TLR-induced local metabolism of vitamin D3 plays an important role in the diversification of adaptive immune responses

Journal of Immunology

Volumn 182, Issue 7, 2009, Pages 4296-4305

  Enioutina, Elena Yu ^a   Bareyan, Diana ^a   Daynes, Raymond A ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIFEDIOL; CALCITRIOL; COLECALCIFEROL; INTERFERON; LIPOPOLYSACCHARIDE; OXYGENASE; PHOSPHORYL LIPID A; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; CALCIDIOL 1 MONOOXYGENASE; DRUG DERIVATIVE; IMMUNOLOGICAL ADJUVANT; LIPID A; TOLL LIKE RECEPTOR; VACCINE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; HUMORAL IMMUNITY; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; VITAMIN METABOLISM; ANIMAL; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL MOTION; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOID TISSUE; METABOLISM; TRANSGENIC MOUSE; WESTERN BLOTTING;

25-HYDROXYVITAMIN D3 1-ALPHA-HYDROXYLASE; ADJUVANTS, IMMUNOLOGIC; ANIMALS; B-LYMPHOCYTES; BLOTTING, WESTERN; CALCITRIOL; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CHOLECALCIFEROL; DENDRITIC CELLS; IMMUNITY, MUCOSAL; INTERFERON TYPE I; LIPID A; LYMPHOCYTE ACTIVATION; LYMPHOID TISSUE; MICE; MICE, TRANSGENIC; TOLL-LIKE RECEPTORS; VACCINES;

EID: 64249133408     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0804344     Document Type: Article

References (41)

