Role of the placental Vitamin D receptor in modulating feto-placental growth in fetal growth restriction and preeclampsia-affected pregnancies

Frontiers in Physiology

Volumn 7, Issue FEB, 2016, Pages

  Murthi, Padma ^a,b,c,d   Yong, Hannah E J ^b,c   Ngyuen, Thy P H ^b,c   Ellery, Stacey ^a,d   Singh, Harmeet ^a,d   Rahman, Rahana ^a,d   Dickinson, Hayley ^a,d   Walker, David W ^a,d   Davies Tuck, Miranda ^a,d   Wallace, Euan M ^a,d   Ebeling, Peter R ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ROYAL WOMEN'S HOSPITAL   (Australia)

^d HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Fetal growth restriction; Placental transport; Trophoblast; VDR

Indexed keywords

VITAMIN D; VITAMIN D RECEPTOR;

APOPTOSIS; BIOAVAILABILITY; CELL CYCLE REGULATION; CELL DIFFERENTIATION; DRUG EFFICACY; DRUG MECHANISM; FETUS DEVELOPMENT; FETUS GROWTH; GROWTH REGULATION; HUMAN; INTRAUTERINE GROWTH RETARDATION; PATHOPHYSIOLOGY; PLACENTA FUNCTION; PLACENTAL TRANSFER; PREECLAMPSIA; PREGNANCY; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; TROPHOBLAST; VITAMIN D DEFICIENCY; VITAMIN METABOLISM;

EID: 84962916531     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2016.00043     Document Type: Review

References (78)

1. Atkinson, S. A. (2011). Defining the process of dietary reference intakes: framework for the United States and Canada. Am. J. Clin. Nutr. 94, 655S-657S. doi: 10.3945/ajcn.110.005728.
2. Avila, E., Diaz, L., Barrera, D., Arranz, C., Halhali, A., and Larrea, F. (2007). Metabolism of vitamin D in the human choriocarcinoma cell line JEG-3. J. Steroid Biochem. Mol. Biol. 103, 781-785. doi: 10.1016/j.jsbmb.2006.12.047.
3. Avila, E., Diaz, L., Halhali, A., and Larrea, F. (2004). Regulation of 25-hydroxyvitamin D3 1alpha-hydroxylase, 1, 25-dihydroxyvitamin D3 24-hydroxylase and vitamin D receptor gene expression by 8-bromo cyclic AMP in cultured human syncytiotrophoblast cells. J. Steroid Biochem. Mol. Biol. 89-90, 115-119. doi: 10.1016/j.jsbmb.2004.03.090.
4. Baker, A. M., Haeri, S., Camargo, C. A. Jr., Espinola, J. A., and Stuebe, A. M. (2010). A nested case-control study of midgestation vitamin D deficiency and risk of severe preeclampsia. J. Clin. Endocrinol. Metab. 95, 5105-5109. doi: 10.1210/jc.2010-0996.
5. Barker, D. J. (1990). The fetal and infant origins of adult disease. BMJ 301, 1111. doi: 10.1136/bmj.301.6761.1111.
6. Barrera, D., Avila, E., Hernandez, G., Mendez, I., Gonzalez, L., Halhali, A., et al. (2008). Calcitriol affects hCG gene transcription in cultured human syncytiotrophoblasts. Reprod. Biol. Endocrinol. 6:3. doi: 10.1186/1477-7827-6-3.
7. Bodnar, L. M., Catov, J. M., Simhan, H. N., Holick, M. F., Powers, R. W., and Roberts, J. M. (2007). Maternal vitamin D deficiency increases the risk of preeclampsia. J. Clin. Endocrinol. Metab. 92, 3517-3522. doi: 10.1210/jc.2007-0718.
8. Bodnar, L. M., Simhan, H. N., Catov, J. M., Roberts, J. M., Platt, R. W., Diesel, J. C., et al. (2014). Maternal vitamin D status and the risk of mild and severe preeclampsia. Epidemiology 25, 207-214. doi: 10.1097/EDE.0000000000000039.
