Immunological role of vitamin D at the maternal-fetal interface

Journal of Endocrinology

Volumn 224, Issue 3, 2015, Pages R107-R121

  Tamblyn, J A ^a   Hewison, M ^a   Wagner, C L ^b   Bulmer, J N ^c   Kilby, M D ^a,d  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d BIRMINGHAM CHILDREN S HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Decidua; Fetal maternal interface; Immunity; Monocyte; T cell; Uterine natural killer cell; Vitamin D

Indexed keywords

VITAMIN D;

ADAPTIVE IMMUNITY; B LYMPHOCYTE; DECIDUA; DENDRITIC CELL; HUMAN; IMMUNOMODULATION; INNATE IMMUNITY; MACROPHAGE; MOTHER FETUS RELATIONSHIP; NATURAL KILLER CELL; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; VITAMIN D DEFICIENCY; VITAMIN D METABOLISM; ANIMAL; CYTOLOGY; FEMALE; FETOMATERNAL TRANSFUSION; IMMUNE SYSTEM; IMMUNOLOGY; PHYSIOLOGY; PLACENTA; UTERUS;

ANIMALS; DECIDUA; FEMALE; HUMANS; IMMUNE SYSTEM; MACROPHAGES; MATERNAL-FETAL EXCHANGE; PLACENTA; PREGNANCY; UTERUS; VITAMIN D;

EID: 84924765095     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0642     Document Type: Review

References (159)

1. Abbas AK, Murphy KM&Sher A 1996 Functional diversity of helper T lymphocytes. Nature 383 787-793. (doi:10.1038/383787a0)
2. Adams JS&Hewison M 2008 Unexpected actions of vitamin D: new perspectives on the regulation of innate and adaptive immunity. Nature Clinical Practice. Endocrinology&Metabolism 4 80-90. (doi:10.1038/ncpendmet0716)
3. Adams JS, Ren S, Liu PT, Chun RF, Lagishetty V, Gombart AF, Borregaard N, Modlin RL&Hewison M 2009 Vitamin D-directed rheostatic regulation of monocyte antibacterial responses. Journal of Immunology 182 4289-4295. (doi:10.4049/jimmunol.0803736)
4. Adorini L, Penna G, Giarratana N, Roncari A, Amuchastegui S, Daniel KC & Uskokovic M 2004 Dendritic cells as key targets for immunomodulation by vitamin D receptor ligands. Journal of Steroid Biochemistry and Molecular Biology 89-90 437-441. (doi:10.1016/j.jsbmb.2004.03.013)
5. Alijotas-Reig J, Llurba E&Gris JM 2014 Potentiating maternal immune tolerance in pregnancy: a new challenging role for regulatory T cells. Placenta 35 241-248. (doi:10.1016/j.placenta.2014.02.004)
6. Arck PC&Hecher K 2013 Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nature Medicine 19 548-556. (doi:10.1038/nm.3160)
7. Arck P, Solano ME, Maciej K&Robertson S 2013 Reproductive immunology: piece by piece. Journal of Reproductive Immunology 97 1. (doi:10.1016/j.jri.2013.02.001)
8. Askelund K, Liddell HS, Zanderigo AM, Fernando NS, Khong TY, Stone PR & Chamley LW 2004 CD83(C)dendritic cells in the decidua of women with recurrent miscarriage and normal pregnancy. Placenta 25 140-145. (doi:10.1016/S0143-4004(03)00182-6)
9. Athanassakis I&Vassiliadis S 2002 Interplay between T helper type 1 and type 2 cytokines and soluble major histocompatibility complex molecules: a paradigm in pregnancy. Immunology 107 281-287. (doi:10.1046/j.1365-2567.2002.01518.x)
10. Bacchetta J, Sea JL, Chun RF, Lisse TS, Wesseling-Perry K, Gales B, Adams JS, Salusky IB&Hewison M 2013 Fibroblast growth factor 23 inhibits extrarenal synthesis of 1,25-dihydroxyvitamin D in human monocytes. Journal of Bone and Mineral Research 28 46-55. (doi:10.1002/jbmr.1740)
11. Bacchetta J, Zaritsky JJ, Sea JL, Chun RF, Lisse TS, Zavala K, Nayak A, Wesseling-Perry K, Westerman M, Hollis BW et al. 2014 Suppression of iron-regulatory hepcidin by vitamin D. Journal of the American Society of Nephrology 25 564-572. (doi:10.1681/ASN.2013040355)
12. Baeke F, Takiishi T, Korf H, Gysemans C&Mathieu C 2010 Vitamin D: modulator of the immune system. Current Opinion in Pharmacology 10 482-496. (doi:10.1016/j.coph.2010.04.001)
13. Bates MD, Quenby S, Takakuwa K, Johnson PM&Vince GS 2002 Aberrant cytokine production by peripheral blood mononuclear cells in recurrent pregnancy loss? Human Reproduction 17 2439-2444. (doi:10.1093/humrep/17.9.2439)
14. Bettelli E, Korn T&Kuchroo VK 2007 Th17: the third member of the effector T cell trilogy. Current Opinion in Immunology 19 652-657. (doi:10.1016/j.coi.2007.07.020)
15. Blois SM, Alba Soto CD, Tometten M, Klapp BF, Margni RA&Arck PC 2004 Lineage, maturity, and phenotype of uterine murine dendritic cells throughout gestation indicate a protective role in maintaining pregnancy. Biology of Reproduction 70 1018-1023. (doi:10.1095/biolreprod.103.022640)
16. Bodnar LM, Simhan HN, Powers RW, Frank MP, Cooperstein E&Roberts JM 2007a High prevalence of vitamin D insufficiency in black and white pregnant women residing in the northern United States and their neonates. Journal of Nutrition 137 447-452.
