Age-specific adjuvant synergy: Dual TLR7/8 and mincle activation of human newborn dendritic cells enables Th1 polarization

Journal of Immunology

Volumn 197, Issue 11, 2016, Pages 4413-4424

  Van Haren, Simon D ^a,b   Dowling, David J ^a,b   Foppen, Willemina ^a,b   Christensen, Dennis ^c   Andersen, Peter ^a,c   Reed, Steven G ^a,d   Hershberg, Robert M ^e   Baden, Lindsey R ^a,f   Levy, Ofer ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c STATENS SERUM INSTITUT   (Denmark)

^d INFECTIOUS DISEASE RESEARCH INSTITUTE   (United States)

^e VentiRx Pharmaceuticals   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ALPHA2 INTERFERON; C TYPE LECTIN RECEPTOR AGONIST; CD4 ANTIGEN; DECTIN 1; GAMMA INTERFERON; GLYCOPYRANOSYL LIPID ADJUVANT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; LECTIN RECEPTOR; RESIQUIMOD; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR AGONIST; TREHALOSE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CLEC4D PROTEIN, HUMAN; IMMUNOGLOBULIN RECEPTOR; LECTIN; TLR7 PROTEIN, HUMAN; TLR8 PROTEIN, HUMAN;

ADULT; AGE; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL CULTURE; CELL POLARITY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG EFFICACY; DRUG POTENTIATION; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; IMMUNOSTIMULATION; INFANT; MACROPHAGE; MONOCYTE; NEWBORN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; T LYMPHOCYTE ACTIVATION; TH1 CELL; UMBILICAL CORD BLOOD; ADOLESCENT; AGED; AGING; AGONISTS; CYTOLOGY; FEMALE; IMMUNOLOGY; MALE;

ADJUVANTS, IMMUNOLOGIC; ADOLESCENT; ADULT; AGED; AGING; CASPASE 1; DENDRITIC CELLS; FEMALE; HUMANS; INFANT, NEWBORN; LECTINS, C-TYPE; MALE; NF-KAPPA B; RECEPTORS, IMMUNOLOGIC; TH1 CELLS; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 8;

EID: 84996520942     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600282     Document Type: Article

References (60)

