Intradermally administered TLR4 agonist GLA-SE enhances the capacity of human skin DCs to activate T cells and promotes emigration of Langerhans cells

Vaccine

Volumn 30, Issue 28, 2012, Pages 4216-4224

  Schneider, Laura P ^a   Schoonderwoerd, Antoinet J ^a   Moutaftsi, Magdalini ^b   Howard, Randall F ^b   Reed, Steven G ^b,c   de Jong, Esther C ^a   Teunissen, Marcel B M ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b INFECTIOUS DISEASE RESEARCH INSTITUTE   (United States)

^c Immune Design Corp   (United States)

Author keywords

Glucopyranosyl lipid A; Human skin; Intradermal vaccination; Langerhans cell; TLR4 agonist

Indexed keywords

GLUCOPYRANOSYL LIPID A; LIPID A DERIVATIVE; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ARTICLE; CD4+ T LYMPHOCYTE; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; DRUG EFFECT; DRUG POTENCY; EMULSION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LANGERHANS CELL; MALE; PHENOTYPE; PRIORITY JOURNAL;

CELL MOVEMENT; FEMALE; HUMANS; INJECTIONS, INTRADERMAL; LANGERHANS CELLS; LIPID A; MALE; SKIN; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 4;

EID: 84861684590     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2012.04.051     Document Type: Article

References (46)