17. Bodnar LM, Catov JM, Simhan HN, Holick MF, Powers RW&Roberts JM 2007b Maternal vitamin D deficiency increases the risk of preeclampsia. Journal of Clinical Endocrinology and Metabolism 92 3517-3522. (doi:10.1210/jc.2007-0718)
18. Boonstra A, Barrat FJ, Crain C, Heath VL, Savelkoul HF&O'Garra A 2001 1α,25-Dihydroxyvitamin D3 has a direct effect on naive CD4(C) T cells to enhance the development of Th2 cells. Journal of Immunology 167 4974-4980. (doi:10.4049/jimmunol.167.9.4974)
19. Boyson JE, Nagarkatti N, Nizam L, Exley MA&Strominger JL 2006 Gestation stage-dependent mechanisms of invariant natural killer T cell-mediated pregnancy loss. PNAS 103 4580-4585. (doi:10.1073/pnas.0511025103)
20. Boyson JE, Aktan I, Barkhuff DA&Chant A 2008 NKT cells at thematernal-fetal interface. Immunological Investigations 37 565-582. (doi:10.1080/08820130802191409)
21. Brannon PM&Picciano MF 2011 Vitamin D in pregnancy and lactation in humans. Annual Review of Nutrition 31 89-115. (doi:10.1146/annurev.nutr.012809.104807)
22. Brehm JM, Schuemann B, Fuhlbrigge AL, Hollis BW, Strunk RC, Zeiger RS, Weiss ST, Litonjua AA&Childhood Asthma Management Program Research Group 2010 Serum vitamin D levels and severe asthma exacerbations in the Childhood Asthma Management Program study. Journal of Allergy and Clinical Immunology 126 52-58 e55. (doi:10.1016/j.jaci.2010.03.043)
23. Bulmer JN&Lash GE 2005 Human uterine natural killer cells: a reappraisal. Molecular Immunology 42 511-521. (doi:10.1016/j.molimm.2004.07.035)
24. Bulmer JN, Pace D&Ritson A 1988 Immunoregulatory cells in human decidua: morphology, immunohistochemistry and function. Reproduction, Nutrition, Development 28 1599-1613. (doi:10.1051/rnd:19881006)
25. Bulmer JN, Longfellow M&Ritson A 1991 Leukocytes and resident blood cells in endometrium. Annals of the New York Academy of Sciences 622 57-68. (doi:10.1111/j.1749-6632.1991.tb37850.x)
26. Bulmer JN, Williams PJ&Lash GE 2010 Immune cells in the placental bed. International Journal of Developmental Biology 54 281-294. (doi:10.1387/ijdb.082763jb)
27. Cannell JJ, Vieth R, Umhau JC, Holick MF, Grant WB, Madronich S, Garland CF&Giovannucci E 2006 Epidemic influenza and vitamin D. Epidemiology and Infection 134 1129-1140. (doi:10.1017/S0950268806007175)
28. Chambon Y 1951 Synergic action of vitamin D and of progesterone in obtaining ovumimplantation in the castrated pregnant rabbit. Comptes Rendus des Séances de la Société de Biologie et de Ses Filiales 145 955-959.
29. Chen S, Sims GP, Chen XX, Gu YY, Chen S & Lipsky PE 2007 Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. Journal of Immunology 179 1634-1647. (doi:10.4049/jimmunol.179.3.1634)
30. Chen J, Bruce D&Cantorna MT 2014 Vitamin D receptor expression controls proliferation of naive CD8+ T cells and development of CD8 mediated gastrointestinal inflammation. BMC Immunology 15 6. (doi:10.1186/1471-2172-15-6)
31. Clifford K, Flanagan AM&Regan L 1999 Endometrial CD56+ natural killer cells in women with recurrentmiscarriage: a histomorphometric study. Human Reproduction 14 2727-2730. (doi:10.1093/humrep/14.11.2727)
32. Colin EM, Asmawidjaja PS, van Hamburg JP, Mus AM, van Driel M, Hazes JM, van Leeuwen JP&Lubberts E 2010 1,25-dihydroxyvitamin D3 modulates Th17 polarization and interleukin-22 expression by memory T cells from patients with early rheumatoid arthritis. Arthritis and Rheumatism 62 132-142. (doi:10.1002/art.25043)
33. Collins MK, Tay CS&Erlebacher A 2009 Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. Journal of Clinical Investigation 119 2062-2073. (doi:10.1172/JCI38714)
34. Correale J, Ysrraelit MC&Gaitan MI 2009 Immunomodulatory effects of vitamin D in multiple sclerosis. Brain 132 1146-1160. (doi:10.1093/brain/awp033)
35. Daniel C, Sartory NA, Zahn N, Radeke HH&Stein JM 2008 Immune modulatory treatment of TNBS colitis with calcitriol is associated with a change of a Th1/Th17 to a Th2 and regulatory T cell profile. Journal of Pharmacology and Experimental Therapeutics 324 23-33. (doi:10.1124/jpet.107.127209)
36. Darby MM, Wallace K, Cornelius D, Chatman KT, Mosely JN, Martin JN, Purser CA, Baker RC, Owens MT&Lamarca BB 2013 Vitamin D supplementation suppresses hypoxia-stimulated placental cytokine secretion, hypertension and CD4+ T cell stimulation in response to placental ischemia. Medical Journal of Obstetrics and Gynecology 1 1012.