1. Elahi, S., J. M. Ertelt, J. M. Kinder, T. T. Jiang, X. Zhang, L. Xin, V. Chaturvedi, B. S. Strong, J. E. Qualls, K. A. Steinbrecher, et al. 2013. Immunosuppressive CD71+ erythroid cells compromise neonatal host defence against infection. Nature 504: 158-162.
2. Pettengill, M. A., S. D. van Haren, and O. Levy. 2014. Soluble mediators reg-ulating immunity in early life. Front. Immunol. 5: 457.
3. Willems, F., S. Vollstedt, and M. Suter. 2009. Phenotype and function of neonatal DC. Eur. J. Immunol. 39: 26-35.
4. Angelone, D. F., M. R. Wessels, M. Coughlin, E. E. Suter, P. Valentini, L. A. Kalish, and O. Levy. 2006. Innate immunity of the human newborn is polarized toward a high ratio of IL-6/TNF-alpha production in vitro and in vivo. Pediatr. Res. 60: 205-209.
5. Kollmann, T. R., J. Crabtree, A. Rein-Weston, D. Blimkie, F. Thommai, X. Y. Wang, P. M. Lavoie, J. Furlong, E. S. Fortuno, III, A. M. Hajjar, et al. 2009. Neonatal innate TLR-mediated responses are distinct from those of adults. J. Immunol. 183: 7150-7160.
6. Allen, A. C., and K. H. Mills. 2014. Improved pertussis vaccines based on adjuvants that induce cell-mediated immunity. Expert Rev. Vaccines 13: 1253-1264.
7. Kamphuis, T., T. Meijerhof, T. Stegmann, J. Lederhofer, J. Wilschut, and A. de Haan. 2012. Immunogenicity and protective capacity of a virosomal respiratory syncytial virus vaccine adjuvanted with monophosphoryl lipid A in mice. PLoS One 7: e36812.
8. Levy, O., S. Goriely, and T. R. Kollmann. 2013. Immune response to vaccine adjuvants during the first year of life. Vaccine 31: 2500-2505.
9. Coffman, R. L., A. Sher, and R. A. Seder. 2010. Vaccine adjuvants: putting innate immunity to work. Immunity 33: 492-503.
10. Schwarz, T. F. 2008. AS04-adjuvanted human papillomavirus-16/18 vaccination: recent advances in cervical cancer prevention. Expert Rev. Vaccines 7: 1465-1473.
11. Clegg, C. H., R. Roque, L. A. Perrone, J. A. Rininger, R. Bowen, and S. G. Reed. 2014. GLA-AF, an emulsion-free vaccine adjuvant for pandemic influenza. PLoS One 9: e88979.
12. Coler, R. N., S. Bertholet, M. Moutaftsi, J. A. Guderian, H. P. Windish, S. L. Baldwin, E. M. Laughlin, M. S. Duthie, C. B. Fox, D. Carter, et al. 2011. Development and characterization of synthetic glucopyranosyl lipid adjuvant system as a vaccine adjuvant. PLoS One 6: e16333.
13. van den Biggelaar, A. H., and W. S. Pomat. 2013. Immunization of newborns with bacterial conjugate vaccines. Vaccine 31: 2525-2530.
14. Kollmann, T. R., O. Levy, R. R. Montgomery, and S. Goriely. 2012. Innate immune function by Toll-like receptors: distinct responses in newborns and the elderly. Immunity 37: 771-783.
15. Burl, S., J. Townend, J. Njie-Jobe, M. Cox, U. J. Adetifa, E. Touray, V. J. Philbin, C. Mancuso, B. Kampmann, H. Whittle, et al. 2011. Age-dependent maturation of Toll-like receptor-mediated cytokine responses in Gambian infants. PLoS One 6: e18185.
16. Belderbos, M. E., O. Levy, F. Stalpers, J. L. Kimpen, L. Meyaard, and L. Bont. 2012. Neonatal plasma polarizes TLR4-mediated cytokine responses towards low IL-12p70 and high IL-10 production via distinct factors. PLoS One 7: e33419.
17. Levy, O., M. Coughlin, B. N. Cronstein, R. M. Roy, A. Desai, and M. R. Wessels. 2006. The adenosine system selectively inhibits TLR-mediated TNF-alpha production in the human newborn. J. Immunol. 177: 1956-1966.
18. Philbin, V. J., D. J. Dowling, L. C. Gallington, G. Cortes, Z. Tan, E. E. Suter, K. W. Chi, A. Shuckett, L. Stoler-Barak, M. Tomai, et al. 2012. 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: 195-204.e9.
19. Levy, O., E. E. Suter, R. L. Miller, and M. R. Wessels. 2006. Unique efficacy of Toll-like receptor 8 agonists in activating human neonatal antigen-presenting cells. Blood 108: 1284-1290.
20. Heldwein, K. A., M. D. Liang, T. K. Andresen, K. E. Thomas, A. M. Marty, N. Cuesta, S. N. Vogel, and M. J. Fenton. 2003. TLR2 and TLR4 serve distinct roles in the host immune response against Mycobacterium bovis BCG. J. Leukoc. Biol. 74: 277-286.
21. Yadav, M., and J. S. Schorey. 2006. The beta-glucan receptor dectin-1 functions together with TLR2 to mediate macrophage activation by mycobacteria. Blood 108: 3168-3175.
22. Matsunaga, I., and D. B. Moody. 2009. Mincle is a long sought receptor for mycobacterial cord factor. J. Exp. Med. 206: 2865-2868.
