Vitamin D metabolism and signaling in the immune system

Reviews in Endocrine and Metabolic Disorders

Volumn 13, Issue 1, 2012, Pages 21-29

  White, John H ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Adaptive immunity; Antimicrobial peptides; CYP27B1; Innate immunity; Macrophages; Pattern recognition receptors; Vitamin D; Vitamin D receptor

Indexed keywords

1,25 DIHYDROXYERGOCALCIFEROL; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CD14 ANTIGEN; CYTOCHROME P 450 27B1; CYTOCHROME P450; INTERLEUKIN 15; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; VITAMIN D; VITAMIN D RECEPTOR;

BIOSYNTHESIS; HOMEOSTASIS; IMMUNE SYSTEM; IMMUNOREGULATION; INFECTION; INNATE IMMUNITY; PATTERN RECOGNITION; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VITAMIN METABOLISM;

25-HYDROXYVITAMIN D3 1-ALPHA-HYDROXYLASE; ADAPTIVE IMMUNITY; ANIMALS; HUMANS; IMMUNE SYSTEM; IMMUNITY, INNATE; RECEPTORS, CALCITRIOL; VITAMIN D;

EID: 84858150326     PISSN: 13899155     EISSN: 15732606     Source Type: Journal    
DOI: 10.1007/s11154-011-9195-z     Document Type: Review

References (95)