37. Dong X, Bachman LA, Kumar R&Griffin MD 2003 Generation of antigen-specific, interleukin-10-producing T-cells using dendritic cell stimulation and steroid hormone conditioning. Transplant Immunology 11 323-333. (doi:10.1016/S0966-3274(03)00049-2)
38. Du H, Daftary GS, Lalwani SI&Taylor HS 2005 Direct regulation of HOXA10 by 1,25-(OH)2D3 in human myelomonocytic cells and human endometrial stromal cells. Molecular Endocrinology 19 2222-2233. (doi:10.1210/me.2004-0336)
39. Equils O&Hewison M 2010 A role for vitamin D in placental immunology. Journal of Infectious Diseases 201 1950-1951 author reply 1951. (doi:10.1086/652804)
40. Erlebacher A 2013a Immunology of the maternal-fetal interface. Annual Review of Immunology 31 387-411. (doi:10.1146/annurev-immunol-032712-100003)
41. Erlebacher A 2013b Mechanisms of T cell tolerance towards the allogeneic fetus. Nature Reviews. Immunology 13 23-33. (doi:10.1038/nri3361)
42. Evans KN, Bulmer JN, Kilby MD&Hewison M 2004 Vitamin D and placental-decidual function. Journal of the Society for Gynecologic Investigation 11 263-271. (doi:10.1016/j.jsgi.2004.02.002)
43. Evans KN, Nguyen L, Chan J, Innes BA, Bulmer JN, Kilby MD&Hewison M 2006 Effects of 25-hydroxyvitamin D3 and 1,25-dihydroxyvitamin D3 on cytokine production by human decidual cells. Biology of Reproduction 75 816-822. (doi:10.1095/biolreprod.106.054056)
44. Fettke F, Schumacher A, Costa SD&Zenclussen AC 2014 B cells: the old new players in reproductive immunology. Frontiers in Immunology 5 285. (doi:10.3389/fimmu.2014.00285)
45. Fujiwara N&Kobayashi K 2005 Macrophages in inflammation. Current Drug Targets. Inflammation and Allergy 4 281-286. (doi:10.2174/1568010054022024)
46. Gale CR, Robinson SM, Harvey NC, Javaid MK, Jiang B, Martyn CN, Godfrey KM, Cooper C&Princess Anne Hospital Study Group 2008 Maternal vitamin D status during pregnancy and child outcomes. European Journal of Clinical Nutrition 62 68-77. (doi:10.1038/sj.ejcn.1602680)
47. Garabedian M, Tanaka Y, Holick MF&Deluca HF 1974 Response of intestinal calcium transport and bone calcium mobilization to 1,25-dihydroxyvitamin D3 in thyroparathyroidectomized rats. Endocrinology 94 1022-1027. (doi:10.1210/endo-94-4-1022)
48. Gellersen B, Brosens IA&Brosens JJ 2007 Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives. Seminars in Reproductive Medicine 25 445-453. (doi:10.1055/s-2007-991042)
49. Ginde AA, Sullivan AF, Mansbach JM&Camargo CA Jr 2010 Vitamin D insufficiency in pregnant and nonpregnant women of childbearing age in the United States. American Journal of Obstetrics and Gynecology 202 436.e1-436.e8. (doi:10.1016/j.ajog.2009.11.036)
50. Gombart AF, Borregaard N&Koeffler HP 2005 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 D3. FASEB Journal 19 1067-1077. (doi:10.1096/fj.04-3284com)
51. Gordon S&Martinez FO 2010 Alternative activation of macrophages: mechanism and functions. Immunity 32 593-604. (doi:10.1016/j.immuni.2010.05.007)
52. Gorman S, Kuritzky LA, Judge MA, Dixon KM, McGlade JP, Mason RS, Finlay-Jones JJ&Hart PH 2007 Topically applied 1,25-dihydroxyvitamin D3 enhances the suppressive activity of CD4+CD25+ cells in the draining lymph nodes. Journal of Immunology 179 6273-6283. (doi:10.4049/jimmunol.179.9.6273)
53. Grant WB&Mohr SB 2009 Ecological studies of ultraviolet B, vitamin D and cancer since 2000. Annals of Epidemiology 19 446-454. (doi:10.1016/j.annepidem.2008.12.014)
54. Gray TK, Lester GE&Lorenc RS 1979 Evidence for extra-renal 1α-hydroxylation of 25-hydroxyvitamin D3 in pregnancy. Science 204 1311-1313. (doi:10.1126/science.451538)
55. Gregori S, Casorati M, Amuchastegui S, Smiroldo S, Davalli AM&Adorini L 2001 Regulatory T cells induced by 1α,25-dihydroxyvitamin D3 and mycophenolate mofetil treatment mediate transplantation tolerance. Journal of Immunology 167 1945-1953. (doi:10.4049/jimmunol.167.4.1945)
56. Gregori S, Giarratana N, Smiroldo S, Uskokovic M&Adorini L 2002 A 1α,25-dihydroxyvitamin D(3) analog enhances regulatory T-cells and arrests autoimmune diabetes in NOD mice. Diabetes 51 1367-1374. (doi:10.2337/diabetes.51.5.1367)
57. Griffin MD, Lutz WH, Phan VA, Bachman LA, McKean DJ&Kumar R 2000 Potent inhibition of dendritic cell differentiation and maturation by vitamin D analogs. Biochemical and Biophysical Research Communications 270 701-708. (doi:10.1006/bbrc.2000.2490)
58. Griffin MD, Lutz W, Phan VA, Bachman LA, McKean DJ&Kumar R 2001 Dendritic cell modulation by 1α,25 dihydroxyvitamin D3 and its analogs: a vitamin D receptor-dependent pathway that promotes a persistent state of immaturity in vitro and in vivo. PNAS 98 6800-6805. (doi:10.1073/pnas.121172198)
59. Gustafsson C, Mjosberg J, Matussek A, Geffers R, Matthiesen L, Berg G, Sharma S, Buer J & Ernerudh J 2008 Gene expression profiling of human decidual macrophages: evidence for immunosuppressive phenotype. PLoS ONE 3 e2078. (doi:10.1371/journal.pone.0002078)
60. Halloran BP&DeLuca HF 1980 Calcium transport in small intestine during early development: role of vitamin D. American Journal of Physiology 239 G473-G479.
