Regulation of CYP27B1 and CYP24A1 hydroxylases limits cell-autonomous activation of vitamin D in dendritic cells

European Journal of Immunology

Volumn 44, Issue 6, 2014, Pages 1781-1790

  Kundu, Rhiannon ^a   Chain, Benjamin M ^a   Coussens, Anna K ^b   Khoo, Bernard ^a   Noursadeghi, Mahdad ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

CYP24A1; CYP27B1; DCs; Macrophages; Vitamin D

Indexed keywords

1,25 DIHYDROXYERGOCALCIFEROL; B7 ANTIGEN; CATHELICIDIN; CD209 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; CYTOCHROME P450; CYTOCHROME P450 24A1 HYDROXYLASE; CYTOCHROME P450 27B1 HYDROXYLASE; GAMMA INTERFERON; OXYGENASE; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR;

ALTERNATIVE RNA SPLICING; AMPLICON; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EXON; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOSTIMULATION; INNATE IMMUNITY; INTRON; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; MONOCYTE; NORMAL HUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION TERMINATION; UPREGULATION;

CYP24A1; CYP27B1; DCS; MACROPHAGES; VITAMIN D;

25-HYDROXYVITAMIN D3 1-ALPHA-HYDROXYLASE; CALCITRIOL; DENDRITIC CELLS; FEMALE; HOMEOSTASIS; HUMANS; LYMPHOCYTE ACTIVATION; MACROPHAGES; MALE; MONOCYTES; STEROID HYDROXYLASES; T-LYMPHOCYTES;

EID: 84901841829     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344157     Document Type: Article

References (42)