23. Schoenen, H., B. Bodendorfer, K. Hitchens, S. Manzanero, K. Werninghaus, F. Nimmerjahn, E. M. Agger, S. Stenger, P. Andersen, J. Ruland, et al. 2010. Cutting edge: mincle is essential for recognition and adjuvanticity of the my-cobacterial cord factor and its synthetic analog trehalose-dibehenate. J. Immunol. 184: 2756-2760.
24. Jensen, K. J., N. Larsen, S. Biering-Sørensen, A. Andersen, H. B. Eriksen, I. Monteiro, D. Hougaard, P. Aaby, M. G. Netea, K. L. Flanagan, and C. S. Benn. 2015. Heterologous immunological effects of early BCG vaccination in low-birth-weight infants in Guinea-Bissau: a randomized-controlled trial. J. Infect. Dis. 211: 956-967.
25. Cambi, A., and C. G. Figdor. 2003. Dual function of C-type lectin-like receptors in the immune system. Curr. Opin. Cell Biol. 15: 539-546.
26. Kamath, A. T., B. Mastelic, D. Christensen, A. F. Rochat, E. M. Agger, D. D. Pinschewer, P. Andersen, P. H. Lambert, and C. A. Siegrist. 2012. Synchronization of dendritic cell activation and antigen exposure is required for the induction of Th1/Th17 responses. J. Immunol. 188: 4828-4837.
27. Kamath, A. T., A. F. Rochat, D. Christensen, E. M. Agger, P. Andersen, P. H. Lambert, and C. A. Siegrist. 2009. A liposome-based mycobacterial vaccine induces potent adult and neonatal multifunctional T cells through the ex-quisite targeting of dendritic cells. PLoS One 4: e5771.
28. Eberle, M. E., and A. H. Dalpke. 2012. Dectin-1 stimulation induces suppressor of cytokine signaling 1, thereby modulating TLR signaling and T cell responses. J. Immunol. 188: 5644-5654.
29. Geijtenbeek, T. B., and S. I. Gringhuis. 2009. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9: 465-479.
30. Kingeter, L. M., and X. Lin. 2012. C-type lectin receptor-induced NF-kB activation in innate immune and inflammatory responses. Cell. Mol. Immunol. 9: 105-112.
31. Feinberg, H., S. A. Jégouzo, T. J. Rowntree, Y. Guan, M. A. Brash, M. E. Taylor, W. I. Weis, and K. Drickamer. 2013. Mechanism for recognition of an unusual mycobacterial glycolipid by the macrophage receptor mincle. J. Biol. Chem. 288: 28457-28465.
32. Dennehy, K. M., G. Ferwerda, I. Faro-Trindade, E. Pyz, J. A. Willment, P. R. Taylor, A. Kerrigan, S. V. Tsoni, S. Gordon, F. Meyer-Wentrup, et al. 2008. Syk kinase is required for collaborative cytokine production induced through Dectin-1 and Toll-like receptors. Eur. J. Immunol. 38: 500-506.
33. Berenbaum, M. C. 1981. Criteria for analyzing interactions between biologically active agents. Adv. Cancer Res. 35: 269-335.
34. Lederhuber, H., K. Baer, I. Altiok, K. Sadeghi, K. R. Herkner, and D. C. Kasper. 2011. MicroRNA-146: tiny player in neonatal innate immunity? Neonatology 99: 51-56.
35. Zaghouani, H., C. M. Hoeman, and B. Adkins. 2009. Neonatal immunity: faulty T-helpers and the shortcomings of dendritic cells. Trends Immunol. 30: 585-591.
36. Adkins, B., Y. Bu, and P. Guevara. 2001. The generation of Th memory in ne-onates versus adults: prolonged primary Th2 effector function and impaired development of Th1 memory effector function in murine neonates. J. Immunol. 166: 918-925.
37. Dowling, D. J., Z. Tan, Z. M. Prokopowicz, C. D. Palmer, M. A. Matthews, G. N. Dietsch, R. M. Hershberg, and O. Levy. 2013. The ultra-potent and selective TLR8 agonist VTX-294 activates human newborn and adult leukocytes. PLoS One 8: e58164.
38. Lemoine, S., B. Jaron, S. Tabka, C. Ettreiki, E. Deriaud, D. Zhivaki, C. Le Ray, O. Launay, L. Majlessi, P. Tissieres, C. Leclerc, and R. Lo-Man. 2015. Dectin-1 activation unlocks IL12A expression and reveals the TH1 potency of neonatal dendritic cells. J. Allergy Clin. Immunol. 136: 1355-1368.e1351-1315.
39. Lang, R., H. Schoenen, and C. Desel. 2011. Targeting Syk-Card9-activating C-type lectin receptors by vaccine adjuvants: findings, implications and open questions. Immunobiology 216: 1184-1191.
40. Strasser, D., K. Neumann, H. Bergmann, M. J. Marakalala, R. Guler, A. Rojowska, K. P. Hopfner, F. Brombacher, H. Urlaub, G. Baier, et al. 2012. Syk kinase-coupled C-type lectin receptors engage protein kinase C-s to elicit Card9 adaptor-mediated innate immunity. Immunity 36: 32-42.