61. Hanna J, Wald O, Goldman-Wohl D, Prus D, Markel G, Gazit R, Katz G, Haimov-Kochman R, Fujii N, Yagel S et al. 2003 CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood 102 1569-1577. (doi:10.1182/blood-2003-02-0517)
62. Haussler MR, Haussler CA, Bartik L, Whitfield GK, Hsieh JC, Slater S & Jurutka PW 2008 Vitamin D receptor: molecular signaling and actions of nutritional ligands in disease prevention. Nutrition Reviews 66 S98-S112. (doi:10.1111/j.1753-4887.2008.00093.x)
63. Heikkinen J, Mottonen M, Pulkki K, Lassila O&Alanen A 2001 Cytokine levels in midtrimester amniotic fluid in normal pregnancy and in the prediction of pre-eclampsia. Scandinavian Journal of Immunology 53 310-314. (doi:10.1046/j.1365-3083.2001.00872.x)
64. Henry HL, Bouillon R, Norman AW, Gallagher JC, Lips P, Heaney RP, Vieth R, Pettifor JM, Dawson-Hughes B, Lamberg-Allardt CJ et al. 2010 14th Vitamin D Workshop consensus on vitamin D nutritional guidelines. Journal of Steroid Biochemistry and Molecular Biology 121 4-6. (doi:10.1016/j.jsbmb.2010.05.008)
65. Hewison M 2010 Vitamin D and the intracrinology of innate immunity. Molecular and Cellular Endocrinology 321 103-111. (doi:10.1016/j.mce.2010.02.013)
66. Hewison M 2011 Vitamin D and innate and adaptive immunity. Vitamins and Hormones 86 23-62. (doi:10.1016/B978-0-12-386960-9.00002-2)
67. Hewison M, Freeman L, Hughes SV, Evans KN, Bland R, Eliopoulos AG, Kilby MD, Moss PA&Chakraverty R 2003 Differential regulation of vitamin D receptor and its ligand in human monocyte-derived dendritic cells. Journal of Immunology 170 5382-5390. (doi:10.4049/jimmunol.170.11.5382)
68. Hewison M, Burke F, Evans KN, Lammas DA, Sansom DM, Liu P, Modlin RL & Adams JS 2007 Extra-renal 25-hydroxyvitamin D3-1α-hydroxylase in human health and disease. Journal of Steroid Biochemistry and Molecular Biology 103 316-321. (doi:10.1016/j.jsbmb.2006.12.078)
69. Holick MF 2007 Vitamin D deficiency. New England Journal of Medicine 357 266-281. (doi:10.1056/NEJMra070553)
70. Holick MF&Chen TC 2008 Vitamin D deficiency: a worldwide problem with health consequences. American Journal of Clinical Nutrition 87 1080S-1086S.
71. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, Murad MH&Weaver CM 2011 Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. Journal of Clinical Endocrinology and Metabolism 96 1911-1930. (doi:10.1210/jc.2011-0385)
72. Houser BL, Tilburgs T, Hill J, Nicotra ML&Strominger JL 2011 Two unique human decidual macrophage populations. Journal of Immunology 186 2633-2642. (doi:10.4049/jimmunol.1003153)
73. Huang SJ, Chen CP, Schatz F, Rahman M, Abrahams VM&Lockwood CJ 2008 Pre-eclampsia is associated with dendritic cell recruitment into the uterine decidua. Journal of Pathology 214 328-336. (doi:10.1002/path.2257)
74. 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. (doi:10.1016/S0140-6736(01)06580-1)
75. Jeffery LE, Burke F, Mura M, Zheng Y, Qureshi OS, Hewison M, Walker LS, Lammas DA, Raza K&Sansom DM 2009 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. Journal of Immunology 183 5458-5467. (doi:10.4049/jimmunol.0803217)
76. Jeffery LE, Wood AM, Qureshi OS, Hou TZ, Gardner D, Briggs Z, Kaur S, Raza K & Sansom DM 2012 Availability of 25-hydroxyvitamin D3 to APCs controls the balance between regulatory and inflammatory T cell responses. Journal of Immunology 189 5155-5164. (doi:10.4049/jimmunol.1200786)
77. Jensen F, Muzzio D, Soldati R, Fest S&Zenclussen AC 2013 Regulatory B10 cells restore pregnancy tolerance in a mouse model. Biology of Reproduction 89 90. (doi:10.1095/biolreprod.113.110791)