9. Caniggia, I., Grisaru-Gravnosky, S., Kuliszewsky, M., Post, M., and Lye, S. J. (1999). Inhibition of TGF-beta 3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies. J. Clin. Invest. 103, 1641-1650. doi: 10.1172/JCI6380.
10. Chen, C. P., Bajoria, R., and Aplin, J. D. (2002). Decreased vascularization and cell proliferation in placentas of intrauterine growth-restricted fetuses with abnormal umbilical artery flow velocity waveforms. Am. J. Obstet. Gynecol. 187, 764-769. doi: 10.1067/mob.2002.125243.
11. Cnattingius, S., Haglund, B., and Kramer, M. S. (1998). Differences in late fetal death rates in association with determinants of small for gestational age fetuses: population based cohort study. BMJ 316, 1483-1487. doi: 10.1136/bmj.316.7143.1483.
12. Crocker, I. P., Cooper, S., Ong, S. C., and Baker, P. N. (2003). Differences in apoptotic susceptibility of cytotrophoblasts and syncytiotrophoblasts in normal pregnancy to those complicated with preeclampsia and intrauterine growth restriction. Am. J. Pathol. 162, 637-643. doi: 10.1016/S0002-9440(10)63857-6.
13. Du, H., Daftary, G. S., Lalwani, S. I., and Taylor, H. S. (2005). Direct regulation of HOXA10 by 1, 25-(OH)2D3 in human myelomonocytic cells and human endometrial stromal cells. Mol. Endocrinol. 19, 2222-2233. doi: 10.1210/me.2004-0336.
14. Fischer, D., Schroer, A., Ludders, D., Cordes, T., Bucker, B., Reichrath, J., et al. (2007). Metabolism of vitamin D3 in the placental tissue of normal and preeclampsia complicated pregnancies and premature births. Clin. Exp. Obstet. Gynecol. 34, 80-84. doi: 10.3410/f.1090752.543986.
15. Frendo, J. L., Cronier, L., Bertin, G., Guibourdenche, J., Vidaud, M., Evain-Brion, D., et al. (2003). Involvement of connexin 43 in human trophoblast cell fusion and differentiation. J. Cell Sci. 116, 3413-3421. doi: 10.1242/jcs.00648.
16. Frisk, V., Amsel, R., and Whyte, H. E. (2002). The importance of head growth patterns in predicting the cognitive abilities and literacy skills of small-for-gestational-age children. Dev. Neuropsychol. 22, 565-593. doi: 10.1207/S15326942DN2203_2.
17. Froen, J. F., Gardosi, J. O., Thurmann, A., Francis, A., and Stray-Pedersen, B. (2004). Restricted fetal growth in sudden intrauterine unexplained death. Acta Obstet. Gynecol. Scand. 83, 801-807. doi: 10.1111/j.0001-6349.2004.00602.x.
18. Gardosi, J., Mul, T., Mongelli, M., and Fagan, D. (1998). Analysis of birthweight and gestational age in antepartum stillbirths. Br. J. Obstet. Gynaecol. 105, 524-530. doi: 10.1111/j.1471-0528.1998.tb10153.x.
19. Ghidini, A. (1996). Idiopathic fetal growth restriction: a pathophysiologic approach. Obstet. Gynecol. Surv. 51, 376-382. doi: 10.1097/00006254-199606000-00023.
20. Godfrey, K. M., and Barker, D. J. (2001). Fetal programming and adult health. Public Health Nutr. 4, 611-624. doi: 10.1079/PHN2001145.
21. Goldenberg, R. L., Dubard, M. B., Cliver, S. P., Nelson, K. G., Blankson, K., Ramey, S. L., et al. (1996). Pregnancy outcome and intelligence at age five years. Am. J. Obstet. Gynecol. 175, 1511-1515. doi: 10.1016/S0002-9378(96)70099-6.
22. Harman, C. R. (2008). Amniotic fluid abnormalities. Semin. Perinatol. 32, 288-294. doi: 10.1053/j.semperi.2008.04.012.