1. HogenEsch, H. 2002. Mechanisms of stimulation of the immune response by aluminum adjuvants. Vaccine 20(Suppl. 3): S34-S39. (Pubitemid 34607673)
2. Silva, D. G., P. D. Cooper, and N. Petrovsky. 2004. Inulin-derived adjuvants efficiently promote both Th1 and Th2 immune responses. Immunol. Cell Biol. 82: 611-616.
3. Persing, D. H., R. N. Coler, M. J. Lacy, D. A. Johnson, J. R. Baldridge, R. M. Hershberg, and S. G. Reed. 2002. Taking toll: lipid A mimetics as adjuvants and immunomodulators. Trends Microbiol. 10: S32-S37.
4. Baldridge, J. R., P. McGowan, J. T. Evans, C. Cluff, S. Mossman, D. Johnson, and D. Persing. 2004. Taking a Toll on human disease: Toll-like receptor 4 agonists as vaccine adjuvants and monotherapeutic agents. Exp. Opin. Biol. Ther. 4: 1129-1138.
5. Casella, C. R., and T. C. Mitchell. 2008. Putting endotoxin to work for us: monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cell Mol. Life Sci. 65: 3231-3240.
6. Mata-Haro, V., C. Cekic, M. Martin, P. M. Chilton, C. R. Casella, and T. C. Mitchell. 2007. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 316: 1628-1632. (Pubitemid 46982038)
7. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17: 1-14.
8. Glenn, G. M., M. Rao, R. L. Richards, G. R. Matyas, and C. R. Alving. 1995. Murine IgG subclass antibodies to antigens incorporated in liposomes containing lipid A. Immunol. Lett. 47: 73-78.
9. Murata, K., M. Lechmann, M. Qiao, T. Gunji, H. J. Alter, and T. J. Liang. 2003. Immunization with hepatitis C virus-like particles protects mice from recombinant hepatitis C virus-vaccinia infection. Proc. Natl. Acad. Sci. USA 100: 6753-6758. (Pubitemid 36666652)
10. Enioutina, E. Y., D. Bareyan, and R. A. Daynes. 2008. TLR ligands that stimulate the metabolism of vitamin D3 in activated murine dendritic cells can function as effective mucosal adjuvants to subcutaneously administered vaccines. Vaccine 26: 601-613.
11. Hayes, C. E., F. E. Nashold, K. M. Spach, and L. B. Pedersen. 2003. The immunological functions of the vitamin D endocrine system. Cell. Mol. Biol. 49: 277-300.
12. Enioutina, E. Y., D. Visic, and R. A. Daynes. 2000. The induction of systemic and mucosal immune responses to antigen-adjuvant compositions administered into the skin: alterations in the migratory properties of dendritic cells appear to be important for stimulating mucosal immunity. Vaccine 18: 2753-2767.
13. Enioutina, E. Y., D. Bareyan, and R. A. Daynes. 2007. Vitamin D3-mediated alterations to myeloid dendritic cell trafficking in vivo expand the scope of their antigen presenting properties. Vaccine 25: 1236-1249.
14. Hoebe, K., and B. Beutler. 2004. LPS, dsRNA and the interferon bridge to adaptive immune responses: Trif, Tram, and other TIR adaptor proteins. J. Endotoxin Res. 10: 130-136. (Pubitemid 38559789)
15. Matsumoto, M., and T. Seya. 2008. TLR3: interferon induction by double-stranded RNA including poly(I:C). Adv. Drug Delivery Rev. 60: 805-812.
16. Bendelac, A., P. Matzinger, R. A. Seder, W. E. Paul, and R. H. Schwartz. 1992. Activation events during thymic selection. J. Exp. Med. 175: 731-742.
17. Wykes, M., A. Pombo, C. Jenkins, and G. G. MacPherson. 1998. Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J. Immunol. 161: 1313-1319. (Pubitemid 28380559)
18. MacPherson, G., N. Kushnir, and M. Wykes. 1999. Dendritic cells, B cells and the regulation of antibody synthesis. Immunol. Rev. 172: 325-334. (Pubitemid 30000489)
19. Itano, A. A., and M. K. Jenkins. 2003. Antigen presentation to naive CD4 T cells in the lymph node. Nat. Immunol. 4: 733-739.
20. Randolph, G. J., K. Inaba, D. F. Robbiani, R. M. Steinman, and W. A. Muller. 1999. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 11: 753-761.
21. Leon, B., and C. Ardavin. 2008. Monocyte-derived dendritic cells in innate and adaptive immunity. Immunol. Cell Biol. 86: 320-324. (Pubitemid 351667991)
22. Alvarez, D., E. H. Vollmann, and U. H. von Andrian. 2008. Mechanisms and consequences of dendritic cell migration. Immunity 29: 325-342.
23. + dendritic cells during infection with intracellular pathogens. Immunol. Lett. 114: 66-72.
24. Belyakov, I. M., S. A. Hammond, J. D. Ahlers, G. M. Glenn, and J. A. Berzofsky. 2004. Transcutaneous immunization induces mucosal CTLs and protective immunity by migration of primed skin dendritic cells. J. Clin. Invest. 113: 998-1007.
25. Cavanagh, L. L., R. Bonasio, I. B. Mazo, C. Halin, G. Cheng, A. W. van der Velden, A. Cariappa, C. Chase, P. Russell, M. N. Starnbach, et al. 2005. Activation of bone marrow-resident memory T cells by circulating, antigen-bearing dendritic cells. Nat. Immunol. 6: 1029-1037.
26. Kawai, T., and S. Akira. 2007. TLR signaling. Semin. Immunol. 19: 24-32.
27. Stoffels, K., L. Overbergh, A. Giulietti, L. Verlinden, R. Bouillon, and C. Mathieu. 2006. Immune regulation of 25-hydroxyvitamin-D3-1α-hydroxylase in human monocytes. J. Bone Miner. Res. 21: 37-47. (Pubitemid 43023225)
28. Fritsche, J., K. Mondal, A. Ehrnsperger, R. Andreesen, and M. Kreutz. 2003. Regulation of 25-hydroxyvitamin D3-1 α-hydroxylase and production of 1 α,25-dihydroxyvitamin D3 by human dendritic cells. Blood 102: 3314-3316. (Pubitemid 37314772)
29. Overbergh, L., K. Stoffels, M. Waer, A. Verstuyf, R. Bouillon, and C. Mathieu. 2006. Immune regulation of 25-hydroxyvitamin D-1α-hydroxylase in human monocytic THP1 cells: mechanisms of interferon-γ-mediated induction. J. Clin. Endocrinol. Metab. 91: 3566-3574. (Pubitemid 44402139)
30. Stoffels, K., L. Overbergh, R. Bouillon, and C. Mathieu. 2007. Immune regulation of 1α-hydroxylase in murine peritoneal macrophages: unravelling the IFNγ pathway. J. Steroid Biochem. Mol. Biol. 103: 567-571. (Pubitemid 46415674)
31. 3-hydroxylases. Steroids 66: 399-408.
32. Schauber, J., R. A. Dorschner, A. B. Coda, A. S. Buchau, P. T. Liu, D. Kiken, Y. R. Helfrich, S. Kang, H. Z. Elalieh, A. Steinmeyer, et al. 2007. Injury enhances TLR2 function and antimicrobial peptide expression through a vitamin D-dependent mechanism. J. Clin. Invest. 117: 803-811. (Pubitemid 46348539)
33. Liu, P. T., S. Stenger, H. Li, L. Wenzel, B. H. Tan, S. R. Krutzik, M. T. Ochoa, J. Schauber, K. Wu, C. Meinken, et al. 2006. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311: 1770-1773.
34. Krutzik, S. R., M. Hewison, P. T. Liu, J. A. Robles, S. Stenger, J. S. Adams, and R. L. Modlin. 2008. IL-15 links TLR2/1-induced macrophage differentiation to the vitamin D-dependent antimicrobial pathway. J. Immunol. 181: 7115-7120.
35. Bouvet, J. P., N. Decroix, and P. Pamonsinlapatham. 2002. Stimulation of local antibody production: parenteral or mucosal vaccination? Trends Immunol. 23: 209-213.
36. Clements, J. D., N. M. Hartzog, and F. L. Lyon. 1988. Adjuvant activity of Escherichia coli heat-labile enterotoxin and effect on the induction of oral tolerance in mice to unrelated protein antigens. Vaccine 6: 269-277.
37. Hajishengallis, G., S. M. Michalek, and M. W. Russell. 1996. Persistence of serum and salivary antibody responses after oral immunization with a bacterial protein antigen genetically linked to the A2/B subunits of cholera toxin. Infect. Immun. 64: 665-667. (Pubitemid 26032846)
38. Holmgren, J., and C. Czerkinsky. 2005. Mucosal immunity and vaccines. Nat. Med. 11: S45-S53.
39. Lefeber, D. J., B. Benaissa-Trouw, J. F. Vliegenthart, J. P. Kamerling, W. T. Jansen, K. Kraaijeveld, and H. Snippe. 2003. Th1-directing adjuvants increase the immunogenicity of oligosaccharide-protein conjugate vaccines related to Streptococcus pneumoniae type 3. Infect. Immun. 71: 6915-6920.
40. Strindelius, L., L. Degling Wikingsson, and I. Sjoholm. 2002. Extracellular antigens from Salmonella enteritidis induce effective immune response in mice after oral vaccination. Infect. Immun. 70: 1434-1442. (Pubitemid 34163421)
41. Sukumar, N., C. F. Love, M. S. Conover, N. D. Kock, P. Dubey, and R. Deora. 2009. Active and passive immunization with Bordetella colonization factor A (BcfA) protects mice against respiratory challenge with Bordetella bronchiseptica. Infect. Immun. 77: 885-895.