78. Josinovich JB 1969 Human Placental Lactogen., New York: Academic Press, Inc.
79. Kachkache M, Rebut-Bonneton C, Demignon J, Cynober E&Garabedian M 1993 Uterine cells other than stromal decidual cells are required for 1,25-dihydroxyvitamin D3 production during early human pregnancy. FEBS Letters 333 83-88. (doi:10.1016/0014-5793(93)80379-9)
80. Kammerer U, Schoppet M, McLellan AD, Kapp M, Huppertz HI, Kampgen E & Dietl J 2000 Human decidua contains potent immunostimulatory CD83(C) dendritic cells. American Journal of Pathology 157 159-169. (doi:10.1016/S0002-9440(10)64527-0)
81. Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TB, Dietl J, van Kooyk Y&Kampgen E 2003 Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. American Journal of Pathology 162 887-896. (doi:10.1016/S0002-9440(10)63884-9)
82. Karmali R, Hewison M, Rayment N, Farrow SM, Brennan A, Katz DR & O'Riordan JL 1991 1,25(OH)2D3 regulates c-myc mRNA levels in tonsillar T lymphocytes. Immunology 74 589-593.
83. Keskin DB, Allan DS, Rybalov B, Andzelm MM, Stern JN, Kopcow HD, Koopman LA&Strominger JL 2007 TGFß promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells. PNAS 104 3378-3383. (doi:10.1073/pnas.0611098104)
84. Kooh SW&Vieth R 1980 25-hydroxyvitamin D metabolism in the sheep fetus and lamb. Pediatric Research 14 360-363. (doi:10.1203/00006450-198004000-00022)
85. Kopcow HD, Eriksson M, Mselle TF, Damrauer SM, Wira CR, Sentman CL & Strominger JL 2010 Human decidual NK cells from gravid uteri and NK cells from cycling endometrium are distinct NK cell subsets. Placenta 31 334-338. (doi:10.1016/j.placenta.2010.01.003)
86. Korn T, Oukka M, Kuchroo V&Bettelli E 2007 Th17 cells: effector T cells with inflammatory properties. Seminars in Immunology 19 362-371. (doi:10.1016/j.smim.2007.10.007)
87. Kovacs CS&Kronenberg HM 1997 Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocrine Reviews 18 832-872. (doi:10.1210/edrv.18.6.0319)
88. Kovacs CS, Woodland ML, Fudge NJ&Friel JK 2005 The vitamin D receptor is not required for fetal mineral homeostasis or for the regulation of placental calcium transfer in mice. American Journal of Physiology. Endocrinology and Metabolism 289 E133-E144. (doi:10.1152/ajpendo.00354.2004)
89. Kreutz M, Andreesen R, Krause SW, Szabo A, Ritz E&Reichel H 1993 1,25-dihydroxyvitamin D3 production and vitamin D3 receptor expression are developmentally regulated during differentiation of human monocytes into macrophages. Blood 82 1300-1307.
90. Kwan M, Hazan A, Zhang J, Jones R, Harris L, Whittle W, Keating S, Dunk C & Lye S 2014 Dynamic changes in maternal decidual leukocyte populations from first to second trimester gestation. Placenta 35 127-134. (doi:10.1016/j.placenta.2014.09.018)
91. Laird SM, Tuckerman EM, Cork BA, Linjawi S, Blakemore AI&Li TC 2003 A review of immune cells and molecules in women with recurrent miscarriage. Human Reproduction Update 9 163-174. (doi:10.1093/humupd/dmg013)
92. Lash GE, Robson SC&Bulmer JN 2010a Review: Functional role of uterine natural killer (uNK) cells in human early pregnancy decidua. Placenta 31(Suppl) S87-S92. (doi:10.1016/j.placenta.2009.12.022)
93. Lash GE, Otun HA, Innes BA, Percival K, Searle RF, Robson SC&Bulmer JN 2010b Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age. Human Reproduction 25 1137-1145. (doi:10.1093/humrep/deq050)
94. Laskarin G, Kammerer U, Rukavina D, Thomson AW, Fernandez N & Blois SM 2007 Antigen-presenting cells and materno-fetal tolerance: an emerging role for dendritic cells. American Journal of Reproductive Immunology 58 255-267. (doi:10.1111/j.1600-0897.2007.00511.x)
95. Lemire JM, Archer DC, Beck L&Spiegelberg HL 1995 Immunosuppressive actions of 1,25-dihydroxyvitamin D3: preferential inhibition of Th1 functions. Journal of Nutrition 125 1704S-1708S.
96. Leung KH 1989 Inhibition of human natural killer cell and lymphokine-activated killer cell cytotoxicity and differentiation by vitamin D3. Scandinavian Journal of Immunology 30 199-208. (doi:10.1111/j.1365-3083.1989.tb01202.x)
97. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C et al. 2006 Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311 1770-1773. (doi:10.1126/science.1123933)
98. Liu N, Nguyen L, Chun RF, Lagishetty V, Ren S, Wu S, Hollis B, DeLuca HF, Adams JS&Hewison M 2008 Altered endocrine and autocrine metabolism of vitamin D in a mouse model of gastrointestinal inflammation. Endocrinology 149 4799-4808. (doi:10.1210/en.2008-0060)
99. Liu PT, Schenk M, Walker VP, Dempsey PW, Kanchanapoomi M, Wheelwright M, Vazirnia A, Zhang X, Steinmeyer A, Zugel U et al. 2009 Convergence of IL-1ß and VDR activation pathways in human TLR2/1-induced antimicrobial responses. PLoS ONE 4 e5810. (doi:10.1371/journal.pone.0005810)
100. Liu NQ, Kaplan AT, Lagishetty V, Ouyang YB, Ouyang Y, Simmons CF, Equils O&Hewison M 2011 Vitamin D and the regulation of placental inflammation. Journal of Immunology 186 5968-5974. (doi:10.4049/jimmunol.1003332)
101. Liu NQ, Ouyang Y, Bulut Y, Lagishetty V, Chan SY, Hollis BW, Wagner C, Equils O&Hewison M 2013 Dietary vitamin D restriction in pregnant female mice is associated with maternal hypertension and altered placental and fetal development. Endocrinology 154 2270-2280. (doi:10.1210/en.2012-2270)
102. Looker AC, Johnson CL, Lacher DA, Pfeiffer CM, Schleicher RL&Sempos CT 2011 Vitamin D status: United States, 2001-2006. NCHS Data Brief 1-8.