41. Vijayan, D., K. J. Radford, A. G. Beckhouse, R. B. Ashman, and C. A. Wells. 2012. Mincle polarizes human monocyte and neutrophil responses to Candida albicans. Immunol. Cell Biol. 90: 889-895.
42. Hayashi, D., T. Takii, N. Fujiwara, Y. Fujita, I. Yano, S. Yamamoto, M. Kondo, E. Yasuda, E. Inagaki, K. Kanai, et al. 2009. Comparable studies of immunostimulating activities in vitro among Mycobacterium bovis bacillus Calmette-Guérin (BCG) substrains. FEMS Immunol. Med. Microbiol. 56: 116-128.
43. Williams, J. W., M. Y. Tjota, B. S. Clay, B. Vander Lugt, H. S. Bandukwala, C. L. Hrusch, D. C. Decker, K. M. Blaine, B. R. Fixsen, H. Singh, et al. 2013. Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation. Nat. Commun. 4: 2990.
44. Gringhuis, S. I., J. den Dunnen, M. Litjens, M. van der Vlist, and T. B. Geijtenbeek. 2009. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat. Immunol. 10: 1081-1088.
45. Openshaw, P. J. 2013. The mouse model of respiratory syncytial virus disease. Curr. Top. Microbiol. Immunol. 372: 359-369.
46. Kawai, T., and S. Akira. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650.
47. Netea, M. G., and L. Maródi. 2010. Innate immune mechanisms for recognition and uptake of Candida species. Trends Immunol. 31: 346-353.
48. Nakaira-Takahagi, E., M. A. Golim, C. F. Bannwart, R. Puccia, and M. T. Peraçoli. 2011. Interactions between TLR2, TLR4, and mannose receptors with gp43 from Paracoccidioides brasiliensis induce cytokine production by human monocytes. Med. Mycol. 49: 694-703.
49. Geijtenbeek, T. B., S. J. Van Vliet, E. A. Koppel, M. Sanchez-Hernandez, C. M. Vandenbroucke-Grauls, B. Appelmelk, and Y. Van Kooyk. 2003. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197: 7-17.
50. Wevers, B. A., T. M. Kaptein, E. M. Zijlstra-Willems, B. Theelen, T. Boekhout, T. B. Geijtenbeek, and S. I. Gringhuis. 2014. Fungal engagement of the C-type lectin mincle suppresses dectin-1-induced antifungal immunity. Cell Host Microbe 15: 494-505.
51. Mortaz, E., I. M. Adcock, P. Tabarsi, M. R. Masjedi, D. Mansouri, A. A. Velayati, J. L. Casanova, and P. J. Barnes. 2015. Interaction of pattern recognition receptors with Mycobacterium tuberculosis. J. Clin. Immunol. 35: 1-10.
52. Becher, B., M. Blain, P. S. Giacomini, and J. P. Antel. 1999. Inhibition of Th1 polarization by soluble TNF receptor is dependent on antigen-presenting cell-derived IL-12. J. Immunol. 162: 684-688.
53. Ferwerda, G., F. Meyer-Wentrup, B. J. Kullberg, M. G. Netea, and G. J. Adema. 2008. Dectin-1 synergizes with TLR2 and TLR4 for cytokine production in human primary monocytes and macrophages. Cell. Microbiol. 10: 2058-2066.
54. Volpe, E., N. Servant, R. Zollinger, S. I. Bogiatzi, P. Hupé, E. Barillot, and V. Soumelis. 2008. A critical function for transforming growth factor-beta, in-terleukin 23 and proinflammatory cytokines in driving and modulating human T (H)-17 responses. Nat. Immunol. 9: 650-657.
55. Hsu, H., S. Boudova, G. Mvula, T. H. Divala, R. G. Mungwira, C. Harman, M. K. Laufer, C. D. Pauza, and C. Cairo. 2016. Prolonged PD1 expression on neonatal Vdelta2 lymphocytes dampens proinflammatory responses: role of epigenetic regulation. J. Immunol. 197: 1884-1892.
56. White, G. P., P. M. Watt, B. J. Holt, and P. G. Holt. 2002. Differential patterns of methylation of the IFN-gamma promoter at CpG and non-CpG sites underlie differences in IFN-gamma gene expression between human neonatal and adult CD45RO-T cells. J. Immunol. 168: 2820-2827.
57. Ostrop, J., K. Jozefowski, S. Zimmermann, K. Hofmann, E. Strasser, B. Lepenies, and R. Lang. 2015. Contribution of MINCLE-SYK signaling to activation of primary human APCs by mycobacterial cord factor and the novel adjuvant TDB. J. Immunol. 195: 2417-2428.
58. Smirnov, D., J. J. Schmidt, J. T. Capecchi, and P. D. Wightman. 2011. Vaccine adjuvant activity of 3M-052: an imidazoquinoline designed for local activity without systemic cytokine induction. Vaccine 29: 5434-5442.
59. Hubbell, J. A., S. N. Thomas, and M. A. Swartz. 2009. Materials engineering for immunomodulation. Nature 462: 449-460.
60. Hansen, J., T. Lindenstrøm, J. Lindberg-Levin, C. Aagaard, P. Andersen, and E. M. Agger. 2012. CAF05: cationic liposomes that incorporate synthetic cord factor and poly(I:C) induce CTL immunity and reduce tumor burden in mice. Cancer Immunol. Immunother. 61: 893-903.