Vitamin D up-regulates the vitamin D receptor by protecting it from proteasomal degradation in human CD4+ T cells

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Kongsbak, Martin ^a   Von Essen, Marina R ^a   Boding, Lasse ^a   Levring, Trine B ^a   Schjerling, Peter ^a,b   Lauritsen, Jens P H ^a   Woetmann, Anders ^a   Ødum, Niels ^a   Bonefeld, Charlotte M ^a   Geisler, Carsten ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b BISPEBJERG HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIFEDIOL; CALCITRIOL; MESSENGER RNA; PROTEASOME; VITAMIN D RECEPTOR; ANTIFUNGAL AGENT; CALCITRIOL RECEPTOR; CD4 ANTIGEN; CYTOCHROME P450 3A INHIBITOR; KETOCONAZOLE; LEPTOMYCIN B; PROTEASOME INHIBITOR; UNSATURATED FATTY ACID;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; PROTECTION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION; T LYMPHOCYTE ACTIVATION; CELL CULTURE; DRUG EFFECTS; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PROTEIN TRANSPORT; UPREGULATION;

ANTIFUNGAL AGENTS; ANTIGENS, CD4; CALCITRIOL; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOCHROME P-450 CYP3A INHIBITORS; FATTY ACIDS, UNSATURATED; HUMANS; KETOCONAZOLE; LYMPHOCYTE ACTIVATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTORS, CALCITRIOL; UP-REGULATION;

EID: 84900427919     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096695     Document Type: Article

References (72)

1. DeLuca HF (2004) Overview of general physiologic features and functions of vitamin D. Am J Clin Nutr 80: 1689S-1696S.
2. Nnoaham KE, Clarke A (2008) Low serum vitamin D levels and tuberculosis: a systematic review and meta-analysis. Int J Epidemiol 37: 113-119. (Pubitemid 351228619)
3. Hypponen E, Laara E, Reunanen A, Jarvelin MR, Virtanen SM (2001) Intake of vitamin D and risk of type 1 diabetes: a birth-cohort study. Lancet 358: 1500-1503. (Pubitemid 33055701)
4. Ascherio A, Munger KL, Simon KC (2010) Vitamin D and multiple sclerosis. Lancet Neurol 9: 599-612.
5. Simpson S Jr, Taylor B, Blizzard L, Ponsonby AL, Pittas F, et al. (2010) Higher 25-hydroxyvitamin D is associated with lower relapse risk in multiple sclerosis. Ann Neurol 68: 193-203.
6. Lemire JM, Ince A, Takashima M (1992) 1,25-Dihydroxyvitamin D3 attenuates the expression of experimental murine lupus of MRL/l mice. Autoimmunity 12: 143-148.
7. Zella JB, DeLuca HF (2003) Vitamin D and autoimmune diabetes. J Cell Biochem 88: 216-222. (Pubitemid 36119889)
8. Nagpal S, Na S, Rathnachalam R (2005) Noncalcemic actions of vitamin D receptor ligands. Endocr Rev 26: 662-687. (Pubitemid 41127276)
9. Bouillon R, Carmeliet G, Verlinden L, van EE, Verstuyf A, et al. (2008) Vitamin D and human health: lessons from vitamin D receptor null mice. Endocr Rev 29: 726-776.
10. Dorr J, Ohlraun S, Skarabis H, Paul F (2012) Efficacy of vitamin D supplementation in multiple sclerosis (EVIDIMS Trial): study protocol for a randomized controlled trial. Trials 13: 15.
11. Coussens AK, Wilkinson RJ, Hanifa Y, Nikolayevskyy V, Elkington PT, et al. (2012) Vitamin D accelerates resolution of inflammatory responses during tuberculosis treatment. Proc Natl Acad Sci U S A 109: 15449-15454.
12. Baker AR, McDonnell DP, Hughes M, Crisp TM, Mangelsdorf DJ, et al. (1988) Cloning and expression of full-length cDNA encoding human vitamin D receptor. Proc Natl Acad Sci U S A 85: 3294-3298.