1. Wack A., Rappuoli R. Vaccinology at the beginning of the 21st century. Current Opinion in Immunology 2005, 17:411-418.
2. Steinman R.M., Hawiger D., Nussenzweig M.C. Tolerogenic dendritic cells. Annual Review of Immunology 2003, 21:685-711.
3. Schnare M., Barton G.M., Holt A.C., Takeda K., Akira S., Medzhitov R. Toll-like receptors control activation of adaptive immune responses. Nature Immunology 2001, 2:947-950.
4. Miyake K. Innate immune sensing of pathogens and danger signals by cell surface Toll-like receptors. Seminars in Immunology 2007, 19:3-10.
5. Hoebe K., Janssen E.M., Kim S.O., Alexopoulou L., Flavell R.A., Han J., et al. Upregulation of costimulatory molecules induced by lipopolysaccharide and double-stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nature Immunology 2003, 4:1223-1229.
6. Cucak H., Yrlid U., Reizis B., Kalinke U., Johansson-Lindbom B. Type I interferon signaling in dendritic cells stimulates the development of lymph-node-resident T follicular helper cells. Immunity 2009, 31:491-501.
7. McAleer J.P., Liu B., Li Z., Ngoi S.M., Dai J., Oft M., et al. Potent intestinal Th17 priming through peripheral lipopolysaccharide-based immunization. Journal of Leukocyte Biology 2010, 88:21-31.
8. Qureshi N., Takayama K., Ribi E. Purification and structural determination of nontoxic lipid A obtained from the lipopolysaccharide of Salmonella typhimurium. Journal of Biological Chemistry 1982, 257:11808-11815.
9. Velez I.D., Gilchrist K., Martinez S., Ramirez-Pineda J.R., Ashman J.A., Alves F.P., et al. Safety and immunogenicity of a defined vaccine for the prevention of cutaneous leishmaniasis. Vaccine 2009, 28:329-337.
10. Goto Y., Bhatia A., Raman V.S., Vidal S.E., Bertholet S., Coler R.N., et al. Leishmania infantum sterol 24-c-methyltransferase formulated with MPL-SE induces cross-protection against L. major infection. Vaccine 2009, 27:2884-2890.
11. Reed S.G., Coler R.N., Dalemans W., Tan E.V., DeLa Cruz E.C., Basaraba R.J., et al. Defined tuberculosis vaccine, Mtb72F/AS02A, evidence of protection in cynomolgus monkeys. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:2301-2306.
12. Bertholet S., Goto Y., Carter L., Bhatia A., Howard R.F., Carter D., et al. Optimized subunit vaccine protects against experimental leishmaniasis. Vaccine 2009, 27:7036-7045.
13. Bojang K.A., Olodude F., Pinder M., Ofori-Anyinam O., Vigneron L., Fitzpatrick S., et al. Safety and immunogenicty of RTS,S/AS02A candidate malaria vaccine in Gambian children. Vaccine 2005, 23:4148-4157.
14. Kester K.E., Cummings J.F., Ofori-Anyinam O., Ockenhouse C.F., Krzych U., Moris P., et al. Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. Journal of Infectious Diseases 2009, 200:337-346.
15. Didierlaurent A.M., Morel S., Lockman L., Giannini S.L., Bisteau M., Carlsen H., et al. AS04, an aluminum salt- and TLR4 agonist-based adjuvant system, induces a transient localized innate immune response leading to enhanced adaptive immunity. Journal of Immunology 2009, 183:6186-6197.
16. + T cells. Journal of Leukocyte Biology 2005, 78:1273-1280.
17. Casella C.R., Mitchell T.C. Putting endotoxin to work for us: monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cellular and Molecular Life Sciences 2008, 65:3231-3240.
18. Anderson R.C., Fox C.B., Dutill T.S., Shaverdian N., Evers T.L., Poshusta G.R., et al. Physicochemical characterization and biological activity of synthetic TLR4 agonist formulations. Colloids and Surfaces B: Biointerfaces 2010, 75:123-132.
19. Baldwin S.L., Bertholet S., Kahn M., Zharkikh I., Ireton G.C., Vedvick T.S., et al. Intradermal immunization improves protective efficacy of a novel TB vaccine candidate. Vaccine 2009, 27:3063-3071.
20. Coler R.N., Bertholet S., Moutaftsi M., Guderian J.A., Windish H.P., Baldwin S.L., et al. Development and characterization of synthetic glucopyranosyl lipid adjuvant system as a vaccine adjuvant. PLoS One 2011, 6:e16333.
21. Pantel A., Cheong C., Dandamudi D., Shrestha E., Mehandru S., Brane L., et al. A new synthetic TLR4 agonist, GLA, allows dendritic cells targeted with antigen to elicit Th1 T-cell immunity in vivo. European Journal of Immunology 2012, 42:101-109.
22. Bertholet S., Ireton G.C., Ordway D.J., Windish H.P., Pine S.O., Kahn M., et al. A defined tuberculosis vaccine candidate boosts BCG and protects against multidrug-resistant Mycobacterium tuberculosis. Science Translational Medicine 2010, 2:53ra74.