23. Hart, P. H., Lucas, R. M., Walsh, J. P., Zosky, G. R., Whitehouse, A. J., Zhu, K., et al. (2015). Vitamin D in fetal development: findings from a birth cohort study. Pediatrics 135, e167-e173. doi: 10.1542/peds.2014-1860.
24. Haugen, M., Brantsaeter, A. L., Trogstad, L., Alexander, J., Roth, C., Magnus, P., et al. (2009). Vitamin D supplementation and reduced risk of preeclampsia in nulliparous women. Epidemiology 20, 720-726. doi: 10.1097/EDE.0b013e3181a70f08.
25. Heaney, R. P. (2005). The Vitamin D requirement in health and disease. J. Steroid Biochem. Mol. Biol. 97, 13-19. doi: 10.1016/j.jsbmb.2005.06.020.
26. Heaney, R. P., Carey, R., and Harkness, L. (2005). Roles of vitamin D, n-3 polyunsaturated fatty acid, and soy isoflavones in bone health. J. Am. Diet. Assoc. 105, 1700-1702. doi: 10.1016/j.jada.2005.09.011.
27. Holick, M. F. (1994). McCollum Award Lecture, 1994: vitamin D-new horizons for the 21st century. Am. J. Clin. Nutr. 60, 619-630.
28. Holick, M. F. (2003). Vitamin D: a millenium perspective. J. Cell. Biochem. 88, 296-307. doi: 10.1002/jcb.10338.
29. Holick, M. F. (2007). Vitamin D deficiency. N. Engl. J. Med. 357, 266-281. doi: 10.1056/NEJMra070553.
30. Huppertz, B., Frank, H. G., Kingdom, J. C., Reister, F., and Kaufmann, P. (1998). Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta. Histochem. Cell Biol. 110, 495-508. doi: 10.1007/s004180050311.
31. Huppertz, B., and Kingdom, J. C. (2004). Apoptosis in the trophoblast-role of apoptosis in placental morphogenesis. J. Soc. Gynecol. Investig. 11, 353-362. doi: 10.1016/j.jsgi.2004.06.002.
32. Ingles, S. A., Ross, R. K., Yu, M. C., Irvine, R. A., La Pera, G., Haile, R. W., et al. (1997). Association of prostate cancer risk with genetic polymorphisms in vitamin D receptor and androgen receptor. J. Natl. Cancer Inst. 89, 166-170. doi: 10.1093/jnci/89.2.166.
33. Jurutka, P. W., Whitfield, G. K., Hsieh, J. C., Thompson, P. D., Haussler, C. A., and Haussler, M. R. (2001). Molecular nature of the vitamin D receptor and its role in regulation of gene expression. Rev. Endocr. Metab. Disord. 2, 203-216. doi: 10.1023/A:1010062929140.
34. Kaufmann, P., Black, S., and Huppertz, B. (2003). Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol. Reprod. 69, 1-7. doi: 10.1095/biolreprod.102.014977.
35. Kramer, M. S., Olivier, M., McLean, F. H., Willis, D. M., and Usher, R. H. (1990). Impact of intrauterine growth retardation and body proportionality on fetal and neonatal outcome. Pediatrics 86, 707-713.
36. Kumar, R., Cohen, W. R., Silva, P., and Epstein, F. H. (1979). Elevated 1, 25-dihydroxyvitamin D plasma levels in normal human pregnancy and lactation. J. Clin. Invest. 63, 342-344. doi: 10.1172/JCI109308.
37. Lyall, F., Bulmer, J. N., Kelly, H., Duffie, E., and Robson, S. C. (1999). Human trophoblast invasion and spiral artery transformation: the role of nitric oxide. Am. J. Pathol. 154, 1105-1114. doi: 10.1016/S0002-9440(10)65363-1.
