Vitamin D and 1,25(OH)2D regulation of T cells

Nutrients

Volumn 7, Issue 4, 2015, Pages 3011-3021

  Cantorna, Margherita T ^a   Snyder, Lindsay ^a   Lin, Yang Ding ^a   Yang, Linlin ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

T cells; Vitamin D; Vitamin D receptor

Indexed keywords

1,25 DIHYDROXY VITAMIN D; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 22; INTERLEUKIN 4; UNCLASSIFIED DRUG; VITAMIN D; 1,25-DIHYDROXYERGOCALCIFEROL; CALCITRIOL RECEPTOR; ERGOCALCIFEROL; INTERLEUKIN 10 RECEPTOR;

ASTHMA; BONE METABOLISM; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL CYCLE REGULATION; CELL DIVISION; CELL EXPANSION; CELL GROWTH; CELL PROLIFERATION; CELLULAR DISTRIBUTION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC TRANSCRIPTION; HUMAN; INFECTION; INFLAMMATORY BOWEL DISEASE; MULTIPLE SCLEROSIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; METABOLISM; MOUSE; NATURAL KILLER CELL;

MURINAE; MUS;

ANIMALS; CELL PROLIFERATION; ERGOCALCIFEROLS; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-17; INTERLEUKIN-4; KILLER CELLS, NATURAL; MICE; RECEPTORS, CALCITRIOL; RECEPTORS, INTERLEUKIN-10; T-LYMPHOCYTES, REGULATORY; VITAMIN D;

EID: 84929377526     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu7043011     Document Type: Review

References (61)