13. Moore DD, Kato S, Xie W, Mangelsdorf DJ, Schmidt DR, et al. (2006) International Union of Pharmacology. LXII. The NR1H and NR1I receptors: constitutive androstane receptor, pregnene X receptor, farnesoid X receptor alpha, farnesoid X receptor beta, liver X receptor alpha, liver X receptor beta, and vitamin D receptor. Pharmacol Rev 58: 742-759. (Pubitemid 44833743)
14. Hsieh JC, Shimizu Y, Minoshima S, Shimizu N, Haussler CA, et al. (1998) Novel nuclear localization signal between the two DNA-binding zinc fingers in the human vitamin D receptor. J Cell Biochem 70: 94-109. (Pubitemid 28310923)
15. Prufer K, Racz A, Lin GC, Barsony J (2000) Dimerization with retinoid X receptors promotes nuclear localization and subnuclear targeting of vitamin D receptors. J Biol Chem 275: 41114-41123. (Pubitemid 32054941)
16. Klopot A, Hance KW, Peleg S, Barsony J, Fleet JC (2007) Nucleo-cytoplasmic cycling of the vitamin D receptor in the enterocyte-like cell line, Caco-2. J Cell Biochem 100: 617-628. (Pubitemid 46180526)
17. Haussler MR, Whitfield GK, Kaneko I, Haussler CA, Hsieh D, et al. (2013) Molecular mechanisms of vitamin D action. Calcif Tissue Int 92: 77-98.
18. Kerner SA, Scott RA, Pike JW (1989) Sequence elements in the human osteocalcin gene confer basal activation and inducible response to hormonal vitamin D3. Proc Natl Acad Sci U S A 86: 4455-4459. (Pubitemid 19164573)
19. Pike JW, Meyer MB, Bishop KA (2012) Regulation of target gene expression by the vitamin D receptor - an update on mechanisms. Rev Endocr Metab Disord 13: 45-55.
20. Walters MR, Rosen DM, Norman AW, Luben RA (1982) 1,25-Dihydroxyvitamin D receptors in an established bone cell line. Correlation with biochemical responses. J Biol Chem 257: 7481-7484. (Pubitemid 12002772)
21. Chen TL, Li JM, Ye TV, Cone CM, Feldman D (1986) Hormonal responses to 1,25-dihydroxyvitamin D3 in cultured mouse osteoblast-like cells - modulation by changes in receptor level. J Cell Physiol 126: 21-28. (Pubitemid 16147700)
22. Li XY, Boudjelal M, Xiao JH, Peng ZH, Asuru A, et al. (1999) 1,25-Dihydroxyvitamin D3 increases nuclear vitamin D3 receptors by blocking ubiquitin/proteasome-mediated degradation in human skin. Mol Endocrinol 13: 1686-1694. (Pubitemid 30645273)
23. Kongsbak M, Levring TB, Geisler C, von Essen MR (2013) The vitamin D receptor and T cell function. Front Immunol 4 (148): 1-10.
24. Costa EM, Hirst MA, Feldman D (1985) Regulation of 1,25-dihydroxyvitamin D3 receptors by vitamin D analogs in cultured mammalian cells. Endocrinology 117: 2203-2210. (Pubitemid 16194281)
25. Pan LC, Price PA (1987) Ligand-dependent regulation of the 1,25-dihydroxyvitamin D3 receptor in rat osteosarcoma cells. J Biol Chem 262: 4670-4675. (Pubitemid 17102836)
26. Healy KD, Frahm MA, DeLuca HF (2005) 1,25-Dihydroxyvitamin D3 upregulates the renal vitamin D receptor through indirect gene activation and receptor stabilization. Arch Biochem Biophys 433: 466-473. (Pubitemid 39592801)
27. Zella LA, Meyer MB, Nerenz RD, Lee SM, Martowicz ML, et al. (2010) Multifunctional enhancers regulate mouse and human vitamin D receptor gene transcription. Mol Endocrinol 24: 128-147.
28. Mangelsdorf DJ, Pike JW, Haussler MR (1987) Avian and mammalian receptors for 1,25-dihydroxyvitamin D3: in vitro translation to characterize size and hormone-dependent regulation. Proc Natl Acad Sci U S A 84: 354-358. (Pubitemid 17006193)
29. Tiosano D, Wildbaum G, Gepstein V, Verbitsky O, Weisman Y, et al. (2013) The role of vitamin D receptor in innate and adaptive immunity: a study in hereditary vitamin D-resistant rickets patients. J Clin Endocrinol Metab 98: 1685-1693.
30. Wiese RJ, Uhland-Smith A, Ross TK, Prahl JM, DeLuca HF (1992) Upregulation of the vitamin D receptor in response to 1,25-dihydroxyvitamin D3 results from ligand-induced stabilization. J Biol Chem 267: 20082-20086.
31. Santiso-Mere D, Sone T, Hilliard GM, Pike JW, McDonnell DP (1993) Positive regulation of the vitamin D receptor by its cognate ligand in heterologous expression systems. Mol Endocrinol 7: 833-839. (Pubitemid 23220633)
32. Davoodi F, Brenner RV, Evans SR, Schumaker LM, Shabahang M, et al. (1995) Modulation of vitamin D receptor and estrogen receptor by 1,25(OH)2-vitamin D3 in T-47D human breast cancer cells. J Steroid Biochem Mol Biol 54: 147-153.