1. Tavera-Mendoza L, White JH. Cell defenses and the sunshine vitamin. Sci Am. 2007;297:62-72. (Pubitemid 350195363)
2. Cheng JB, Levine MA, Bell NH, et al. Genetic evidence that the human CYP2R1 enzyme is a key vitamin D 25-hydroxylase. Proc Natl Acad Sci U S A. 2004;101:7711-5. (Pubitemid 38658094)
3. Holick MF. Vitamin D deficiency. New Engl J Med. 2007;357:266-81.
4. Prosser DE, Jones G. Enzymes involved in the activation and inactivation of vitamin D. Trends Biochem Sci. 2004;29:664-73. (Pubitemid 39491265)
5. Shinkyo R, Sakaki T, Kamakura M, et al. Metabolism of vitamin D by human microsomal CYP2R1. Biochem Biophys Res Commun. 2004;324:451-7. (Pubitemid 39311516)
6. Zehnder D, Bland R, Williams MC, et al. Extrarenal expression of 25-hydroxyvitamin d(3)-1 alpha-hydroxylase. J Clin Endocrinol Metab. 2001;86:888-94. (Pubitemid 32207511)
7. Hewison M, Burke F, Evans KN, et al. Extra-renal 25- hydroxyvitamin D3-1alpha-hydroxylase in human health and disease. J Ster Biochem Mol Biol. 2007;103:316-21. (Pubitemid 46420518)
8. Malabanan A, Veronikis IE, Holick MF. Redefining vitamin D insufficiency. Lancet. 1998;351:805-6. (Pubitemid 28112350)
9. Bischoff-Ferrari HA, Giovannucci E, Willett WC, et al. Estimation of optimal serum concentrations of 25-hydroxyvitamin D for multiple health outcomes. Am J Clin Nutr. 2006;84:18-28. (Pubitemid 44699167)
10. Holick MF. High prevalence of vitamin D inadequacy and implications for health. Mayo Clin Proc. 2006;81:353-73. (Pubitemid 43334631)
11. Chapuy MC, Preziosi P, Maamer M, et al. Prevalence of vitamin D insufficiency in an adult normal population. Osteoporos Int. 1997;7:439-43. (Pubitemid 27443069)
12. Thomas MK, Lloyd-Jones DM, Thadhani RI, et al. Hypovitaminosis D in medical inpatients. New Engl J Med. 1998;338:777-83. (Pubitemid 28135983)
13. Holick MF, Siris ES, Binkley N, et al. Prevalence of vitamin D inadequacy among postmenopausal North American women receiving osteoporosis therapy. J Clin Endocrinol Metab. 2005;90:3215-24. (Pubitemid 41014278)
14. Ross AC, Manson JE, Abrams SA, et al. The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. J Clin Endocrinol Metab. 2011;96:53-8.
15. Heaney RP, Holick MF. Why the IOM recommendations for vitamin D are deficient. J Bone Miner Res. 2011;26:455-7.
16. Slomski A. IOM endorses vitamin D, calcium only for bone health, dispels deficiency claims. JAMA. 2011;305:455-7.
17. Chawla A, Repa J, Evans RM, et al. Nuclear receptors and lipid physiology: opening the X-files. Science. 2001;294:1866-70. (Pubitemid 33101573)
18. Lin R, White JH. The pleiotropic actions of vitamin D. BioEssays. 2004;26:21-8. (Pubitemid 38095345)
19. Lin R, Nagai Y, Sladek R, et al. Expression profiling in squamous carcinoma cells reveals pleiotropic effects of vitamin D3 signaling on cell proliferation, differentiation and immune system regulation. Mol Endocrinol. 2002;16:1243-56. (Pubitemid 34621073)
20. Wang TT, Tavera-Mendoza L, Laperriere D, et al. Large-scale in silico and microarray-based genomic screening of 1,25-dihydroxyvitamin D3 target genes. Mol Endocrinol. 2005;19:2685-95. (Pubitemid 41577243)
21. Matthews D, LaPorta E, Zinser GM, et al. Genomic vitamin D signaling in breast cancer: insights from animal models and human cells. J Steroid Biochem Mol Biol. 2010;121:362-7.
22. Rochel N, Wurtz JM, Mitschler A, et al. The crystal structure of the nuclear receptor for vitamin D bound to its natural ligand. Mol Cell. 2000;5:173-9. (Pubitemid 30105446)
23. Drocourt L, Ourlin JC, Pascussi JM, et al. Expression of CYP3A4, CYP2B6, and CYP2C9 is regulated by the vitamin D receptor pathway in primary human hepatocytes. J Biol Chem. 2002;277:25125-32. (Pubitemid 34951818)
24. Thompson PD, Jurutka PW, Whitfield GK, et al. Liganded VDR induces CYP3A4 in small intestinal and colon cancer cells via DR3 and ER6 vitamin D responsive elements. Biochem Biophys Res Comm. 2002;299:730-8. (Pubitemid 36034548)