1. Reeve, L.; Tanaka, Y.; DeLuca, H. F. Studies on the site of 1, 25-dihydroxyvitamin d3 synthesis in vivo. J. Biol. Chem. 1983, 258, 3615-3617.
2. Christakos, S.; Ajibade, D. V.; Dhawan, P.; Fechner, A. J.; Mady, L. J. Vitamin D: Metabolism. Rheum. Dis. Clin. N. Am. 2012, 38, 1-11, vii.
3. DeLuca, H. F. Overview of general physiologic features and functions of vitamin d. Am. J. Clin. Nutr. 2004, 80, 1689S-1696S.
4. Pike, J. W.; Meyer, M. B. Fundamentals of vitamin d hormone-regulated gene expression. J. Steroid Biochem. Mol. Biol. 2014, 144 (Pt. A), 5-11.
5. Grant, W. B.; Holick, M. F. Benefits and requirements of vitamin d for optimal health: A review. Altern. Med. Rev. 2005, 10, 94-111.
6. Veldman, C. M.; Cantorna, M. T.; DeLuca, H. F. Expression of 1, 25-dihydroxyvitamin d(3) receptor in the immune system. Arch. Biochem. Biophys. 2000, 374, 334-338.
7. Swain, S. L.; McKinstry, K. K.; Strutt, T. M. Expanding roles for cd4(+) t cells in immunity to viruses. Nat. Rev. Immunol. 2012, 12, 136-148.
8. Hsieh, C. S.; Macatonia, S. E.; Tripp, C. S.; Wolf, S. F.; O'Garra, A.; Murphy, K. M. Development of th1 cd4+ t cells through il-12 produced by listeria-induced macrophages. Science 1993, 260, 547-549.
9. Haanen, J. B.; de Waal Malefijt, R.; Res, P. C.; Kraakman, E. M.; Ottenhoff, T. H.; de Vries, R. R.; Spits, H. Selection of a human t helper type 1-like t cell subset by mycobacteria. J. Exp. Med. 1991, 174, 583-592.
10. Maizels, R. M.; Hewitson, J. P.; Smith, K. A. Susceptibility and immunity to helminth parasites. Curr. Opin. Immunol. 2012, 24, 459-466.
11. Weaver, C. T.; Elson, C. O.; Fouser, L. A.; Kolls, J. K. The th17 pathway and inflammatory diseases of the intestines, lungs, and skin. Annu. Rev. Pathol. 2013, 8, 477-512.
12. Ishigame, H.; Kakuta, S.; Nagai, T.; Kadoki, M.; Nambu, A.; Komiyama, Y.; Fujikado, N.; Tanahashi, Y.; Akitsu, A.; Kotaki, H.; et al. Differential roles of interleukin-17a and-17f in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009, 30, 108-119.
13. Matsuda, J. L.; Mallevaey, T.; Scott-Browne, J.; Gapin, L. Cd1d-restricted inkt cells, the 'swiss-army knife' of the immune system. Curr. Opin. Immunol. 2008, 20, 358-368.
14. Gratz, I. K.; Campbell, D. J. Organ-specific and memory treg cells: Specificity, development, function, and maintenance. Front. Immunol. 2014, 5, 333.
15. Iwamura, C.; Nakayama, T. Role of nkt cells in allergic asthma. Curr. Opin. Immunol. 2010, 22, 807-813.
16. Rigby, W. F.; Stacy, T.; Fanger, M. W. Inhibition of t lymphocyte mitogenesis by 1, 25-dihydroxyvitamin d3 (calcitriol). J. Clin. Investig. 1984, 74, 1451-1455.
17. Provvedini, D. M.; Tsoukas, C. D.; Deftos, L. J.; Manolagas, S. C. 1, 25-dihydroxyvitamin d3 receptors in human leukocytes. Science 1983, 221, 1181-1183.
18. Tsoukas, C. D.; Provvedini, D. M.; Manolagas, S. C. 1, 25-dihydroxyvitamin d3: A novel immunoregulatory hormone. Science 1984, 224, 1438-1440.
19. Palmer, M. T.; Lee, Y. K.; Maynard, C. L.; Oliver, J. R.; Bikle, D. D.; Jetten, A. M.; Weaver, C. T. Lineage-specific effects of 1, 25-dihydroxyvitamin d(3) on the development of effector cd4 t cells. J. Biol. Chem. 2011, 286, 997-1004.
20. Boonstra, A.; Barrat, F. J.; Crain, C.; Heath, V. L.; Savelkoul, H. F.; O'Garra, A. 1alpha, 25-dihydroxyvitamin d3 has a direct effect on naive cd4(+) t cells to enhance the development of th2 cells. J. Immunol. 2001, 167, 4974-4980.
21. Mahon, B. D.; Wittke, A.; Weaver, V.; Cantorna, M. T. The targets of vitamin d depend on the differentiation and activation status of cd4 positive t cells. J. Cell. Biochem. 2003, 89, 922-932.
22. Pichler, J.; Gerstmayr, M.; Szepfalusi, Z.; Urbanek, R.; Peterlik, M.; Willheim, M. 1alpha, 25(oh)2d3 inhibits not only th1 but also th2 differentiation in human cord blood t cells. Pediatr. Res. 2002, 52, 12-18.
23. Staeva-Vieira, T. P.; Freedman, L. P. 1, 25-dihydroxyvitamin d3 inhibits ifn-gamma and il-4 levels during in vitro polarization of primary murine cd4+ t cells. J. Immunol. 2002, 168, 1181-1189.
24. Korf, H.; Wenes, M.; Stijlemans, B.; Takiishi, T.; Robert, S.; Miani, M.; Eizirik, D. L.; Gysemans, C.; Mathieu, C. 1, 25-dihydroxyvitamin d(3) curtails the inflammatory and t cell stimulatory capacity of macrophages through an il-10-dependent mechanism. Immunobiology. 2012, 217, 1292-1300.
