Placental vitamin D receptor (VDR) expression is related to neonatal vitamin D status, placental calcium transfer, and fetal bone length in pregnant adolescents

FASEB Journal

Volumn 28, Issue 5, 2014, Pages 2029-2037

  Young, Bridget E ^a   Cooper, Elizabeth M ^b   McIntyre, Allison W ^b   Kent, Tera ^a   Witter, Frank ^c   Harris, Z Leah ^c   O'Brien, Kimberly O ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

1,25(OH)2D; 25(OH)D; Calcidiol; Gestation

Indexed keywords

25 HYDROXYVITAMIN D; CALCITRIOL; CALCIUM; PARATHYROID HORMONE; VITAMIN D RECEPTOR;

ADOLESCENT; ADOLESCENT PREGNANCY; ARTICLE; BONE DEVELOPMENT; BONE GROWTH; BONE LENGTH; CALCIUM TRANSPORT; CONTROLLED STUDY; FEMALE; FEMUR; FETUS DEVELOPMENT; GENE EXPRESSION; HUMAN; HUMAN TISSUE; LABOR; LONG BONE; MATERNAL SERUM; PLACENTA; PLACENTA CIRCULATION; PLACENTA FUNCTION; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; UMBILICAL CORD BLOOD;

1,25(OH)2D; 25(OH)D; CALCIDIOL; GESTATION;

ADMINISTRATION, ORAL; ADOLESCENT; BONE DEVELOPMENT; CALCIUM; CALCIUM ISOTOPES; COHORT STUDIES; DIET; FEMALE; FETAL BLOOD; FETUS; GENE EXPRESSION REGULATION; HUMANS; MATERNAL EXPOSURE; MATERNAL-FETAL EXCHANGE; PARATHYROID HORMONE; PLACENTA; PREGNANCY; RECEPTORS, CALCITRIOL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS; VITAMIN D;

EID: 84901049782     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-246736     Document Type: Article

References (48)