1. Mehta, S., Giovannucci, E. and Mugusi, F., Vitamin D status of HIV-infected women and its association with HIV disease progression, anemia, and mortality. PLoS One 2010. 5: 1-7.
2. Martineau, A. R., Timms, P. M., Bothamley, G. H., Hanifa, Y., Islam, K., Claxton, A. P., Packe, G. E. et al., High-dose vitamin D 3 during intensive-phase antimicrobial treatment of pulmonary tuberculosis: a double-blind randomised controlled trial. Lancet 2011. 377: 14-17.
3. Wilkinson, R. J., Llewelyn, M., Toossi, Z., Patel, P., Pasvol, G., Lalvani, A., Wright, D. et al., Early report Influence of vitamin D deficiency and vitamin D receptor polymorphisms on tuberculosis among Gujarati Asians in west London: a case-control study. Lancet 2000. 355: 618-621.
4. Martineau, A. R., Wilkinson, R. J., Wilkinson, K. A., Newton, S. M., Kampmann, B., Hall, B. M., Packe, G. E. et al., A single dose of vitamin D enhances immunity to mycobacteria. Am. J. Respir. Crit. Care Med. 2007. 176: 208-213.
5. Nikolic, T. and Roep, B. O., Regulatory multitasking of tolerogenic dendritic cells-lessons taken from vitamin D3-treated tolerogenic dendritic cells. Front. Immunol. 2013. 4: 113.
6. Hewison, M., Vitamin D and the intracrinology of innate immunity. Mol. Cell. Endocrinol. 2010. 321: 103-111.
7. Sakaki, T., Sawada, N., Komai, K., Shiozawa, S., Yamada, S., Yamamoto, K., Ohyama, Y. et al., Dual metabolic pathway of 25-hydroxyvitamin D3 catalyzed by human CYP24. Eur. J. Biochem. 2000. 267: 6158-6165.
8. Liu, P. T., Stenger, S., Li, H., Wenzel, L., Tan, B. H., Krutzik, S. R., Ochoa, M. T. et al., Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006. 311: 1770-1773.
9. Martineau, A. R., Wilkinson, K. A., Sandra, M., Floto, R. A., Norman, A. W., Davidson, R. N., Sørensen, O. E. et al., Suppression of Mycobacteria: the role of cathelicidin LL-37 1. J. Immunol. 2010. 178: 7190-7198.
10. Campbell, G. R. and Spector, S. A., Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog. 2012. 8: e1002689.
11. Fabri, M., Stenger, S., Shin, D.-M, Yuk, J.-M, Liu, P. T., Realegeno, S., Lee, H.-M. et al., Vitamin D is required for IFN-gamma-mediated antimicrobial activity of human macrophages. Sci. Transl. Med. 2011. 3: 104ra102.
12. Penna, G. and Adorini, L., 1 Alpha, 25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J. Immunol. 2000. 164: 2405-2411.
13. Pedersen, a. W., Holmstrøm, K., Jensen, S. S., Fuchs, D., Rasmussen, S., Kvistborg, P., Claesson, M. H. et al., Phenotypic and functional markers for 1 alpha, 25-dihydroxyvitamin D(3)-modified regulatory dendritic cells. Clin. Exp. Immunol. 2009. 157: 48-59.
14. Hollis, B., Assessment and interpretation of circulating 25-hydroxyvitamin D and 1, 25-dihydroxyvitamin D in the clinical environment. Endocrinol. Metab. Clin. North Am. 2010. 39: 1-16.
15. Szeles, L., Keresztes, G., Torocsik, D., Balajthy, Z., Krenacs, L., Poliska, S., Steinmeyer, A. et al., 1, 25-dihydroxyvitamin D3 is an autonomous regulator of the transcriptional changes leading to a tolerogenic dendritic cell phenotype. J. Immunol. 2009. 182: 2074-2083.
16. Gottfried, E., Rehli, M., Hahn, J., Holler, E., Andreesen, R. and Kreutz, M., Monocyte-derived cells express CYP27A1 and convert vitamin D3 into its active metabolite. Biochem. Biophys. Res. Commun. 2006. 349: 209-213.
17. Fritsche, J., Mondal, K., Ehrnsperger, A., Andreesen, R. and Kreutz, M., Regulation of 25-hydroxyvitamin D3-1 alpha-hydroxylase and production of 1 alpha, 25-dihydroxyvitamin D3 by human dendritic cells. Blood 2003. 102: 3314-3316.
18. Hewison, M., Freeman, L., Hughes, S. V, Evans, K. N., Bland, R., Eliopoulos, A. G., Kilby, M. D. et al., Differential regulation of vitamin D receptor and its ligand in human monocyte-derived dendritic cells. J. Immunol. 2003. 170: 5382-5390.
19. Jeffery, L. E., Wood, A. M., Qureshi, O. S., Hou, T. Z., Gardner, D., Briggs, Z., Kaur, S. et al., Availability of 25-hydroxyvitamin D3 to APCs controls the balance between regulatory and inflammatory T cell responses. J. Immunol. 2012. 189: 5155-5164.
20. Wu, S., Ren, S., Nguyen, L., Adams, J. S. and Hewison, M., Splice variants of the CYP27b1 gene and the regulation of 1, 25-dihydroxyvitamin D3 production. Endocrinology 2007. 148: 3410-3418.
21. Fischer, D., Thome, M., Becker, S., Cordes, T., Diedrich, K., Friedrich, M. and Thill, M., Expression of 25-hydroxyvitamin D3-24-hydroxylase in benign and malignant ovarian cell lines and tissue. Anticancer Res. 2009. 29: 3635-3639.
22. Muindi, J. R., Yu, W.-D., Ma, Y., Engler, K. L., Kong, R.-X., Trump, D. L. and Johnson, C. S., CYP24A1 inhibition enhances the antitumor activity of calcitriol. Endocrinology 2010. 151: 4301-4312.
23. Jeffery, L. E., Burke, F., Mura, M., Zheng, Y., Qureshi, O. S., Hewison, M., Walker, L. S. K. et al., 1, 25-Dihydroxyvitamin D3 and IL-2 combine to inhibit T cell production of inflammatory cytokines and promote development of regulatory T cells expressing CTLA-4 and FoxP3. J. Immunol. 2009. 183: 5458-5467.