25. Sigmundsdottir, H.; Pan, J.; Debes, G. F.; Alt, C.; Habtezion, A.; Soler, D.; Butcher, E. C. Dcs metabolize sunlight-induced vitamin d3 to 'program' t cell attraction to the epidermal chemokine ccl27. Nat. Immunol. 2007, 8, 285-293.
26. Chen, J.; Bruce, D.; Cantorna, M. T. Vitamin d receptor expression controls proliferation of naive cd8+ t cells and development of cd8 mediated gastrointestinal inflammation. BMC Immunol. 2014, 15, 6.
27. Rigby, W. F.; Yirinec, B.; Oldershaw, R. L.; Fanger, M. W. Comparison of the effects of 1, 25-dihydroxyvitamin d3 on t lymphocyte subpopulations. Eur. J. Immunol. 1987, 17, 563-566.
28. Yuzefpolskiy, Y.; Baumann, F. M.; Penny, L. A.; Studzinski, G. P.; Kalia, V.; Sarkar, S. Vitamin d receptor signals regulate effector and memory cd8 t cell responses to infections in mice. J. Nutr. 2014, 144, 2073-2082.
29. Bruce, D.; Cantorna, M. T. Intrinsic requirement for the vitamin d receptor in the development of cd8alphaalpha-expressing t cells. J. Immunol. 2011, 186, 2819-2825.
30. Yu, S.; Cantorna, M. T. The vitamin d receptor is required for inkt cell development. Proc. Natl. Acad. Sci. USA 2008, 105, 5207-5212.
31. Yu, S.; Cantorna, M. T. Epigenetic reduction in invariant nkt cells following in utero vitamin d deficiency in mice. J. Immunol. 2011, 186, 1384-1390.
32. Waddell, A.; Zhao, J.; Cantorna, M. T. Natural killer t cells can help mediate the protective effects of 1, 25-dihydroxyvitamin d3 in experimental autoimmune encephalomyelitis in mice. Int. Immunol. 2015, in press.
33. Zella, J. B.; McCary, L. C.; DeLuca, H. F. Oral administration of 1, 25-dihydroxyvitamin d3 completely protects nod mice from insulin-dependent diabetes mellitus. Arch. Biochem. Biophys. 2003, 417, 77-80.
34. Gregori, S.; Giarratana, N.; Smiroldo, S.; Uskokovic, M.; Adorini, L. A 1alpha, 25-dihydroxyvitamin d(3) analog enhances regulatory t-cells and arrests autoimmune diabetes in nod mice. Diabetes 2002, 51, 1367-1374.
35. Cantorna, M. T.; Munsick, C.; Bemiss, C.; Mahon, B. D. 1, 25-dihydroxycholecalciferol prevents and ameliorates symptoms of experimental murine inflammatory bowel disease. J. Nutr. 2000, 130, 2648-2652.
36. Froicu, M.; Zhu, Y.; Cantorna, M. T. Vitamin d receptor is required to control gastrointestinal immunity in il-10 knockout mice. Immunology 2006, 117, 310-318.
37. Cantorna, M. T.; Humpal-Winter, J.; DeLuca, H. F. In vivo upregulation of interleukin-4 is one mechanism underlying the immunoregulatory effects of 1, 25-dihydroxyvitamin d(3). Arch. Biochem. Biophys. 2000, 377, 135-138.
38. Spach, K. M.; Nashold, F. E.; Dittel, B. N.; Hayes, C. E. Il-10 signaling is essential for 1, 25-dihydroxyvitamin d3-mediated inhibition of experimental autoimmune encephalomyelitis. J. Immunol. 2006, 177, 6030-6037.
39. Cantorna, M. T. Vitamin d, multiple sclerosis and inflammatory bowel disease. Arch. Biochem. Biophys. 2012, 523, 103-106.
40. Cantorna, M. T.; McDaniel, K.; Bora, S.; Chen, J.; James, J. Vitamin d, immune regulation, the microbiota, and inflammatory bowel disease. Exp. Biol. Med. (Maywood) 2014, 239, 1524-1530.
41. Ooi, J. H.; Chen, J.; Cantorna, M. T. Vitamin d regulation of immune function in the gut: Why do t cells have vitamin d receptors? Mol. Aspects Med. 2012, 33, 77-82.
42. Colin, E. M.; Asmawidjaja, P. S.; van Hamburg, J. P.; Mus, A. M.; van Driel, M.; Hazes, J. M.; van Leeuwen, J. P.; Lubberts, E. 1, 25-dihydroxyvitamin d3 modulates th17 polarization and interleukin-22 expression by memory t cells from patients with early rheumatoid arthritis. Arthritis Rheum 2010, 62, 132-142.
43. Van der Eerden, B. C.; van der Heyden, J. C.; van Hamburg, J. P.; Schreuders-Koedam, M.; Asmawidjaja, P. S.; de Muinck Keizer-Schrama, S. M.; Boot, A. M.; Lubberts, E.; Drop, S. L.; van Leeuwen, J. P. A human vitamin d receptor mutation causes rickets and impaired th1/th17 responses. Bone 2014, 69, 6-11.
44. Keating, P.; Munim, A.; Hartmann, J. X. Effect of vitamin d on t-helper type 9 polarized human memory cells in chronic persistent asthma. Ann. Allergy Asthma Immunol. Off. Publ. Am. Coll. Allergy Asthma Immunol. 2014, 112, 154-162.