103. Lund B&Selnes A 1979 Plasma 1,25-dihydroxyvitamin D levels in pregnancy and lactation. Acta Endocrinologica 92 330-335. (doi:10.1530/acta.0.0920330)
104. Lynch L, Golden-Mason L, Eogan M, O'Herlihy C&O'Farrelly C 2007 Cells with haematopoietic stem cell phenotype in adult human endometrium: relevance to infertility? Human Reproduction 22 919-926. (doi:10.1093/humrep/del456)
105. Male V, Hughes T, McClory S, Colucci F, Caligiuri MA&Moffett A 2010 Immature NK cells, capable of producing IL-22, are present in human uterine mucosa. Journal of Immunology 185 3913-3918. (doi:10.4049/jimmunol.1001637)
106. Mathieu C&Badenhoop K 2005 Vitamin D and type 1 diabetes mellitus: state of the art. Trends in Endocrinology and Metabolism 16 261-266. (doi:10.1016/j.tem.2005.06.004)
107. Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M&Tedder TF 2008 Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. Journal of Clinical Investigation 118 3420-3430. (doi:10.1172/JCI36030)
108. Mehta S, Hunter DJ, Mugusi FM, Spiegelman D, Manji KP, Giovannucci EL, Hertzmark E, Msamanga GI&Fawzi WW 2009 Perinatal outcomes, including mother-to-child transmission of HIV, and child mortality and their association with maternal vitamin D status in Tanzania. Journal of Infectious Diseases 200 1022-1030. (doi:10.1086/605699)
109. Merino F, Alvarez-Mon M, de la Hera A, Ales JE, Bonilla F&Durantez A 1989 Regulation of natural killer cytotoxicity by 1,25-dihydroxyvitamin D3. Cellular Immunology 118 328-336. (doi:10.1016/0008-8749(89)90381-X)
110. Mithal A, Wahl DA, Bonjour JP, Burckhardt P, Dawson-Hughes B, Eisman JA, El-Hajj Fuleihan G, Josse RG, Lips P&Morales-Torres J 2009 Global vitamin D status and determinants of hypovitaminosis D. Osteoporosis International 20 1807-1820. (doi:10.1007/s00198-009-0954-6)
111. Moffett A&Loke C 2006 Implantation, embryo-maternal interactions, immunology and modulation of the uterine environment - a workshop report. Placenta 27 S54-S55. (doi:10.1016/j.placenta.2006.01.021)
112. Moran-Auth Y, Penna-Martinez M, Shoghi F, Ramos-Lopez E&Badenhoop K 2013 Vitamin D status and gene transcription in immune cells. Journal of Steroid Biochemistry and Molecular Biology 136 83-85. (doi:10.1016/j.jsbmb.2013.02.005)
113. Mosser DM 2003 The many faces of macrophage activation. Journal of Leukocyte Biology 73 209-212. (doi:10.1189/jlb.0602325)
114. Munger KL, Levin LI, Hollis BW, Howard NS&Ascherio A 2006 Serum 25-hydroxyvitamin D levels and risk of multiple sclerosis. Journal of the American Medical Association 296 2832-2838. (doi:10.1001/jama.296.23.2832)
115. Murphy LC, Wild J, Stone GM&Posen S 1980 The effect of estradiol on a 25-hydroxycholecalciferol binding protein in the uterus of the mouse. Steroids 35 1-8. (doi:10.1016/0039-128X(80)90106-3)
116. Nunn JD, Katz DR, Barker S, Fraher LJ, Hewison M, Hendy GN & O'Riordan JL 1986 Regulation of human tonsillar T-cell proliferation by the active metabolite of vitamin D3. Immunology 59 479-484.