33. Jaaskelainen T, Ryhanen S, Mahonen A, DeLuca HF, Maenpaa PH (2000) Mechanism of action of superactive vitamin D analogs through regulated receptor degradation. J Cell Biochem 76: 548-558. (Pubitemid 30083137)
34. Peleg S, Nguyen CV (2010) The importance of nuclear import in protection of the vitamin D receptor from polyubiquitination and proteasome-mediated degradation. J Cell Biochem 110: 926-934.
35. Kaiser MF, Heider U, Mieth M, Zang C, von M, I, et al. (2013) The proteasome inhibitor bortezomib stimulates osteoblastic differentiation of human osteoblast precursors via upregulation of vitamin D receptor signalling. Eur J Haematol 90: 263-272.
36. Murphy KM, Reiner SL (2002) The lineage decisions of helper T cells. Nat Rev Immunol 2: 933-944. (Pubitemid 37323214)
37. Littman DR, Rudensky AY (2010) Th17 and regulatory T cells in mediating and restraining inflammation. Cell 140: 845-858.
38. Thien R, Baier K, Pietschmann P, Peterlik M, Willheim M (2005) Interactions of 1 alpha,25-dihydroxyvitamin D3 with IL-12 and IL-4 on cytokine expression of human T lymphocytes. J Allergy Clin Immunol 116: 683-689. (Pubitemid 41267147)
39. van Etten E, Mathieu C (2005) Immunoregulation by 1,25-dihydroxyvitamin D3: basic concepts. J Steroid Biochem Mol Biol 97: 93-101.
40. Mora JR, Iwata M, von Andrian UH (2008) Vitamin effects on the immune system: vitamins A and D take centre stage. Nat Rev Immunol 8: 685-698.
41. Jeffery LE, Burke F, Mura M, Zheng Y, Qureshi OS, et al. (2009) 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 183: 5458-5467.
42. Correale J, Ysrraelit MC, Gaitan MI (2009) Immunomodulatory effects of Vitamin D in multiple sclerosis. Brain 132: 1146-1160.
43. Palmer MT, Lee YK, Maynard CL, Oliver JR, Bikle DD, et al. (2011) Lineage-specific effects of 1,25-dihydroxyvitamin D(3) on the development of effector CD4 T cells. J Biol Chem 286: 997-1004.
44. Peelen E, Knippenberg S, Muris AH, Thewissen M, Smolders J, et al. (2011) Effects of vitamin D on the peripheral adaptive immune system: a review. Autoimmun Rev 10: 733-743.
45. Joshi S, Pantalena LC, Liu XK, Gaffen SL, Liu H, et al. (2011) 1,25-dihydroxyvitamin D(3) ameliorates Th17 autoimmunity via transcriptional modulation of interleukin-17A. Mol Cell Biol 31: 3653-3669.
46. Urry Z, Chambers ES, Xystrakis E, Dimeloe S, Richards DF, et al. (2012) The role of 1alpha,25-dihydroxyvitamin D3 and cytokines in the promotion of distinct Foxp3+ and IL-10+ CD4+ T cells. Eur J Immunol 42: 2697-2708.
47. Provvedini DM, Tsoukas CD, Deftos LJ, Manolagas SC (1983) 1,25-dihydroxyvitamin D3 receptors in human leukocytes. Science 221: 1181-1183.
48. Bhalla AK, Amento EP, Clemens TL, Holick MF, Krane SM (1983) Specific high-affinity receptors for 1,25-dihydroxyvitamin D3 in human peripheral blood mononuclear cells: presence in monocytes and induction in T lymphocytes following activation. J Clin Endocrinol Metab 57: 1308-1310. (Pubitemid 14209439)
49. Provvedini DM, Manolagas SC (1989) 1 Alpha,25-dihydroxyvitamin D3 receptor distribution and effects in subpopulations of normal human T lymphocytes. J Clin Endocrinol Metab 68: 774-779. (Pubitemid 19089008)
50. Kizaki M, Norman AW, Bishop JE, Lin CW, Karmakar A, et al. (1991) 1,25-Dihydroxyvitamin D3 receptor RNA: expression in hematopoietic cells. Blood 77: 1238-1247.