25. Thummel KE, Brimer C, Yasuda K, et al. Transcriptional control of intestinal cytochrome P-4503A by 1alpha,25-dihydroxyvitamin D3. Mol Pharmacol. 2001;60:1399-406. (Pubitemid 33144911)
26. Tavera-Mendoza L, Wang TT, Lallemant B, et al. Convergence of vitamin D and retinoic acid signaling at a common hormone response element. EMBO Rep. 2006;7:180-5.
27. 3 on IL-10 expression in monocytes is short-term down-regulation. Biochim Biophys Acta. 2010;1803:1276-86.
28. Dilworth FJ, Chambon P. Nuclear receptors coordinate the activities of chromatin remodeling complexes and coactivators to facilitate initiation of transcription. Oncogene. 2001;20:3047-54. (Pubitemid 32553559)
29. McKenna NJ, O'Malley BW. Combinatorial control of gene expression by nuclear receptors and coregulators. Cell. 2002;108:465-74. (Pubitemid 34260872)
30. Kim S, Yamazaki M, Zella LA, et al. Activation of receptor activator of NF-kappaB ligand gene expression by 1,25-dihydroxyvitamin D3 is mediated through multiple long-range enhancers. Mol Cell Biol. 2006;26:6469-86. (Pubitemid 44277887)
31. Meyer MB, Goetsch PD, Pike JW. A downstream intergenic cluster of regulatory enhancers contributes to the induction of CYP24A1 expression by 1alpha,25-dihydroxyvitamin D3. J Biol Chem. 2010;285:15599-610.
32. Takeuchi A, Reddy G, Kobayashi T, et al. Nuclear factor of activated T cells (NFAT) as a molecular target for 1,25-dihydroxyvitamin D3-mediated effects. J Immunol. 1998;160:209-18. (Pubitemid 28116731)
33. An B-S, Tavera-Mendoza LE, Dimitrov V, et al. Stimulation of SIRT1-regulated FoxO protein function by the ligand-bound vitamin D receptor. Mol Cell Biol. 2010;30:4890-900.
34. Masten AR. Sunlight in tuberculosis. Chest. 1935;1:8-23.
35. Guy RA. The history of cod liver oil as a remedy. Am J Dis Child. 1923;26:112-6.
36. Grad R. Cod and the consumptive: a brief history of cod-liver oil in the treatment of pulmonary tuberculosis. Pharm Hist. 2004;46:106-20.
37. Martineau AR, Honecker FU, Wilkinson RJ, Griffiths CJ. Vitamin D in the treatment of pulmonary tuberculosis. J Ster Biochem Mol Biol. 2007;103:793-8. (Pubitemid 46401341)
38. Rook GA, Steele J, Fraher L, Barker S, Karmali R, O'Riordan J, et al. Vitamin D3, interferon, and control of proliferation of mycobacterium tuberculosis by human monocytes. Immunol. 1986;57:159-63. (Pubitemid 16232232)
39. White JH. Vitamin D signaling, infectious diseases, and regulation of innate immunity. Infect Immun. 2008;76:3837-43.
40. Martineau AR, Timms PM, Bothamley GH, et al. High-dose vitamin D-3 during intensive-phase antimicrobial treatment of pulmonary tuberculosis: a double-blind randomised controlled trial. Lancet. 2011;377:242-50.
41. Urashima M, Segawa T, Okazaki M, et al. Randomized trial of vitamin D supplementation to prevent seasonal influenza A in schoolchildren. Am J Clin Nutr. 2010;91:1255-60.
42. Ichinohe T, Pang IK, Kumamoto Y, et al. Micobiota regulates immune defense against respiratory tract influenza A virus infection. Proc Nat Acad Sci U S A. 2011;108:5354-9.
43. Bhalla AK, Amento EP, Serog B, Glimcher LH. 1,25-Dihydroxyvitamin D3 inhibits antigen-induced T cell activation. J Immunol. 1984;133:1748-54. (Pubitemid 14035260)
44. Brennan A, Katz DR, Nunn JD, Barker S, et al. Dendritic cells from human tissues express receptors for the immunoregulatory vitamin D3 metabolite, dihydroxycholecalciferol. Immunol. 1987;61:457-61. (Pubitemid 17127352)
45. Adorini L, Penna G. Dendritic cell tolerogenicity: a key mechanism in immunomodulation by vitamin D receptor agonists. Human Immunol. 2009;70:345-52.
46. Baeke F, Takiishi T, Korf H, et al. Vitamin D: modulator of the immune system. Curr Opin Pharmacol. 2010;10:482-96.
47. Von Essen MR, Kongsbak M, Schjerling P, et al. Vitamin D controls T cell antigen receptor signaling and activation of human T cells. Nat Immunol. 2010;11:344-9.