23. Lumsden J.M., Pichyangkul S., Srichairatanakul U., Yongvanitchit K., Limsalakpetch A., Nurmukhambetova S., et al. Evaluation of the safety and immunogenicity in rhesus monkeys of a recombinant malaria vaccine for Plasmodium vivax with a synthetic Toll-like receptor 4 agonist formulated in an emulsion. Infection and Immunity 2011, 79:3492-3500.
24. Windish H.P., Duthie M.S., Ireton G., Lucas E., Laurance J.D., Bailor R.H., et al. Protection of mice from Mycobacterium tuberculosis by ID87/GLA-SE, a novel tuberculosis subunit vaccine candidate. Vaccine 2011, 29:7842-7848.
25. Teunissen M.B.M., Haniffa M., Collin M.P. Insight into the immunobiology of human skin and functional specialization of skin dendritic cell subsets to innovate intradermal vaccination design. Current Topics in Microbiology and Immunology 2012, 351:25-76.
26. + T cell-stimulating skin-emigrated dendritic cells. Journal of Immunology 2006, 177:2208-2215.
27. + dermal dendritic cells. Immunity 2008, 29:497-510.
28. + T cell responses elicited by different subsets of human skin migratory dendritic cells. Journal of Immunology 2005, 175:7905-7915.
29. Romani N., Thurnher M., Idoyaga J., Steinman R.M., Flacher V. Targeting of antigens to skin dendritic cells: possibilities to enhance vaccine efficacy. Immunology and Cell Biology 2010, 88:424-430.
30. Valladeau J., Saeland S. Cutaneous dendritic cells. Seminars in Immunology 2005, 17:273-283.
31. van der Aar A.M.G., Sylva-Steenland R.M., Bos J.D., Kapsenberg M.L., de Jong E.C., Teunissen M.B.M. Loss of TLR2, TLR4, and TLR5 on Langerhans cells abolishes bacterial recognition. Journal of Immunology 2007, 178:1986-1990.
32. Takeuchi J., Watari E., Shinya E., Norose Y., Matsumoto M., Seya T., et al. Down-regulation of Toll-like receptor expression in monocyte-derived Langerhans cell-like cells: implications of low-responsiveness to bacterial components in the epidermal Langerhans cells. Biochemical and Biophysical Research Communications 2003, 306:674-679.
33. Flacher V., Bouschbacher M., Verronese E., Massacrier C., Sisirak V., Berthier-Vergnes O., et al. Human Langerhans cells express a specific TLR profile and differentially respond to viruses and Gram-positive bacteria. Journal of Immunology 2006, 177:7959-7967.
34. Klechevsky E., Liu M., Morita R., Banchereau R., Thompson-Snipes L., Palucka A.K., et al. Understanding human myeloid dendritic cell subsets for the rational design of novel vaccines. Human Immunology 2009, 70:281-288.
35. + hematopoietic progenitors stimulate greater cytolytic T lymphocyte activity in the absence of bioactive IL-12p70, by either single peptide presentation or cross-priming, than do dermal-interstitial or monocyte-derived dendritic cells. Journal of Immunology 2004, 173:2780-2791.
36. + T cell responses. Journal of Immunology 2011, 187:3488-3492.
37. + counterparts. International Immunology 2007, 19:1271-1279.
38. Nestle F.O., Zheng X.G., Thompson C.B., Turka L.A., Nickoloff B.J. Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets. Journal of Immunology 1993, 151:6535-6545.
39. + dendritic cells: the levels of IL-12 are determined during the final dendritic cell maturation and are resistant to further modulation. Journal of Immunology 1998, 161:2804-2809.
40. de Jong E.C., Vieira P.L., Kalinski P., Schuitemaker J.H., Tanaka Y., Wierenga E.A., et al. Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse th cell-polarizing signals. Journal of Immunology 2002, 168:1704-1709.
41. Pearton M., Kang S.M., Song J.M., Anstey A.V., Ivory M., Compans R.W., et al. Changes in human Langerhans cells following intradermal injection of influenza virus-like particle vaccines. PLoS One 2010, 5:e12410.
42. Lebre M.C., van der Aar A.M.G., van Baarsen L., van Capel T.M., Schuitemaker J.H., Kapsenberg M.L., et al. Human keratinocytes express functional Toll-like receptor 3, 4, 5, and 9. Journal of Investigative Dermatology 2007, 127:331-341.
43. Grone A. Keratinocytes and cytokines. Veterinary Immunology and Immunopathology 2002, 88:1-12.
44. Uchi H., Terao H., Koga T., Furue M. Cytokines and chemokines in the epidermis. Journal of Dermatological Science 2000, 24(Suppl. 1):S29-S38.
45. Mosca F., Tritto E., Muzzi A., Monaci E., Bagnoli F., Iavarone C., et al. Molecular and cellular signatures of human vaccine adjuvants. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:10501-10506.
46. Baldwin S.L., Shaverdian N., Goto Y., Duthie M.S., Raman V.S., Evers T., et al. Enhanced humoral and Type 1 cellular immune responses with Fluzone adjuvanted with a synthetic TLR4 agonist formulated in an emulsion. Vaccine 2009, 27:5956-5963.