117. O'Kelly J, Hisatake J, Hisatake Y, Bishop J, Norman A&Koeffler HP 2002 Normal myelopoiesis but abnormal T lymphocyte responses in vitamin D receptor knockout mice. Journal of Clinical Investigation 109 1091-1099. (doi:10.1172/JCI0212392)
118. Ooi JH, McDaniel KL, Weaver V&Cantorna MT 2014 Murine CD8+ T cells but not macrophages express the vitamin D 1a-hydroxylase. Journal of Nutritional Biochemistry 25 58-65. (doi:10.1016/j.jnutbio.2013.09.003)
119. Oreshkova T, Dimitrov R&Mourdjeva M 2012 A cross-talk of decidual stromal cells, trophoblast, and immune cells: a prerequisite for the success of pregnancy. American Journal of Reproductive Immunology 68 366-373. (doi:10.1111/j.1600-0897.2012.01165.x)
120. Overbergh L, Decallonne B, Waer M, Rutgeerts O, Valckx D, Casteels KM, Laureys J, Bouillon R&Mathieu C 2000 1α,25-dihydroxyvitamin D3 induces an autoantigen-specific T-helper 1/T-helper 2 immune shift in NOD mice immunized with GAD65 (p524-543). Diabetes 49 1301-1307. (doi:10.2337/diabetes.49.8.1301)
121. Pace D, Morrison L&Bulmer JN 1989 Proliferative activity in endometrial stromal granulocytes throughout menstrual cycle and early pregnancy. Journal of Clinical Pathology 42 35-39. (doi:10.1136/jcp.42.1.35)
122. Palmer MT, Lee YK, Maynard CL, Oliver JR, Bikle DD, Jetten AM&Weaver CT 2010 Lineage-specific effects of 1,25-dihydroxyvitamin D(3) on the development of effector CD4 T cells. Journal of Biological Chemistry 286 997-1004. (doi:10.1074/jbc.M110.163790)
123. Piccinni MP, Beloni L, Livi C, Maggi E, Scarselli G&Romagnani S 1998 Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nature Medicine 4 1020-1024. (doi:10.1038/2006)
124. Provvedini DM&Manolagas SC 1989 1α,25-dihydroxyvitamin D3 receptor distribution and effects in subpopulations of normal human T lymphocytes. Journal of Clinical Endocrinology and Metabolism 68 774-779. (doi:10.1210/jcem-68-4-774)
125. Provvedini DM, Tsoukas CD, Deftos LJ&Manolagas SC 1986 1α,25-Dihydroxyvitamin D3-binding macromolecules in human B lymphocytes: effects on immunoglobulin production. Journal of Immunology 136 2734-2740.
126. Public Health England and Food Standards Agency 2014. National Diet and Nutrition Survey. Headline results from Years 1, 2 and 3 (combined) of the Rolling Programme (2008/2009-2010/11). https://www.gov.uk.
127. Quenby S&Farquharson R 2006 Uterine natural killer cells, implantation failure and recurrent miscarriage. Reproductive Biomedicine Online 13 24-28. (doi:10.1016/S1472-6483(10)62012-3)
128. Ramathal CY, Bagchi IC, Taylor RN&Bagchi MK 2010 Endometrial decidualization: of mice and men. Seminars in Reproductive Medicine 28 17-26. (doi:10.1055/s-0029-1242989)
129. Reichrath J&Querings K 2005 Vitamin D deficiency during pregnancy: a risk factor not only for fetal growth and bone metabolism but also for correct development of the fetal immune system? American Journal of Clinical Nutrition 81 1177 author reply 1177-1178.
130. Rieger L, Honig A, Sutterlin M, Kapp M, Dietl J, Ruck P&Kammerer U 2004 Antigen-presenting cells in human endometrium during the menstrual cycle compared to early pregnancy. Journal of the Society for Gynecologic Investigation 11 488-493. (doi:10.1016/j.jsgi.2004.05.007)
131. Rieger L, Segerer S, Bernar T, Kapp M, Majic M, Morr AK, Dietl J & Kammerer U 2009 Specific subsets of immune cells in human decidua differ between normal pregnancy and preeclampsia - a prospective observational study. Reproductive Biology and Endocrinology 7 132. (doi:10.1186/1477-7827-7-132)
132. Robson A, Harris LK, Innes BA, Lash GE, Aljunaidy MM, Aplin JD, Baker PN, Robson SC&Bulmer JN 2012 Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB Journal 26 4876-4885. (doi:10.1096/fj.12-210310)
133. Romagnani S 2006 Regulation of the T cell response. Clinical and Experimental Allergy 36 1357-1366. (doi:10.1111/j.1365-2222.2006.02606.x)
134. Saito S, Umekage H, Sakamoto Y, Sakai M, Tanebe K, Sasaki Y&Morikawa H 1999 Increased T-helper-1-type immunity and decreased T-helper-2-type immunity in patients with preeclampsia. American Journal of Reproductive Immunology 41 297-306. (doi:10.1111/j.1600-0897.1999.tb00442.x)
135. Saito S, Nakashima A, Shima T&Ito M 2010 Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. American Journal of Reproductive Immunology 63 601-610. (doi:10.1111/j.1600-0897.2010.00852.x)
136. Salamonsen LA, Hannan NJ&Dimitriadis E 2007 Cytokines and chemokines during human embryo implantation: roles in implantation and early placentation. Seminars in Reproductive Medicine 25 437-444. (doi:10.1055/s-2007-991041)
137. Scaife P, Searle R, Robson S, Innes B&Bulmer J 2003 A comparison of cytotoxic decidual leukocyte populations in early and late pregnancy. Journal of the Society for Gynecologic Investigation 10 360A.
138. Schonkeren D, van derHoorn ML, Khedoe P, Swings G, van Beelen E, Claas F, van Kooten C, de Heer E&Scherjon S 2011 Differential distribution and phenotype of decidual macrophages in preeclamptic versus control pregnancies. American Journal of Pathology 178 709-717. (doi:10.1016/j.ajpath.2010.10.011)
139. Shin DM, Yuk JM, Lee HM, Lee SH, Son JW, Harding CV, Kim JM, Modlin RL & Jo EK 2011 Mycobacterial lipoprotein activates autophagy via TLR2/1/CD14 and a functional vitamin D receptor signalling. Cellular Microbiology 12 1648-1665. (doi:10.1111/j.1462-5822.2010.01497.x)
140. Shiozawa K, Shiozawa S, Shimizu S&Fujita T 1985 1α,25-dihydroxyvitamin D3 inhibits pokeweed mitogen-stimulated human B-cell activation: an analysis using serum-free culture conditions. Immunology 56 161-167.