45. Zhong, H.; Zhou, X. J.; Hong, J. G. The effects of vitamin d on allergen-induced expression of interleukin-13 and interleukin-17 in cord blood cd4(+)t cells. Iran. J. Allergy Asthma Immunol. 2014, 13, 93-97.
46. Yu, S.; Zhao, J.; Cantorna, M. T. Invariant nkt cell defects in vitamin d receptor knockout mice prevents experimental lung inflammation. J. Immunol. 2011, 187, 4907-4912.
47. Wittke, A.; Chang, A.; Froicu, M.; Harandi, O. F.; Weaver, V.; August, A.; Paulson, R. F.; Cantorna, M. T. Vitamin d receptor expression by the lung micro-environment is required for maximal induction of lung inflammation. Arch. Biochem. Biophys. 2007, 460, 306-313.
48. Akbari, O.; Stock, P.; Meyer, E.; Kronenberg, M.; Sidobre, S.; Nakayama, T.; Taniguchi, M.; Grusby, M. J.; DeKruyff, R. H.; Umetsu, D. T. Essential role of nkt cells producing il-4 and il-13 in the development of allergen-induced airway hyperreactivity. Nat. Med. 2003, 9, 582-588.
49. Wittke, A.; Weaver, V.; Mahon, B. D.; August, A.; Cantorna, M. T. Vitamin d receptor-deficient mice fail to develop experimental allergic asthma. J. Immunol. 2004, 173, 3432-3436.
50. Matheu, V.; Back, O.; Mondoc, E.; Issazadeh-Navikas, S. Dual effects of vitamin d-induced alteration of th1/th2 cytokine expression: Enhancing ige production and decreasing airway eosinophilia in murine allergic airway disease. J. Allergy Clin. Immunol. 2003, 112, 585-592.
51. Topilski, I.; Flaishon, L.; Naveh, Y.; Harmelin, A.; Levo, Y.; Shachar, I. The anti-inflammatory effects of 1, 25-dihydroxyvitamin d3 on th2 cells in vivo are due in part to the control of integrin-mediated t lymphocyte homing. Eur. J. Immunol. 2004, 34, 1068-1076.
52. Gorman, S.; Judge, M. A.; Burchell, J. T.; Turner, D. J.; Hart, P. H. 1, 25-dihydroxyvitamin d3 enhances the ability of transferred cd4+ cd25+ cells to modulate t helper type 2-driven asthmatic responses. Immunology 2010, 130, 181-192.
53. Gorman, S.; Judge, M. A.; Hart, P. H. Topical 1, 25-dihydroxyvitamin d3 subverts the priming ability of draining lymph node dendritic cells. Immunology 2010, 131, 415-425.
54. Taher, Y. A.; van Esch, B. C.; Hofman, G. A.; Henricks, P. A.; van Oosterhout, A. J. 1alpha, 25-dihydroxyvitamin d3 potentiates the beneficial effects of allergen immunotherapy in a mouse model of allergic asthma: Role for il-10 and tgf-beta. J. Immunol. 2008, 180, 5211-5221.
55. Rigby, W. F.; Noelle, R. J.; Krause, K.; Fanger, M. W. The effects of 1, 25-dihydroxyvitamin d3 on human t lymphocyte activation and proliferation: A cell cycle analysis. J. Immunol. 1985, 135, 2279-2286.
56. Joshi, S.; Pantalena, L. C.; Liu, X. K.; Gaffen, S. L.; Liu, H.; Rohowsky-Kochan, C.; Ichiyama, K.; Yoshimura, A.; Steinman, L.; Christakos, S.; et al. 1, 25-dihydroxyvitamin d3 ameliorates th17 autoimmunity via transcriptional modulation of interleukin-17a. Mol. Cell. Biol. 2011, 31, 3653-3669.
57. Kongsbak, M.; von Essen, M. R.; Boding, L.; Levring, T. B.; Schjerling, P.; Lauritsen, J. P.; Woetmann, A.; Odum, N.; Bonefeld, C. M.; Geisler, C. Vitamin d up-regulates the vitamin d receptor by protecting it from proteasomal degradation in human cd4+ t cells. PLoS ONE 2014, 9, e96695.
58. Healy, K. D.; Frahm, M. A.; DeLuca, H. F. 1, 25-dihydroxyvitamin d3 up-regulates the renal vitamin d receptor through indirect gene activation and receptor stabilization. Arch. Biochem. Biophys. 2005, 433, 466-473.
59. Ooi, J. H.; McDaniel, K. L.; Weaver, V.; Cantorna, M. T. Murine cd8+ t cells but not macrophages express the vitamin d 1alpha-hydroxylase. J. Nutr. Biochem. 2014, 25, 58-65.
60. Kongsbak, M.; von Essen, M. R.; Levring, T. B.; Schjerling, P.; Woetmann, A.; Odum, N.; Bonefeld, C. M.; Geisler, C. Vitamin d-binding protein controls t cell responses to vitamin d. BMC Immunol. 2014, 15, 35.
61. Barrat, F. J.; Cua, D. J.; Boonstra, A.; Richards, D. F.; Crain, C.; Savelkoul, H. F.; de Waal-Malefyt, R.; Coffman, R. L.; Hawrylowicz, C. M.; O'Garra, A. In vitro generation of interleukin 10-producing regulatory cd4(+) t cells is induced by immunosuppressive drugs and inhibited by t helper type 1 (th1)-and th2-inducing cytokines. J. Exp. Med. 2002, 195, 603-616.