Evidence of sexual dimorphism in placental vitamin D metabolism: Testosterone inhibits calcitriol-dependent cathelicidin expression

Journal of Steroid Biochemistry and Molecular Biology

Volumn 163, Issue , 2016, Pages 173-182

  Olmos Ortiz, Andrea ^a,f   García Quiroz, Janice ^a   López Marure, Rebeca ^b   González Curiel, Irma ^c   Rivas Santiago, Bruno ^d   Olivares, Aleida ^e   Avila, Euclides ^a   Barrera, David ^a   Halhali, Ali ^a   Caldiño, Felipe ^d   Larrea, Fernando ^a   Díaz, Lorenza ^a  

^a INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^b INSTITUTO NACIONAL DE CARDIOLOGÍA IGNACIO CHÁVEZ   (Mexico)

^c UNIVERSIDAD AUTÓNOMA DE ZACATECAS   (Mexico)

^d INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^e Unidad de Investigación Médica en Medicina Reproductiva   (Mexico)

^f UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Androgen; cAMP; Cord blood; LL 37; Male

Indexed keywords

ANDROGEN RECEPTOR; CALCIFEDIOL; CALCITRIOL; CATHELICIDIN; CHORIONIC GONADOTROPIN; COLECALCIFEROL 24 HYDROXYLASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOCHROME P450; CYTOCHROME P450 FAMILY 27 SUBFAMILY B MEMBER 1; CYTOKERATIN 7; ESTRADIOL; TESTOSTERONE; UNCLASSIFIED DRUG; AR PROTEIN, HUMAN; CALCIDIOL 1 MONOOXYGENASE; CATHELICIDIN ANTIMICROBIAL PEPTIDE; CREB1 PROTEIN, HUMAN; CYP24A1 PROTEIN, HUMAN; CYP27B1 PROTEIN, HUMAN; VITAMIN D;

ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; MALE; NEWBORN; PLACENTA; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TROPHOBLAST; UMBILICAL CORD BLOOD; VITAMIN D METABOLISM; CYTOLOGY; DRUG EFFECTS; FETUS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PREGNANCY; PRIMARY CELL CULTURE; SEXUAL DEVELOPMENT;

25-HYDROXYVITAMIN D3 1-ALPHA-HYDROXYLASE; CATHELICIDINS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEMALE; FETUS; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNITY, INNATE; MALE; PREGNANCY; PRIMARY CELL CULTURE; RECEPTORS, ANDROGEN; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; TESTOSTERONE; TROPHOBLASTS; VITAMIN D; VITAMIN D3 24-HYDROXYLASE;

EID: 84976477174     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2016.05.017     Document Type: Article

References (58)