141. Spach KM, Nashold FE, Dittel BN&Hayes CE 2006 IL-10 signaling is essential for 1,25-dihydroxyvitamin D3-mediated inhibition of experimental autoimmune encephalomyelitis. Journal of Immunology 177 6030-6037. (doi:10.4049/jimmunol.177.9.6030)
142. Takeda K&Akira S 2005 Toll-like receptors in innate immunity. International Immunology 17 1-14. (doi:10.1093/intimm/dxh186)
143. Trundley A&Moffett A 2004 Human uterine leukocytes and pregnancy. Tissue Antigens 63 1-12. (doi:10.1111/j.1399-0039.2004.00170.x)
144. Turner M, Barre PE, Benjamin A, Goltzman D&Gascon-Barre M 1988 Does the maternal kidney contribute to the increased circulating 1,25-dihydroxyvitamin D concentrations during pregnancy? Mineral and Electrolyte Metabolism 14 246-252.
145. Urrutia RP&Thorp JM 2012 Vitamin D in pregnancy: current concepts. Current Opinion in Obstetrics&Gynecology 24 57-64. (doi:10.1097/GCO.0b013e3283505ab3)
146. Urry Z, Xystrakis E, Richards DF, McDonald J, Sattar Z, Cousins DJ, Corrigan CJ, Hickman E, Brown Z & Hawrylowicz CM 2009 Ligation of TLR9 induced on human IL-10-secreting Tregs by 1α,25-dihydroxyvitamin D3 abrogates regulatory function. Journal of Clinical Investigation 119 387-398.
147. Vacca P, Moretta L, Moretta A&Mingari MC 2011 Origin, phenotype and function of human natural killer cells in pregnancy. Trends in Immunology 32 517-523. (doi:10.1016/j.it.2011.06.013)
148. Van Cromphaut SJ, Rummens K, Stockmans I, Van Herck E, Dijcks FA, Ederveen AG, Carmeliet P, Verhaeghe J, Bouillon R&Carmeliet G 2003 Intestinal calcium transporter genes are upregulated by estrogens and the reproductive cycle through vitamin D receptor-independent mechanisms. Journal of Bone and Mineral Research 18 1725-1736. (doi:10.1359/jbmr.2003.18.10.1725)
149. Wang TT, Nestel FP, Bourdeau V, Nagai Y, Wang Q, Liao J, Tavera-Mendoza L, Lin R, Hanrahan JW, Mader S et al. 2004 Cutting edge: 1,25- dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. Journal of Immunology 173 2909-2912. (doi:10.4049/jimmunol.173.5.2909)
150. Warning JC, McCracken SA&Morris JM 2011 A balancing act: mechanisms by which the fetus avoids rejection by the maternal immune system. Reproduction 141 715-724. (doi:10.1530/REP-10-0360)
151. Wegmann TG, Lin H, Guilbert L&Mosmann TR 1993 Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunology Today 14 353-356. (doi:10.1016/0167-5699(93)90235-D)
152. Weisman Y, Vargas A, Duckett G, Reiter E&Root AW 1978 Synthesis of 1,25-dihydroxyvitamin D in the nephrectomized pregnant rat. Endocrinology 103 1992-1996. (doi:10.1210/endo-103-6-1992)
153. Weisman Y, Harell A, Edelstein S, David M, Spirer Z&Golander A 1979 1α,25-Dihydroxyvitamin D3 and 24,25-dihydroxyvitamin D3 in vitro synthesis by human decidua and placenta. Nature 281 317-319. (doi:10.1038/281317a0)
154. Willheim M, Thien R, Schrattbauer K, Bajna E, Holub M, Gruber R, Baier K, Pietschmann P, Reinisch W, Scheiner O et al. 1999 Regulatory effects of 1α,25-dihydroxyvitamin D3 on the cytokine production of human peripheral blood lymphocytes. Journal of Clinical Endocrinology and Metabolism 84 3739-3744.
155. Williams PJ, Bulmer JN, Searle RF, Innes BA&Robson SC 2009 Altered decidual leucocyte populations in the placental bed in pre-eclampsia and fetal growth restriction: a comparison with late normal pregnancy. Reproduction 138 177-184. (doi:10.1530/REP-09-0007)
156. Woodham PC, Brittain JE, Baker AM, Long DL, Haeri S, Camargo CA Jr, Boggess KA&Stuebe AM 2011 Midgestation maternal serum 25- hydroxyvitamin D level and soluble fms-like tyrosine kinase 1/placental growth factor ratio as predictors of severe preeclampsia. Hypertension 58 1120-1125. (doi:10.1161/HYPERTENSIONAHA.111.179069)
157. Yu S&Cantorna MT 2011 Epigenetic reduction in invariant NKT cells following in utero vitamin D deficiency in mice. Journal of Immunology 186 1384-1390. (doi:10.4049/jimmunol.1002545)
158. Zehnder D, Evans KN, Kilby MD, Bulmer JN, Innes BA, Stewart PM & Hewison M 2002 The ontogeny of 25-hydroxyvitamin D(3) 1a-hydroxylase expression in human placenta and decidua. American Journal of Pathology 161 105-114. (doi:10.1016/S0002-9440(10)64162-4)
159. Zittermann A, Gummert JF&Borgermann J 2011 The role of vitamin D in dyslipidemia and cardiovascular disease. Current Pharmaceutical Design 17 933-942. (doi:10.2174/138161211795428786)