1. Jansson, T., and Powell, T. L. (2006) IFPA 2005 Award in Placentology Lecture. Human placental transport in altered fetal growth: does the placenta function as a nutrient sensor? A review. Placenta 27(Suppl. A), S91-S97
2. Sibley, C. P., Brownbill, P., Dilworth, M., and Glazier, J. D. (2010) Review: adaptation in placental nutrient supply to meet fetal growth demand: implications for programming. Placenta 31(Suppl.), S70-S74
3. Lewis, S., Lucas, R. M., Halliday, J., and Ponsonby, A. L. (2010) Vitamin D deficiency and pregnancy: from preconception to birth. Mol. Nutr. Food Res. 54, 1092-1102
4. Wagner, C. L., Taylor, S. N., Dawodu, A., Johnson, D. D., and Hollis, B. W. (2012) Vitamin D and its role during pregnancy in attaining optimal health of mother and fetus. Nutrients 4, 208-230
5. Brannon, P. M., and Picciano, M. F. (2011) Vitamin D in pregnancy and lactation in humans. Annu. Rev. Nutr. 31, 89-115
6. Kovacs, C. S. (2012) The role of vitamin D in pregnancy and lactation: insights from animal models and clinical studies. Annu. Rev. Nutr. 32, 97-123
7. Mahon, P., Harvey, N., Crozier, S., Inskip, H., Robinson, S., Arden, N., Swaminathan, R., Cooper, C., Godfrey, K., and SWS Study Group (2009) Low maternal vitamin D status and fetal bone development: cohort study. J. Bone Miner. Res. 25, 14-19
8. Namgung, R., and Tsang, R. C. (2000) Factors affecting newborn bone mineral content: in utero effects on newborn bone mineralization. Proc. Nutr. Soc. 59, 55-63
9. Morley, R., Carlin, J. B., Pasco, J. A., and Wark, J. D. (2006) Maternal 25-hydroxyvitamin D and parathyroid hormone concentrations and offspring birth size. J. Clin. Endocrinol. Metab. 91, 906-912
10. Javaid, M. K., Crozier, S. R., Harvey, N. C., Gale, C. R., Dennison, E. M., Boucher, B. J., Arden, N. K., Godfrey, K. M., Cooper, C., and Princess Anne Hospital Study Group (2006) Maternal vitamin D status during pregnancy and childhood bone mass at age 9 years: a longitudinal study. Lancet 367, 36-43
11. Young, B. E., McNanley, T. J., Cooper, E. M., McIntyre, A. W., Witter, F., Harris, Z. L., and O'Brien, K. O. (2012) Maternal vitamin D status and calcium intake interact to affect fetal skeletal growth in utero in pregnant adolescents. Am. J. Clin. Nutr. 95, 1103-1112
12. Karras, S. N., Anagnostis, P., Bili, E., Naughton, D., Petroczi, A., Papadopoulou, F., and Goulis, D. G. (2013) Maternal vitamin D status in pregnancy and offspring bone development: the unmet needs of vitamin D era. [E-pub ahead of print] Osteoporos. Int. doi: 10.1007/s00198-013-2468-5
13. Evans, K. N., Bulmer, J. N., Kilby, M. D., and Hewison, M. (2004) Vitamin D and placental-decidual function. J. Soc. Gynecol. Investig. 11, 263-271
14. Zehnder, D., Evans, K. N., Kilby, M. D., Bulmer, J. N., Innes, B. A., Stewart, P. M., and Hewison, M. (2002) The ontogeny of 25-hydroxyvitamin D(3) 1alpha-hydroxylase expression in human placenta and decidua. Am. J. Pathol. 161, 105-114
15. Pospechova, K., Rozehnal, V., Stejskalova, L., Vrzal, R., Pospisilova, N., Jamborova, G., May, K., Siegmund, W., Dvorak, Z., Nachtigal, P., Semecky, V., and Pavek, P. (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
16. 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
17. Novakovic, B., Sibson, M., Ng, H. K., Manuelpillai, U., Rakyan, V., Down, T., Beck, S., Fournier, T., Evain-Brion, D., Dimitriadis, E., Craig, J. M., Morley, R., and Saffery, R. (2009) Placentaspecific 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
18. Suzuki, Y., Kovacs, C. S., Takanaga, H., Peng, J. B., Landowski, C. P., and Hediger, M. A. (2008) Calcium channel TRPV6 is involved in murine maternal-fetal calcium transport. J. Bone Miner. Res. 23, 1249-1256
19. Belkacemi, L., Zuegel, U., Steinmeyer, A., Dion, J. P., and Lafond, J. (2005) Calbindin-D28k (CaBP28k) identification and regulation by 1,25-dihydroxyvitamin D3 in human choriocarcinoma cell line JEG-3. Mol. Cell. Endocrinol. 236, 31-41
20. 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, 333-342
21. Young, B., McNanley, T., Cooper, E., McIntyre, A., Witter, F., Harris, Z., and O'Brien, K. (2012) Vitamin D insufficiency is prevalent and vitamin D is inversely associated with PTH and calcitriol in pregnant adolescents. J. Bone Miner. Res. 127, 177-186
22. Essley, B. V., McNanley, T., Cooper, E., McIntyre, A. W., Witter, F., Harris, Z. L., and O'Brien, K. O. (2011) Osteoprotegerin (OPG) Differs by race and is related to infant birth weight Z-score in pregnant adolescents. J. Dev. Origins Health Dis. 2, 272-279
23. O'Brien, K. O., Shuang, L., Cao, C., Kent, T., Young, B. E., Quennan, R., Pressman, E., and Cooper, E. (2013) Placental CYP27B1 and CYP24A1 expression in human placental tisse and their association with maternal and neonatal calcitropic hormones. [E-pub ahead of print] J. Clin. Endocrinol. Metab. doi: 10.1210/jc.2013-1366
24. Chang, S. C., O'Brien, K. O., Nathanson, M. S., Caulfield, L. E., Mancini, J., and Witter, F. R. (2003) Fetal femur length is influenced by maternal dairy intake in pregnant African American adolescents. Am. J. Clin. Nutr. 77, 1248-1254