38. Ma, R., Gu, Y., Zhao, S., Sun, J., Groome, L. J., and Wang, Y. (2012). Expressions of vitamin D metabolic components VDBP, CYP2R1, CYP27B1, CYP24A1, and VDR in placentas from normal and preeclamptic pregnancies. Am. J. Physiol. Endocrinol. Metab. 303, E928-E935. doi: 10.1152/ajpendo.00279.2012.
39. Matte, T. D., Bresnahan, M., Begg, M. D., and Susser, E. (2001). Influence of variation in birth weight within normal range and within sibships on IQ at age 7 years: cohort study. BMJ 323, 310-314. doi: 10.1136/bmj.323.7308.310.
40. McGrath, J. J., Saha, S., Burne, T. H., and Eyles, D. W. (2010). A systematic review of the association between common single nucleotide polymorphisms and 25-hydroxyvitamin D concentrations. J. Steroid Biochem. Mol. Biol. 121, 471-477. doi: 10.1016/j.jsbmb.2010.03.073.
41. McIntire, D. D., Bloom, S. L., Casey, B. M., and Leveno, K. J. (1999). Birth weight in relation to morbidity and mortality among newborn infants. N. Engl. J. Med. 340, 1234-1238. doi: 10.1056/NEJM199904223401603.
42. Mi, S., Lee, X., Li, X., Veldman, G. M., Finnerty, H., Racie, L., et al. (2000). Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403, 785-789. doi: 10.1038/35001608.
43. Morley, R., Carlin, J. B., Pasco, J. A., Wark, J. D., and Ponsonby, A. L. (2009). Maternal 25-hydroxyvitamin D concentration and offspring birth size: effect modification by infant VDR genotype. Eur. J. Clin. Nutr. 63, 802-804. doi: 10.1038/ejcn.2008.55.
44. Morrish, D. W., Dakour, J., and Li, H. (1998). Functional regulation of human trophoblast differentiation. J. Reprod. Immunol. 39, 179-195. doi: 10.1016/S0165-0378(98)00021-7.
45. Nelissen, E. C., Van Montfoort, A. P., Dumoulin, J. C., and Evers, J. L. (2011). Epigenetics and the placenta. Hum. Reprod. Update 17, 397-417. doi: 10.1093/humupd/dmq052.
46. Newhouse, S. M., Davidge, S. T., Winkler-Lowen, B., Demianczuk, N., and Guilbert, L. J. (2007). In vitro differentiation of villous trophoblasts from pregnancies complicated by intrauterine growth restriction with and without pre-eclampsia. Placenta 28, 999-1003. doi: 10.1016/j.placenta.2007.04.008.
47. Nguyen, T., Yong, H., Borg, A., Brennecke, S., and Murthi, P. (2015b). Decreased placental vitamin D receptor contributes to aberrant cell-cycle gene regulation in human idiopathic fetal growth restriction. Placenta 36, A44. doi: 10.1016/j.placenta.2015.07.318.
48. Nguyen, T. P. H., Yong, H. E. J., Chollangi, T., Borg, A. J., Brennecke, S. P., and Murthi, P. (2015a). Placental vitamin D receptor expression is decreased in human idiopathic fetal growth restriction. J. Mol. Med. 93, 795-805. doi: 10.1007/s00109-015-1267-1.
49. Niimi, T., Tomita, H., Sato, S., Kawaguchi, H., Akita, K., Maeda, H., et al. (1999). Vitamin D receptor gene polymorphism in patients with sarcoidosis. Am. J. Respir. Crit. Care Med. 160, 1107-1109. doi: 10.1164/ajrccm.160.4.9811096.
50. Norman, A. W. (2012). The history of the discovery of vitamin D and its daughter steroid hormone. Ann. Nutr. Metab. 61, 199-206. doi: 10.1159/000343104.
51. Novakovic, B., Sibson, M., Ng, H. K., Manuelpillai, U., Rakyan, V., Down, T., et al. (2009). Placenta-specific methylation of the vitamin D 24-hydroxylase gene: implications for feedback autoregulation of active vitamin D levels at the fetomaternal interface. J. Biol. Chem. 284, 14838-14848. doi: 10.1074/jbc.M809542200.