48. Gorman S, Judge MA, Hart PH. Immune-modifying properties of topical vitamin D: focus on dendritic cell and T cells. J Ster Biochem Mol Biol. 2010;121:247-9.
49. Bowcock AM, Krueger JG. Getting under the skin: the immunogenetics of psoriasis. Nat Rev Immunol. 2005;5:699-711. (Pubitemid 43090738)
50. Prinz JC. From bench to bedside - translational research in psoriasis. J Eur Acad Dermatol Vernerol. 2010;24:1-4.
51. Solomon AJ, Whitham RH. Curr Neurol Neurosci Rep. 2010;10:389-96.
52. Hypponen E, Laara E, Reunanen E, et al. Intake of vitamin D and risk of type 1 diabetes: a birth-cohort study. Lancet. 2001;358:1500-3. (Pubitemid 33055701)
53. Jeffery LE, Burke F, Mura M, et al. 1,25-dihydroxyvitamin D- 3 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;183:5458-67.
54. Oberg F, Botlin J, Nilsson K. Functional antagonisms between vitamin-D3 and retinoic acid in the regulation of CD14 and CD23 expression during monocytic differentiation of U-937 cells. J Immunol. 1993;150:3487-95. (Pubitemid 23129729)
55. Wang TT, Nestel F, Bourdeau V, et al. Cutting edge: 1,25- dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J Immunol. 2004;173:2909-12. (Pubitemid 39141992)
56. Hancock REW, Sahl HG. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol. 2006;24:1551-7. (Pubitemid 44967479)
57. Doss M, White MR, Tecle T, Hartshorn KL. Human defensins and LL-37 in mucosal immunity. J Leuk Biol. 2010;87:79-92.
58. Liu PT, Krutzik SR, Modlin RL. Therapeutic implications of the TLR and VDR partnership. Trends Mol Med. 2007;13:117-24. (Pubitemid 46341960)
59. Gombart AF, Borregaard N, Koeffler HP. Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D-3. FASEB J. 2005;19:1067-77. (Pubitemid 40946432)
60. Liu PT, Stenger S, Li HY, et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science. 2006;311:1770-3.
61. Weber G, Heilborn JD, Chamorro Jimenez CI, et al. Vitamin D induces the antimicrobial protein hCAP18 in human skin. J Invest Dermatol. 2005;124:1080-2. (Pubitemid 40629115)
62. White JH. Vitamin D as an inducer of cathelicidin antimicrobial peptide expression: past, present and future. J Ster Biochem Mol Biol. 2010;121:234-8.
63. D'Aldebert E, Biyeyeme Bi Mve MJ, Mergey M, et al. Bile salts control the antimicrobial peptide cathelicidin through nuclear receptors in the human biliary epithelium. Gastroenterol. 2009;136:1435-43.
64. Makishima M, Lu TT, Xie W, et al. Vitamin D receptor as an intestinal bile acid sensor. Science. 2002;296:1313-6. (Pubitemid 34522785)
65. Gombart AF, Saito T, Koeffler HP. Exaptation of an ancient Alu short interspersed element provides a highly conserved vitamin D-mediated innate immune response in humans and primates. BMC Genomics. 2009;10:321.
66. Liu PT, Schenk M, Walker VP, et al. Convergence of IL-1 beta and VDR Activation Pathways in Human TLR2/1-Induced Antimicrobial Responses. PLoS ONE. 2009;4:e5810.
67. Wang TT, Dabbas B, Laperriere D, et al. Direct and indirect induction by 1,25-dihydroxyvitamin D3 of the NOD2/CARD15- beta defensin 2 innate immune pathway defective in Crohn's disease. J Biol Chem. 2010;285:2227-31.
68. Voss E, Wehkamp J, Wehkamp K, et al. NOD2/CARD15 mediates induction of the antimicrobial peptide human beta-defensin-2. J Biol Chem. 2006;281:2005-11. (Pubitemid 43845788)
69. Cho JH. The genetics and immunopathogenesis of inflammatory bowel disease. Nat Rev Immunol. 2008;8:458-66. (Pubitemid 351733422)
70. Fellermann K, Stange DE, Schaeffeler E, et al. Am J Hum Genet. 2006;79:439-48.
71. Coulombe F, Behr MA. Crohn's disease as an immune deficiency? Lancet. 2009;374:769-70.
72. Smith AM, Rahman FZ, Bu'Hussain H, et al. Disordered macrophage cytokine secretion underlies impaired acute inflammation and bacterial clearance in Crohn's disease. J Exp Med. 2009;206:1883-97.