25. Kramer, M. S., Platt, R. W., Wen, S. W., Joseph, K. S., Allen, A., Abrahamowicz, M., Blondel, B., Breart, G., and Fetal/Infant Health Study Group of the Canadian Perinatal Surveillance System (2001) A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics 108, E35
26. Institute of Medicine (2011) Dietary Reference Intakes for Calcium and Vitamin D. National Academy of Sciences Press, Washington, DC
27. Chen, T. C., Turner, A. K., and Holick, M. F. (1990) A method for the determination of the circulating concentration of 1,25-dihydroxyvitamin D. J. Nutr. Biochem. 1, 320-327
28. Jaacks, L. M., Young, M. F., Essley, B. V., McNanley, T. J., Cooper, E. M., Pressman, E. K., McIntyre, A. W., Orlando, M. S., Abkowitz, J. L., Guillet, R., and O'Brien, K. O. (2011) Placental expression of the heme transporter, feline leukemia virus subgroup c receptor, is related to maternal iron status in pregnant adolescents. J. Nutr. 141, 1267-1272
29. Yergey, A. L., Vieira, N. E., and Covell, D. G. (1987) Direct measurement of dietary fractional absorption using calcium isotopic tracers. Biomed. Environ. Mass. Spectrom. 14, 603-607
30. Abrams, S. A., Esteban, N. V., Vieira, N. E., Sidbury, J. B., Specker, B. L., and Yergey, A. L. (1992) Developmental changes in calcium kinetics in children assessed using stable isotopes. J. Bone Miner. Res. 7, 287-293
31. Kovacs, C. S., and Kronenberg, H. M. (1997) Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr. Rev. 18, 832-872
32. Moore, E. S., Langman, C. B., Favus, M. J., and Coe, F. L. (1985) Role of fetal 1,25-dihydroxyvitamin D production in intrauterine phosphorus and calcium homeostasis. Pediatr. Res. 19, 566-569
33. Pike, J. W., and Meyer, M. B. (2010) The vitamin D receptor: new paradigms for the regulation of gene expression by 1,25-dihydroxyvitamin D(3). Endocrinol. Metab. Clin. North Am. 39, 255-269
34. Shany, S., Biale, Y., Zuili, I., Yankowitz, N., Berry, J. L., and Mawer, E. B. (1984) Feto-maternal relationships between vitamin D metabolites in Israeli Bedouins and Jews. Am.J. Clin. Nutr. 40, 1290-1294
35. Gertner, J. M., Glassman, M. S., Coustan, D. R., and Goodman, D. B. (1980) Fetomaternal vitamin D relationships at term. J. Pediatr. 97, 637-640
36. Markestad, T., Aksnes, L., Ulstein, M., and Aarskog, D. (1984) 25-Hydroxyvitamin D and 1,25-dihydroxyvitamin D of D2 and D3 origin in maternal and umbilical cord serum after vitamin D2 supplementation in human pregnancy. Am. J. Clin. Nutr. 40, 1057-1063
37. Hollis, B. W., Johnson, D., Hulsey, T. C., Ebeling, M., and Wagner, C. L. (2011) Vitamin D supplementation during pregnancy: Double blind, randomized clinical trial of safety and effectiveness. J. Bone Miner. Res. 26, 2341-2357
38. Meyer, M. B., Watanuki, M., Kim, S., Shevde, N. K., and Pike, J. W. (2006) The human transient receptor potential vanilloid type 6 distal promoter contains multiple vitamin D receptor binding sites that mediate activation by 1,25-dihydroxyvitamin D3 in intestinal cells. Mol. Endocrinol. 20, 1447-1461
39. Halhali, A., Figueras, A. G., Diaz, L., Avila, E., Barrera, D., Hernandez, G., and Larrea, F. (2010) Effects of calcitriol on calbindins gene expression and lipid peroxidation in human placenta. J. Steroid Biochem. Mol. Biol. 121, 448-451
40. Bond, H., Dilworth, M. R., Baker, B., Cowley, E., Requena Jimenez, A., Boyd, R. D., Husain, S. M., Ward, B. S., Sibley, C. P., and Glazier, J. D. (2008) Increased maternofetal calcium flux in parathyroid hormone-related protein-null mice. J. Physiol. 586, 2015-2025
41. Dilworth, M. R., Kusinski, L. C., Cowley, E., Ward, B. S., Husain, S. M., Constancia, M., Sibley, C. P., and Glazier, J. D. (2010) Placental-specific Igf2 knockout mice exhibit hypocalcemia and adaptive changes in placental calcium transport. Proc. Natl. Acad. Sci. U. S. A. 107, 3894-3899
42. Strid, H., Bucht, E., Jansson, T., Wennergren, M., and Powell, T. L. (2003) ATP dependent Ca2+ transport across basal membrane of human syncytiotrophoblast in pregnancies complicated by intrauterine growth restriction or diabetes. Placenta 24, 445-452
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
44. Fischer, D., Schroer, A., Ludders, D., Cordes, T., Bucker, B., Reichrath, J., and Friedrich, M. (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
45. Martin, R., Harvey, N. C., Crozier, S. R., Poole, J. R., Javaid, M. K., Dennison, E. M., Inskip, H. M., Hanson, M., Godfrey, K. M., Cooper, C., and Lewis, R. (2007) Placental calcium transporter (PMCA3) gene expression predicts intrauterine bone mineral accrual. Bone 40, 1203-1208
46. Kato, S., Yoshizazawa, T., Kitanaka, S., Murayama, A., and Takeyama, K. (2002) Molecular genetics of vitamin D-dependent hereditary rickets. Horm. Res. 57, 73-78
47. Kovacs, C. S., Woodland, M. L., Fudge, N. J., and Friel, J. K. (2005) The vitamin D receptor is not required for fetal mineral homeostasis or for the regulation of placental calcium transfer in mice. Am. J. Physiol. Endocrinol. Metab. 289, E133-E144
48. Rummens, K., van Cromphaut, S. J., Carmeliet, G., van Herck, E., van Bree, R., Stockmans, I., Bouillon, R., and Verhaeghe, J. (2003) Pregnancy in mice lacking the vitamin D receptor: normal maternal skeletal response, but fetal hypomineralization rescued by maternal calcium supplementation. Pediatr. Res. 54, 466-473