51. Yu XP, Mocharla H, Hustmyer FG, Manolagas SC (1991) Vitamin D receptor expression in human lymphocytes. Signal requirements and characterization by western blots and DNA sequencing. J Biol Chem 266: 7588-7595. (Pubitemid 21906406)
52. Yu XP, Hustmyer FG, Garvey WT, Manolagas SC (1991) Demonstration of a 1,25-dihydroxyvitamin D3-responsive protein in human lymphocytes: immunologic crossreactivity and inverse regulation with the vitamin D receptor. Proc Natl Acad Sci U S A 88: 8347-8351. (Pubitemid 21915353)
53. Chen L, Cencioni MT, Angelini DF, Borsellino G, Battistini L, et al. (2005) Transcriptional profiling of gamma delta T cells identifies a role for vitamin D in the immunoregulation of the V gamma 9V delta 2 response to phosphatecontaining ligands. J Immunol 174: 6144-6152. (Pubitemid 40663804)
54. von Essen MR, Kongsbak M, Schjerling P, Olgaard K, Odum N, et al. (2010) Vitamin D controls T cell antigen receptor signaling and activation of human T cells. Nat Immunol 11: 344-349.
55. Baeke F, Korf H, Overbergh L, van EE, Verstuyf A, et al. (2010) Human T lymphocytes are direct targets of 1,25-dihydroxyvitamin D(3) in the immune system. J Steroid Biochem Mol Biol.
56. Joseph RW, Bayraktar UD, Kim TK, St John LS, Popat U, et al. (2012) Vitamin D receptor upregulation in alloreactive human T cells. Hum Immunol 73: 693-698.
57. Veldman CM, Cantorna MT, DeLuca HF (2000) Expression of 1,25-dihydroxyvitamin D(3) receptor in the immune system. Arch Biochem Biophys 374: 334-338. (Pubitemid 30120270)
58. Diaz L, Martinez-Reza I, Garcia-Becerra R, Gonzalez L, Larrea F, et al. (2011) Calcitriol stimulates prolactin expression in non-activated human peripheral blood mononuclear cells: breaking paradigms. Cytokine 55: 188-194.
59. Nielsen MM, Lovato P, Macleod AS, Witherden DA, Skov L, et al. (2014) IL-1beta-Dependent Activation of Dendritic Epidermal T Cells in Contact Hypersensitivity. J Immunol.
60. Dietrich J, Geisler C (1998) T cell receptor zeta allows stable expression of receptors containing the CD3c leucine-based receptor-sorting motif. J Biol Chem 273: 26281-26284. (Pubitemid 28471626)
61. Feldman D, Pike JW, Glowacki J (2011) Vitamin D. Burlington: Elsevier Academic Press.
62. Jeffery LE, Wood AM, Qureshi OS, Hou TZ, Gardner D, et al. (2012) Availability of 25-hydroxyvitamin D(3) to APCs controls the balance between regulatory and inflammatory T cell responses. J Immunol 189: 5155-5164.
63. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, et al. (2006) Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311: 1770-1773.
64. von Mikecz A (2006) The nuclear ubiquitin-proteasome system. J Cell Sci 119: 1977-1984.
65. Schwartz AL, Ciechanover A (2009) Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu Rev Pharmacol Toxicol 49: 73-96.
66. Freedman DA, Levine AJ (1998) Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol Cell Biol 18: 7288-7293. (Pubitemid 28533048)
67. Prufer K, Barsony J (2002) Retinoid X receptor dominates the nuclear import and export of the unliganded vitamin D receptor. Mol Endocrinol 16: 1738-1751. (Pubitemid 34828085)
68. Hutten S, Kehlenbach RH (2007) CRM1-mediated nuclear export: to the pore and beyond. Trends Cell Biol 17: 193-201. (Pubitemid 46507806)
69. Wang Y, Becklund BR, DeLuca HF (2010) Identification of a highly specific and versatile vitamin D receptor antibody. Arch Biochem Biophys 494: 166-177.
70. Dame MC, Pierce EA, Prahl JM, Hayes CE, DeLuca HF (1986) Monoclonal antibodies to the porcine intestinal receptor for 1,25-dihydroxyvitamin D3: interaction with distinct receptor domains. Biochemistry 25: 4523-4534. (Pubitemid 16010187)
71. Masuyama H, MacDonald PN (1998) Proteasome-mediated degradation of the vitamin D receptor (VDR) and a putative role for SUG1 interaction with the AF-2 domain of VDR. J Cell Biochem 71: 429-440. (Pubitemid 28516333)
72. Chi Y, Hong Y, Zong H, Wang Y, Zou W, et al. (2009) CDK11p58 represses vitamin D receptor-mediated transcriptional activation through promoting its ubiquitin-proteasome degradation. Biochem Biophys Res Commun 386: 493-498.