1. [1] Klein, S.L., The effects of hormones on sex differences in infection: from genes to behavior. Neurosci. Biobehav. Rev. 24 (2000), 627–638.
2. [2] Clifton, V.L., Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta(Suppl. 31), 2010, S33–S39.
3. [3] Challis, J., Newnham, J., Petraglia, F., Yeganegi, M., Bocking, A., Fetal sex and preterm birth. Placenta 34 (2013), 95–99.
4. [4] Elsmen, E., Kallen, K., Marsal, K., Hellstrom-Westas, L., Fetal gender and gestational-age-related incidence of pre-eclampsia. Acta Obstet. Gynecol. Scand. 85 (2006), 1285–1291.
5. [5] Vatten, L.J., Skjaerven, R., Offspring sex and pregnancy outcome by length of gestation. Early Hum. Dev. 76 (2004), 47–54.
6. [6] Goldenberg, R.L., Andrews, W.W., Faye-Petersen, O.M., Goepfert, A.R., Cliver, S.P., Hauth, J.C., The Alabama preterm birth study: intrauterine infection and placental histologic findings in preterm births of males and females less than 32 weeks. Am. J. Obstet. Gynecol. 195 (2006), 1533–1537.
7. [7] Muralimanoharan, S., Maloyan, A., Myatt, L., Evidence of sexual dimorphism in the placental function with severe preeclampsia. Placenta 34 (2013), 1183–1189.
8. [8] Diaz, L., Noyola-Martinez, N., Barrera, D., Hernandez, G., Avila, E., Halhali, A., Larrea, F., Calcitriol inhibits TNF-alpha-induced inflammatory cytokines in human trophoblasts. J. Reprod. Immunol. 81 (2009), 17–24.
9. [9] Noyola-Martinez, N., Diaz, L., Avila, E., Halhali, A., Larrea, F., Barrera, D., Calcitriol downregulates TNF-alpha and IL-6 expression in cultured placental cells from preeclamptic women. Cytokine 61 (2013), 245–250.
10. [10] Bandurska, K., Berdowska, A., Barczynska-Felusiak, R., Krupa, P., Unique features of human cathelicidin LL-37. Biofactors 41 (2015), 289–300.
11. [11] Slominski, A.T., Kim, T.K., Shehabi, H.Z., Semak, I., Tang, E.K., Nguyen, M.N., Benson, H.A., Korik, E., Janjetovic, Z., Chen, J., Yates, C.R., Postlethwaite, A., Li, W., Tuckey, R.C., In vivo evidence for a novel pathway of vitamin D(3) metabolism initiated by P450scc and modified by CYP27B1. FASEB J. 26 (2012), 3901–3915.
12. [12] Slominski, A., Semak, I., Zjawiony, J., Wortsman, J., Li, W., Szczesniewski, A., Tuckey, R.C., The cytochrome P450scc system opens an alternate pathway of vitamin D3 metabolism. FEBS J. 272 (2005), 4080–4090.
13. [13] Slominski, A.T., Kim, T.K., Li, W., Postlethwaite, A., Tieu, E.W., Tang, E.K., Tuckey, R.C., Detection of novel CYP11A1-derived secosteroids in the human epidermis and serum and pig adrenal gland. Sci. Rep., 5, 2015, 14875.
14. [14] Slominski, A.T., Li, W., Kim, T.K., Semak, I., Wang, J., Zjawiony, J.K., Tuckey, R.C., Novel activities of CYP11A1 and their potential physiological significance. J. Steroid Biochem. Mol. Biol. 151 (2015), 25–37.
15. [15] Evans, K.N., Nguyen, L., Chan, J., Innes, B.A., Bulmer, J.N., Kilby, M.D., Hewison, M., Effects of 25-hydroxyvitamin D3 and 1,25-dihydroxyvitamin D3 on cytokine production by human decidual cells. Biol. Reprod. 75 (2006), 816–822.
16. [16] Liu, N., Kaplan, A.T., Low, J., Nguyen, L., Liu, G.Y., Equils, O., Hewison, M., Vitamin D induces innate antibacterial responses in human trophoblasts via an intracrine pathway. Biol. Reprod. 80 (2009), 398–406.
17. [17] Avila, E., Diaz, L., Barrera, D., Halhali, A., Mendez, I., Gonzalez, L., Zuegel, U., Steinmeyer, A., Larrea, F., Regulation of vitamin D hydroxylases gene expression by 1,25-dihydroxyvitamin D3 and cyclic AMP in cultured human syncytiotrophoblasts. J. Steroid Biochem. Mol. Biol. 103 (2007), 90–96.
18. [18] Avila, E., Diaz, L., Halhali, A., Larrea, F., 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 (2004), 115–119.
19. [19] Weedon-Fekjaer, M.S., Tasken, K., Review: spatiotemporal dynamics of hCG/cAMP signaling and regulation of placental function. Placenta(Suppl. 33), 2012, S87–S91.
20. [20] Fix, C., Jordan, C., Cano, P., Walker, W.H., Testosterone activates mitogen-activated protein kinase and the cAMP response element binding protein transcription factor in Sertoli cells. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 10919–10924.
21. [21] Kong, X.F., Zhu, X.H., Pei, Y.L., Jackson, D.M., Holick, M.F., Molecular cloning, characterization, and promoter analysis of the human 25-hydroxyvitamin D3-1alpha-hydroxylase gene. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 6988–6993.
