as vaccine delivery systems. Curr Drug Deliv 2006, 3:115-120.
46. Wagner H. The immunogenicity of CpG-antigen conjugates. Adv Drug Deliv Rev 2009, 61:243-247.
47. Zambaux M.F., Bonneaux F., Gref R., Dellacherie E., Vigneron C. MPEO-PLA nanoparticles: effect of MPEO content on some of their surface properties. J Biomed Mater Res 1999, 44:109-115.
48. Dechy-Cabaret O., Martin-Vaca B., Bourissou D. Controlled ring-opening polymerization of lactide and glycolide. Chem Rev 2004, 104:6147-6176.
49. Astete C., Sabliov C. Synthesis and characterization of PLGA nanoparticles. J Biomater Sci Polym Ed 2006, 17:247-289.
50. Udenfriend S.S., Stein S., Böhlen P., Dairman W., Leimgruber W., Weigele M. Fluorescamine: a reagent for assay of amino acids, peptides, proteins, and primary amines in the picomole range. Science 1972, 178:871-872.
51. Li C., Goudy K., Hirsch M., Asokan A., Fan Y., Alexander J., et al. Cellular immune response to cryptic epitopes during therapeutic gene transfer. Proc Natl Acad Sci U S A 2009, 106:10770-10774.
52. Graul A., Castañer J. S-28463. Treatment of hepatitis C interferon inducer. Drugs Future 1999, 24:622-627.
53. Carpentier A.F., Xie J., Mokhtari K., Delattre J.Y. Successful treatment of intracranial gliomas in rat by oligodeoxynucleotides containing CpG motifs. Clin Cancer Res 2000, 6:2469-2473.
54. Heckelsmiller K., Rall K., Beck S., Schlamp A., Seiderer J., Jahrsdörfer B., et al. Peritumoral CpG DNA elicits a coordinated response of CD8 T cells and innate effectors to cure established tumors in a murine colon carcinoma model. J Immunol 2002, 169:3892-3899.
55. Lonsdorf A.S., Kuekrek H., Stern B.V., Boehm B.O., Lehmann P.V., Tary-Lehmann M. Intratumor CpG-oligodeoxynucleotide injection induces protective antitumor T cell immunity. J Immunol 2003, 171:3941-3946.
56. Sauder D.N., Smith M.H., Senta-McMillian T., Soria I., Meng T.C. Randomized, single-blind, placebo-controlled study of topical application of the immune response modulator resiquimod in healthy adults. Antimicrob Agents Chemother 2003, 47:3846-3852.
57. Carpentier A., Laigle-Donadey F., Zohar S., Capelle L., Behin A., Tibi A., et al. Phase 1 trial of a CpG oligodeoxynucleotide for patients with recurrent glioblastoma. Neuro-Oncology 2006, 8:60-66.
58. Pashenkov M., Goëss G., Wagner C., Hörmann M., Jandl T., Moser A., et al. Phase II trial of a Toll-like receptor 9-activating oligonucleotide in patients with metastatic melanoma. J Clin Oncol 2006, 24:5716-5724.
59. Mark K.E., Corey L., Meng T.C., Magaret A.S., Huang M.L., Selke S., et al. Topical resiquimod 0.01% gel decreases herpes simplex virus type 2 genital shedding: a randomized, controlled trial. J Infect Dis 2007, 195:1324-1331.
60. Wu C.C., Hayashi T., Takabayashi K., Sabet M., Smee D.F., Guiney D.D., et al. Immunotherapeutic activity of a conjugate of a Toll-like receptor 7 ligand. Proc Natl Acad Sci U S A 2007, 104:3990-3995.
61. Fife K.H., Meng T.C., Ferris D.G., Liu P. Effect of resiquimod 0.01% gel on lesion healing and viral shedding when applied to genital herpes lesions. Antimicrob Agents Chemother 2008, 52:477-482.
62. Thomsen L.L., Topley P., Daly M.G., Brett S.J., Tite J.P. Imiquimod and resiquimod in a mouse model: adjuvants for DNA vaccination by particle-mediated immunotherapeutic delivery. Vaccine 2004, 22:1799-1809.
63. Chu R.S., Targoni O.S., Krieg A.M., Lehmann P.V., Harding C.V. CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J Exp Med 1997, 186:1623-1631.
64. Wille-Reece U., Flynn B.J., Loré K., Koup R.A., Kedl R.M., Mattapallil J.J., et al. HIV Gag protein conjugated to a Toll-like receptor 7/8 agonist improves the magnitude and quality of Th1 and CD8+ T cell responses in nonhuman primates. Proc Natl Acad Sci U S A 2005, 102:15190-15194.
65. Wille-Reece U., Wu C.Y., Flynn B.J., Kedl R.M., Seder R.A. Immunization with HIV-1 Gag protein conjugated to a TLR7/8 agonist results in the generation of HIV-1 Gag-specific Th1 and CD8+ T cell responses. J Immunol 2005, 174:7676-7683.
66. Wille-Reece U., Flynn B.J., Loré K., KoupA R.A., Miles A.P., Saul A., et al. Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J Exp Med 2006, 203:1249-1258.
67. Klinman D.M., Klaschik S., Tomaru K., Shirota H., Tross D., Ikeuchi H. Immunostimulatory CpG oligonucleotides: effect on gene expression and utility as vaccine adjuvants. Vaccine 2010, 28:1919-1923.
68. Murad Y.M., Clay T.M. CpG oligodeoxynucleotides as TLR9 agonists: therapeutic applications in cancer. BioDrugs 2009, 23:361-375.
69. O'Hagan D.T., De Gregorio E. The path to a successful vaccine adjuvant-'the long and winding road'. Drug Discov Today 2009, 14:541-551.
70. Batista-Duharte A., Lindblad E.B., Oviedo-Orta E. Progress in understanding adjuvant immunotoxicity mechanisms. Toxicol Lett 2011, 203:97-105.
71. 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 2011, 118:6836-6844.
72. Bauer S., Kirschning C.J., Häcker H., Redecke V., Hausmann S., Akira S., et al. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci U S A 2001, 98:9237-9242.
73. Verthelyi D., Ishii K.J., Gursel M., Takeshita F., Klinman D.M. Human peripheral blood cells differentially recognize and respond to two distinct CPG motifs. J Immunol 2001, 166:2372-2377.