52. Omdahl, J. L., Morris, H. A., and May, B. K. (2002). Hydroxylase enzymes of the vitamin D pathway: expression, function, and regulation. Annu. Rev. Nutr. 22, 139-166. doi: 10.1146/annurev.nutr.22.120501.150216.
53. Pathirage, N. A., Cocquebert, M., Sadovsky, Y., Abumaree, M., Manuelpillai, U., Borg, A., et al. (2013). Homeobox gene transforming growth factor beta-induced factor-1 (TGIF-1) is a regulator of villous trophoblast differentiation and its expression is increased in human idiopathic fetal growth restriction. Mol. Hum. Reprod. 19, 665-675. doi: 10.1093/molehr/gat042.
54. Paulson, S. K., and Deluca, H. F. (1986). Vitamin D metabolism during pregnancy. Bone 7, 331-336. doi: 10.1016/8756-3282(86)90252-8.
55. Ponsonby, A. L., Lucas, R. M., Lewis, S., and Halliday, J. (2010). Vitamin D status during pregnancy and aspects of offspring health. Nutrients 2, 389-407. doi: 10.3390/nu2030389.
56. Pospechova, K., Rozehnal, V., Stejskalova, L., Vrzal, R., Pospisilova, N., Jamborova, G., et al. (2009). Expression and activity of vitamin D receptor in the human placenta and in choriocarcinoma BeWo and JEG-3 cell lines. Mol. Cell. Endocrinol. 299, 178-187. doi: 10.1016/j.mce.2008.12.003.
57. Robinson, C. J., Alanis, M. C., Wagner, C. L., Hollis, B. W., and Johnson, D. D. (2010). Plasma 25-hydroxyvitamin D levels in early-onset severe preeclampsia. Am. J. Obstet. Gynecol. 203, 366.e1-366.e6. doi: 10.1016/j.ajog.2010.06.036.
58. Robinson, J. S., Moore, V. M., Owens, J. A., and McMillen, I. C. (2000). Origins of fetal growth restriction. Eur. J. Obstet. Gynecol. Reprod. Biol. 92, 13-19. doi: 10.1016/S0301-2115(00)00421-8.
59. Saffery, R., Ellis, J., and Morley, R. (2009). A convergent model for placental dysfunction encompassing combined sub-optimal one-carbon donor and vitamin D bioavailability. Med. Hypotheses 73, 1023-1028. doi: 10.1016/j.mehy.2009.03.057.
60. Salafia, C. M., Pezzullo, J. C., Minior, V. K., and Divon, M. Y. (1997). Placental pathology of absent and reversed end-diastolic flow in growth-restricted fetuses. Obstet. Gynecol. 90, 830-836. doi: 10.1016/S0029-7844(97)00473-0.
61. Samuel, S., and Sitrin, M. D. (2008). Vitamin D's role in cell proliferation and differentiation. Nutr. Rev. 66, S116-S124. doi: 10.1111/j.1753-4887.2008.00094.x.
62. Sandovici, I., Hoelle, K., Angiolini, E., and Constancia, M. (2012). Placental adaptations to the maternal-fetal environment: implications for fetal growth and developmental programming. Reprod. Biomed. Online 25, 68-89. doi: 10.1016/j.rbmo.2012.03.017.
63. Sankaran, S., and Kyle, P. M. (2009). Aetiology and pathogenesis of IUGR. Best Pract. Res. Clin. Obstet. Gynaecol. 23, 765-777. doi: 10.1016/j.bpobgyn.2009.05.003.
64. Scifres, C. M., and Nelson, D. M. (2009). Intrauterine growth restriction, human placental development and trophoblast cell death. J. Physiol. 587, 3453-3458. doi: 10.1113/jphysiol.2009.173252.
65. Shahbazi, M., Jeddi-Tehrani, M., Zareie, M., Salek-Moghaddam, A., Akhondi, M. M., Bahmanpoor, M., et al. (2011). Expression profiling of vitamin D receptor in placenta, decidua and ovary of pregnant mice. Placenta 32, 657-664. doi: 10.1016/j.placenta.2011.06.013.