22. [22] Zierold, C., Darwish, H.M., DeLuca, H.F., Identification of a vitamin D-response element in the rat calcidiol (25-hydroxyvitamin D3) 24-hydroxylase gene. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 900–902.
23. [23] Kliman, H.J., Nestler, J.E., Sermasi, E., Sanger, J.M., Strauss, J.F. 3rd, Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 118 (1986), 1567–1582.
24. [24] Tscherning-Casper, C., Papadogiannakis, N., Anvret, M., Stolpe, L., Lindgren, S., Bohlin, A.B., Albert, J., Fenyo, E.M., The trophoblastic epithelial barrier is not infected in full-term placentae of human immunodeficiency virus-seropositive mothers undergoing antiretroviral therapy. J. Virol. 73 (1999), 9673–9678.
25. [25] Olmos-Ortiz, A., Noyola-Martinez, N., Barrera, D., Zaga-Clavellina, V., Avila, E., Halhali, A., Biruete, B., Larrea, F., Diaz, L., IL-10 inhibits while calcitriol reestablishes placental antimicrobial peptides gene expression. J. Steroid Biochem. Mol. Biol. 148 (2015), 187–193.
26. [26] Olivares, A., Mendez, J.P., Zambrano, E., Cardenas, M., Tovar, A., Perera-Marin, G., Ulloa-Aguirre, A., Reproductive axis function and gonadotropin microheterogeneity in a male rat model of diet-induced obesity. Gen. Comp. Endocrinol. 166 (2010), 356–364.
27. [27] Castaneda-Delgado, J.E., Miranda-Castro, N.Y., Gonzalez-Amaro, R., Gonzalez-Curiel, I., Montoya-Rosales, A., Rivas-Calderon, B., Rivas-Santiago, B., Production of antimicrobial peptides is preserved in aging. Clin. Immunol. 148 (2013), 198–205.
28. [28] Rettew, J.A., Huet-Hudson, Y.M., Marriott, I., Testosterone reduces macrophage expression in the mouse of toll-like receptor 4, a trigger for inflammation and innate immunity. Biol. Reprod. 78 (2008), 432–437.
29. [29] Correale, J., Ysrraelit, M.C., Gaitan, M.I., Gender differences in 1,25-dihydroxyvitamin D3 immunomodulatory effects in multiple sclerosis patients and healthy subjects. J. Immunol. 185 (2010), 4948–4958.
30. [30] Pike, J.W., Spanos, E., Colston, K.W., MacIntyre, I., Haussler, M.R., Influence of estrogen on renal vitamin D hydroxylases and serum 1alpha 25-(OH)2D3 in chicks. Am. J. Physiol. 235 (1978), E338–343.
31. [31] Cheema, C., Grant, B.F., Marcus, R., Effects of estrogen on circulating free and total 1,25-dihydroxyvitamin D and on the parathyroid-vitamin D axis in postmenopausal women. J. Clin. Invest. 83 (1989), 537–542.
32. [32] Aronica, S.M., Kraus, W.L., Katzenellenbogen, B.S., Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 8517–8521.
33. [33] Lechner, D., Bajna, E., Adlercreutz, H., Cross, H.S., Genistein and 17beta-estradiol but not equol, regulate vitamin D synthesis in human colon and breast cancer cells. Anticancer Res. 26 (2006), 2597–2603.
34. [34] Keelan, J.A., Mattes, E., Tan, H., Dinan, A., Newnham, J.P., Whitehouse, A.J., Jacoby, P., Hickey, M., Androgen concentrations in umbilical cord blood and their association with maternal, fetal and obstetric factors. PLoS One, 7, 2012, e42827.
35. [35] Wang, T.T., Nestel, F.P., Bourdeau, V., Nagai, Y., Wang, Q., Liao, J., Tavera-Mendoza, L., Lin, R., Hanrahan, J.W., Mader, S., White, J.H., Cutting edge: 1,25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J. Immunol. 173 (2004), 2909–2912.
36. [36] Klaffenbach, D., Friedrich, D., Strick, R., Strissel, P.L., Beckmann, M.W., Rascher, W., Gessner, A., Dotsch, J., Meissner, U., Schnare, M., Contribution of different placental cells to the expression and stimulation of antimicrobial proteins (AMPs). Placenta 32 (2016), 830–837.
37. [37] Chakraborty, K., Ghosh, S., Koley, H., Mukhopadhyay, A.K., Ramamurthy, T., Saha, D.R., Mukhopadhyay, D., Roychowdhury, S., Hamabata, T., Takeda, Y., Das, S., Bacterial exotoxins downregulate cathelicidin (hCAP-18/LL-37) and human beta-defensin 1 (HBD-1) expression in the intestinal epithelial cells. Cell. Microbiol. 10 (2008), 2520–2537.
38. [38] Ron, M., Menczel, J., Schwartz, L., Palti, Z., Kidroni, G., Vitamin D3 metabolites in amniotic fluid in relation with maternal and fetal sera in term pregnancies. J. Perinat. Med. 15 (1987), 282–290.
39. [39] Gupta, M.M., Kuppuswamy, G., Subramanian, A.R., Transplacental transfer of 25-hydroxy-cholecalciferol. Postgrad. Med. J. 58 (1982), 408–410.