24. Von Essen, M. R., Kongsbak, M., Schjerling, P., Olgaard, K., Odum, N. and Geisler, C., Vitamin D controls T cell antigen receptor signaling and activation of human T cells. Nat. Immunol. 2010. 11: 344-349.
25. Kleijwegt, F. S., Laban, S., Duinkerken, G., Joosten, A. M., Koeleman, B. P. C., Nikolic, T. and Roep, B. O., Transfer of regulatory properties from tolerogenic to proinflammatory dendritic cells via induced autoreactive regulatory T cells. J. Immunol. 2011. 187: 6357-6364.
26. Kleijwegt, F. S., Jansen, D. T. S. L., Teeler, J., Joosten, A. M., Laban, S., Nikolic, T. and Roep, B. O., Tolerogenic dendritic cells impede priming of naïve CD8(+) T cells and deplete memory CD8(+) T cells. Eur. J. Immunol. 2013. 43: 85-92.
27. Kleijwegt, F. S., Laban, S., Duinkerken, G., Joosten, A. M., Zaldumbide, A., Nikolic, T. and Roep, B. O., Critical role for TNF in the induction of human antigen-specific regulatory T cells by tolerogenic dendritic cells. J. Immunol. 2010. 185: 1412-1418.
28. Baeke, F., Korf, H., Overbergh, L., Verstuyf, A., Thorrez, L., Van Lommel, L., Waer, M. et al., The vitamin D analog, TX527, promotes a human CD4+CD25 high CD127 low regulatory T cell profile and induces a migratory signature specific for homing to sites of inflammation. J. Immunol. 2011. 186: 132-142.
29. Van der Aar, A. M. G., Sibiryak, D. S., Bakdash, G., van Capel, T. M. M., van der Kleij, H. P. M., Opstelten, D.-J. E., Teunissen, M. B. M. et al., Vitamin D3 targets epidermal and dermal dendritic cells for induction of distinct regulatory T cells. J. Allergy Clin. Immunol. 2011. 127: 1532-1540. e7.
30. Kang, S. W., Kim, S. H., Lee, N., Lee, W.-W., Hwang, K.-A., Shin, M. S., Lee, S.-H. et al., 1, 25-Dihyroxyvitamin D3 promotes FOXP3 expression via binding to vitamin D response elements in its conserved noncoding sequence region. J. Immunol. 2012. 188: 5276-5282.
31. Edfeldt, K., Liu, P. T., Chun, R., Fabri, M., Schenk, M., Wheelwright, M., Keegan, C. et al., T-cell cytokines differentially control human monocyte antimicrobial responses by regulating vitamin D metabolism. Proc. Natl. Acad. Sci. USA 2010. 107: 22593-22598.
32. Adorini, L., Tolerogenic dendritic cells induced by vitamin D receptor ligands enhance regulatory T cells inhibiting autoimmune diabetes. Ann. NY Acad. Sci. 2003. 987: 258-261.
33. Sochorová, K., Budinský, V., Rozková, D., Tobiasová, Z., Dusilová-Sulková, S., Spísek, R. and Bartůnková, J., Paricalcitol (19-nor-1, 25-dihydroxyvitamin D2) and calcitriol (1, 25-dihydroxyvitamin D3) exert potent immunomodulatory effects on dendritic cells and inhibit induction of antigen-specific T cells. Clin. Immunol. 2009. 133: 69-77.
34. Rogge, L., D'Ambrosio, D., Biffi, M., Penna, G., Minetti, L. J., Presky, D. H., Adorini, L. et al., The role of Stat4 in species-specific regulation of Th cell development by type I IFNs. J. Immunol. 1998. 161: 6567-6574.
35. Penna, G., Amuchastegui, S., Giarratana, N., Daniel, K. C., Vulcano, M., Sozzani, S. and Adorini, L., 1, 25-Dihydroxyvitamin D3 selectively modulates tolerogenic properties in myeloid but not plasmacytoid dendritic cells. J. Immunol. 2007. 178: 145-153.
36. Schrumpf, J. a., van Sterkenburg, M. A. J. A., Verhoosel, R. M., Zuyderduyn, S. and Hiemstra, P. S., Interleukin 13 exposure enhances vitamin D-mediated expression of the human cathelicidin antimicrobial peptide 18/LL-37 in bronchial epithelial cells. Infect. Immun. 2012. 80: 4485-4494.
37. Chun, R. F., Lauridsen, A. L., Suon, L., Zella, L. A., Pike, J. W., Modlin, R. L., Martineau, A. R. et al., Vitamin D-binding protein directs monocyte responses to 25-hydroxy- and 1, 25-dihydroxyvitamin D. J. Clin. Endocrinol. Metab. 2010. 95: 3368-3376.
38. Hidalgo, A. A., Deeb, K. K., Pike, J. W., Johnson, C. S. and Trump, D. L., Dexamethasone enhances 1alpha, 25-dihydroxyvitamin D3 effects by increasing vitamin D receptor transcription. J. Biol. Chem. 2011. 286: 36228-36237.
39. Zella, L. A., Shevde, N. K., Hollis, B. W., Cooke, N. E. and Pike, J. W., Vitamin D-binding protein influences total circulating levels of 1, 25-dihydroxyvitamin D3 but does not directly modulate the bioactive levels of the hormone in vivo. Endocrinology 2008. 149: 3656-3667.
40. Adams, J. S. and Gacad, M. A., Characterization of 1 alpha-hydroxylation of vitamin D3 sterols by cultured alveolar macrophages from patients with sarcoidosis. J. Exp. Med. 1985. 161: 755-765.
41. Tsang, J., Chain, B. M., Miller, R. F., Webb, B. L. J., Barclay, W., Towers, G. J., Katz, D. R. et al., HIV-1 infection of macrophages is dependent on evasion of innate immune cellular activation. AIDS 2009. 23: 2255-2263.
42. Le Bert, N., Chain, B. M., Rook, G. and Noursadeghi, M., DC priming by M. vaccae inhibits Th2 responses in contrast to specific TLR2 priming and is associated with selective activation of the CREB pathway. PLoS One 2011. 6: e18346.