73. Marks DJB, Rahman FZ, Sewell GW, et al. Crohn's disease: an immune deficiency state. Clin Rev Allergy Immunol. 2010;38:20-31.
74. Lim W-C, Hanauer SB, Li YC. Mechanisms of disease: vitamin D and inflammatory bowel disease. Nat Clin Pract Gastroenterol Hepatol. 2005;2:308-15. (Pubitemid 41102862)
75. Loftus Jr EV. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterol. 2004;126:1504-17. (Pubitemid 38649869)
76. Zeng L, Anderson FH. Seasonal change in the exacerbations of Crohn's disease. Scand J Gastroenterol. 1996;31:79-82. (Pubitemid 26018609)
77. Lewis JD, Aberra FN, Lichtenstein GR, et al. Seasonal variation in flares of inflammatory bowel disease. Gastroenterol. 2004;126:665-73. (Pubitemid 38298314)
78. Aratari A, Papi C, Galletti B, et al. Seasonal variations in onset of symptoms in Crohn's disease. Dig Liver Dis. 2006;38:319-23. (Pubitemid 44356190)
79. Simmons JD, Mullighan C, Welsh KL, Jelwell DP. Vitamin D receptor gene polymorphism: association with Crohn's disease susceptibility. Gut. 2000;47:211-4. (Pubitemid 30489764)
80. Hewison M. Vitamin D and the immune system: new perspectives on an old theme. Endocrinol Metab Clin N Am. 2010;39:365-79.
81. Kreutz M, Andreesen R, Krause SW, et al. 1,25-dihydroxyvitamin- D3 production and vitamin-D3 receptor expression are developmentally regulated during differentiation of human monocytes into macrophages. Blood. 1990;76:2457-61.
82. Hewison M, Freeman L, Hughes SV, et al. Differential regulation of the vitamin D receptor and its ligand in human monocyte-derived dendritic cells. J Immunol. 2003;170:5382-90. (Pubitemid 36617823)
83. Burke RR, Rybicki BA, Rao DS. Calcium and vitamin D in sarcoidosis: how to assess and manage. Sem Resp Crit Care. 2010;31:474-84.
84. Stoffels K, Overbergh L, Giulietti A, et al. Immune regulation of 25-hydroxyvitamin-D-3-1 alpha-hydroxylase in human monocytes. J Bone Min Res. 2006;21:37-47. (Pubitemid 43023225)
85. Evans KN, Taylor H, Zehnder D, et al. Increased expression of 25- hydroxyvitamin D-1 alpha-hydroxylase in dysgerminomas - a novel form of humoral hypercalcemia of malignancy. Am J Pathol. 2004;165:807-13. (Pubitemid 39129288)
86. Evans KN, Nguyen L, Chan J, et al. Effects of 25- hydroxyvitamin D-3 and 1,25-dihydroxyvitamin D-3 on cytokine production by human decidual cells. Biol Reprod. 2006;75:816-22. (Pubitemid 44845586)
87. Nesby-O'Dell S, Scanlon KS, Cogswell ME, et al. Hypovitaminosis D prevalence and determinants among African American and white women of reproductive age: Third National Health and Nutrition Examination Survey, 1988-1994. Am J Clin Nutr. 2002;76:187-92. (Pubitemid 34686565)
88. Stead WW, Senner JW, Reddick WT, Lofgren JP. Racial differences in sensitivity to infection by mycobacterium tuberculosis. N Engl J Med. 1990;322:422-7. (Pubitemid 20059510)
89. Krutzik SR, Hewison M, Liu PT, et al. IL-15 links TLR2/1- induced macrophage differentiation to the vitamin D-dependent antimicrobial pathway. J Immunol. 2008;181:7115-20.
90. Edfeldt K, Liu PT, Chun R, et al. T-cell cytokines differentially control human monocyte antimicrobial responses by regulating vitamin D metabolism. Proc Nat Acad Sci U S A. 2010;107:22593-8.
91. Akira S. Innate immunity to pathogens: diversity in receptors for microbial recognition. Immunol Rev. 2009;227:5-8.
92. Irazoqui JE, Urbach JM, Ausubel FM. Evolution of host innate defence: insights from caenorhabditis elegans and primitive invertebrates. Nat Rev Immunol. 2010;10:47-58.
93. Patil A, Hughes AL, Zhang G. Rapid evolution and diversification of mammalian α-defensins as revealed by comparative analysis of rodent and primate genomes. Physiol Genom. 2004;20:1-11.
94. Zanetti M. Cathelicidins: multifunctional peptides of the innate immunity. J Leuk Biol. 2004;75:39-48. (Pubitemid 38166778)
95. Kumar H, Kawai T, Akira S. Toll-like receptors and innate immunity. Biochem Biophys Res Comm. 2009;388:621-5.