40. [40] Salamalekis, E., Bakas, P., Vitoratos, N., Eleptheriadis, M., Creatsas, G., Androgen levels in the third trimester of pregnancy in patients with preeclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 126 (2006), 16–19.
41. [41] Carlsen, S.M., Romundstad, P., Jacobsen, G., Early second-trimester maternal hyperandrogenemia and subsequent preeclampsia: a prospective study. Acta Obstet. Gynecol. Scand. 84 (2005), 117–121.
42. [42] Troisi, R., Potischman, N., Roberts, J.M., Ness, R., Crombleholme, W., Lykins, D., Siiteri, P., Hoover, R.N., Maternal serum oestrogen and androgen concentrations in preeclamptic and uncomplicated pregnancies. Int. J. Epidemiol. 32 (2003), 455–460.
43. [43] Tache, V., Baer, R.J., Currier, R.J., Li, C.S., Towner, D., Waetjen, L.E., Jelliffe-Pawlowski, L.L., Population-based biomarker screening and the development of severe preeclampsia in California. Am. J. Obstet. Gynecol. 211 (2014), 377.e1–377.e8.
44. [44] Hsu, T.Y., Lan, K.C., Tsai, C.C., Ou, C.Y., Cheng, B.H., Tsai, M.Y., Kang, H.Y., Tung, Y.H., Wong, Y.H., Huang, K.E., Expression of androgen receptor in human placentas from normal and preeclamptic pregnancies. Taiwan J. Obstet. Gynecol. 48 (2009), 262–267.
45. [45] Sathishkumar, K., Balakrishnan, M., Chinnathambi, V., Chauhan, M., Hankins, G.D., Yallampalli, C., Fetal sex-related dysregulation in testosterone production and their receptor expression in the human placenta with preeclampsia. J. Perinatol. 32 (2012), 328–335.
46. [46] Diaz, L., Arranz, C., Avila, E., Halhali, A., Vilchis, F., Larrea, F., Expression and activity of 25-hydroxyvitamin D-1 alpha-hydroxylase are restricted in cultures of human syncytiotrophoblast cells from preeclamptic pregnancies. J. Clin. Endocrinol. Metab. 87 (2002), 3876–3882.
47. [47] Halhali, A., Diaz, L., Barrera, D., Avila, E., Larrea, F., Placental calcitriol synthesis and IGF-I levels in normal and preeclamptic pregnancies. J. Steroid Biochem. Mol. Biol. 144:Pt. A (2014), 44–49.
48. [48] Halhali, A., Tovar, A.R., Torres, N., Bourges, H., Garabedian, M., Larrea, F., Preeclampsia is associated with low circulating levels of insulin-like growth factor I and 1,25-dihydroxyvitamin D in maternal and umbilical cord compartments. J. Clin. Endocrinol. Metab. 85 (2000), 1828–1833.
49. [49] Halhali, A., Diaz, L., Avila, E., Ariza, A.C., Garabedian, M., Larrea, F., Decreased fractional urinary calcium excretion and serum 1,25-dihydroxyvitamin D and IGF-I levels in preeclampsia. J. Steroid Biochem. Mol. Biol. 103 (2007), 803–806.
50. [50] Thys-Jacobs, S., Donovan, D., Papadopoulos, A., Sarrel, P., Bilezikian, J.P., Vitamin D and calcium dysregulation in the polycystic ovarian syndrome. Steroids 64 (1999), 430–435.
51. [51] Li, H.W., Brereton, R.E., Anderson, R.A., Wallace, A.M., Ho, C.K., Vitamin D deficiency is common and associated with metabolic risk factors in patients with polycystic ovary syndrome. Metabolism 60 (2011), 1475–1481.
52. [52] Koster, M.P., de Wilde, M.A., Veltman-Verhulst, S.M., Houben, M.L., Nikkels, P.G., van Rijn, B.B., Fauser, B.C., Placental characteristics in women with polycystic ovary syndrome. Hum. Reprod. 30 (2015), 2829–2837.
53. [53] Davidopoulou, S., Diza, E., Menexes, G., Kalfas, S., Salivary concentration of the antimicrobial peptide LL-37 in children. Arch. Oral Biol. 57 (2012), 865–869.
54. [54] Xue, Y., Ying, L., Horst, R.L., Watson, G., Goltzman, D., Androgens attenuate Vitamin D production induced by UVB irradiation of the skin of male mice by an enzymatic mechanism. J. Invest. Dermatol. 135 (2015), 3125–3132.
55. [55] Gombart, A.F., Borregaard, N., Koeffler, H.P., 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 J. 19 (2005), 1067–1077.
56. [56] Olmos-Ortiz, A., Avila, E., Durand-Carbajal, M., Diaz, L., Regulation of calcitriol biosynthesis and activity: focus on gestational vitamin D deficiency and adverse pregnancy outcomes. Nutrients 7 (2015), 443–480.
57. [57] Rajan, T.V., Nelson, F.K., Shultz, L.D., Shultz, K.L., Beamer, W.G., Yates, J., Greiner, D.L., Influence of gonadal steroids on susceptibility to Brugia malayi in scid mice. Acta Trop. 56 (1994), 307–314.
58. [58] Klein, S.L., Bird, B.H., Glass, G.E., Sex differences in Seoul virus infection are not related to adult sex steroid concentrations in Norway rats. J. Virol. 74 (2000), 8213–8217.