66. Shin, J. S., Choi, M. Y., Longtine, M. S., and Nelson, D. M. (2010). Vitamin D effects on pregnancy and the placenta. Placenta 31, 1027-1034. doi: 10.1016/j.placenta.2010.08.015.
67. Stephanou, A., Ross, R., and Handwerger, S. (1994). Regulation of human placental lactogen expression by 1, 25-dihydroxyvitamin D3. Endocrinology 135, 2651-2656.
68. Tarcin, O., Yavuz, D. G., Ozben, B., Telli, A., Ogunc, A. V., Yuksel, M., et al. (2009). Effect of vitamin D deficiency and replacement on endothelial function in asymptomatic subjects. J. Clin. Endocrinol. Metab. 94, 4023-4030. doi: 10.1210/jc.2008-1212.
69. Taylor, D. J., and Howie, P. W. (1989). Fetal growth achievement and neurodevelopmental disability. Br. J. Obstet. Gynaecol. 96, 789-794. doi: 10.1111/j.1471-0528.1989.tb03317.x.
70. Tuan, R. S., Moore, C. J., Brittingham, J. W., Kirwin, J. J., Akins, R. E., and Wong, M. (1991). In vitro study of placental trophoblast calcium uptake using JEG-3 human choriocarcinoma cells. J. Cell Sci. 98(Pt 3), 333-342.
71. Vargas, A., Moreau, J., Le Bellego, F., Lafond, J., and Barbeau, B. (2008). Induction of trophoblast cell fusion by a protein tyrosine phosphatase inhibitor. Placenta 29, 170-174. doi: 10.1016/j.placenta.2007.10.012.
72. Vik, T., Markestad, T., Ahlsten, G., Gebre-Medhin, M., Jacobsen, G., Hoffman, H. J., et al. (1997). Body proportions and early neonatal morbidity in small-for-gestational-age infants of successive births. Acta Obstet. Gynecol. Scand. Suppl. 165, 76-81.
73. Wei, S. Q., Qi, H. P., Luo, Z. C., and Fraser, W. D. (2013). Maternal vitamin D status and adverse pregnancy outcomes: a systematic review and meta-analysis. J. Matern. Fetal Neonatal Med. 26, 889-899. doi: 10.3109/14767058.2013.765849.
74. Weisman, Y., Harell, A., Edelstein, S., David, M., Spirer, Z., and Golander, A. (1979). 1 alpha, 25-Dihydroxyvitamin D3 and 24, 25-dihydroxyvitamin D3 in vitro synthesis by human decidua and placenta. Nature 281, 317-319. doi: 10.1038/281317a0.
75. Weisman, Y., Sapir, R., Harell, A., and Edelstein, S. (1976). Maternal-perinatal interrelationships of vitamin D metabolism in rats. Biochim. Biophys. Acta 428, 388-395. doi: 10.1016/0304-4165(76)90046-5.
76. Whitfield, G. K., Remus, L. S., Jurutka, P. W., Zitzer, H., Oza, A. K., Dang, H. T., et al. (2001). Functionally relevant polymorphisms in the human nuclear vitamin D receptor gene. Mol. Cell. Endocrinol. 177, 145-159. doi: 10.1016/S0303-7207(01)00406-3.
77. Yu, C. K., Ertl, R., Skyfta, E., Akolekar, R., and Nicolaides, K. H. (2013). Maternal serum vitamin D levels at 11-13 weeks of gestation in preeclampsia. J. Hum. Hypertens. 27, 115-118. doi: 10.1038/jhh.2012.1.
78. Zehnder, D., Evans, K. N., Kilby, M. D., Bulmer, J. N., Innes, B. A., Stewart, P. M., et al. (2002). The ontogeny of 25-hydroxyvitamin D(3) 1alpha-hydroxylase expression in human placenta and decidua. Am. J. Pathol. 161, 105-114. doi: 10.1016/S0002-9440(10)64162-4.