Calcium transport in male reproduction is possibly influenced by vitamin D and CaSR

in Journal of Endocrinology
Authors:
Ida Marie Boisen Group of Skeletal, Mineral, and Gonadal Endocrinology, Department of Growth and Reproduction, Copenhagen University Hospital – Rigshospitalet, Copenhagen, Denmark

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John Erik Nielsen Department of Growth and Reproduction, Copenhagen University Hospital – Rigshospitalet, Copenhagen, Denmark

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Lieve Verlinden Clinical and Experimental Endocrinology, Department of Chronic Diseases and Metabolism, KU Leuven, Leuven, Belgium

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https://orcid.org/0000-0002-9621-3662
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Mette Lorenzen Group of Skeletal, Mineral, and Gonadal Endocrinology, Department of Growth and Reproduction, Copenhagen University Hospital – Rigshospitalet, Copenhagen, Denmark

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Rune Holt Group of Skeletal, Mineral, and Gonadal Endocrinology, Department of Growth and Reproduction, Copenhagen University Hospital – Rigshospitalet, Copenhagen, Denmark

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Anja Pinborg The Fertility Clinic, Copenhagen University Hospital – Rigshospitalet, Copenhagen, Denmark
Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark

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Christine Hjorth Andreassen Group of Skeletal, Mineral, and Gonadal Endocrinology, Department of Growth and Reproduction, Copenhagen University Hospital – Rigshospitalet, Copenhagen, Denmark

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Anders Juul Department of Growth and Reproduction, Copenhagen University Hospital – Rigshospitalet, Copenhagen, Denmark
Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark

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Beate Lanske Division of Bone and Mineral Research, HSDM/HMS Harvard University, Boston, Massachusetts, USA

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Geert Carmeliet Clinical and Experimental Endocrinology, Department of Chronic Diseases and Metabolism, KU Leuven, Leuven, Belgium

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Martin Blomberg Jensen Group of Skeletal, Mineral, and Gonadal Endocrinology, Department of Growth and Reproduction, Copenhagen University Hospital – Rigshospitalet, Copenhagen, Denmark
Division of Bone and Mineral Research, HSDM/HMS Harvard University, Boston, Massachusetts, USA

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Correspondence should be addressed to M Blomberg Jensen: blombergjensen@gmail.com
DOI:
https://doi.org/10.1530/JOE-20-0321
Volume/Issue:
Volume 251: Issue 3
Article Type:
Research Article
Page Range:
207–222
Online Publication Date:
05 Nov 2021
Copyright:
© Society for Endocrinology 2021
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Vitamin D is important for gonadal function in rodents, and improvement of vitamin D status in men with low sperm counts increases live birth rate. Vitamin D is a regulator of transcellular calcium transport in the intestine and kidney and may influence the dramatic changes in the luminal calcium concentration in epididymis. Here, we show spatial expression in the male reproductive tract of vitamin D receptor (VDR)-regulated factors involved in calcium transport: transient receptor potential vanilloid 5/6 , sodium/calcium exchanger 1, plasma membrane calcium ATPase 1, calbindin D9k, calcium-sensing receptor (CaSR), and parathyroid hormone-related peptide (PTHrP) in mouse and human testis and epididymis. Testicular Casr expression was lower in Vdr ablated mice compared with controls. Moreover, expression levels of Casr and Pthrp were strongly correlated in both testis and epididymis and Pthrp was suppressed by 1,25(OH)2D3 in a spermatogonial cell line. The expression of CaSR in epididymis may be of greater importance than in the gonad in mice as germ cell-specific Casr deficient mice had no major reproductive phenotype, and coincubation with a CaSR-agonist had no effect on human sperm–oocyte binding. In humans, seminal calcium concentration between 5 and 10 mM was associated with a higher fraction of motile and morphologically normal sperm cells, and the seminal calcium concentration was not associated with serum calcium levels. In conclusion, VDR regulates CaSR and PTHrP, and both factors may be involved in the regulation of calcium transport in the male reproductive tract with possible implications for sperm function and storage.

Supplementary Materials

    • Supplementary figure 1 – Verification of antibodies in human kidney and intestine. The scale bar corresponds to 100 µm. Negative controls are shown as insets in the right upper corner of each image. Counterstaining with Mayer’s hematoxylin.
    • Supplementary figure 2 - Western blotting of CaSR in mouse testis with two different antibodies. Upper antibody: gift from W. Chang (C-term 1 made from the region N’-NSEDRFPQPERQKQ-C’ (Graca et al. 2016) (not commercially available)), lower: ab19347. Western blotting of kidney tissue from Casr+/+ or Casr-/- to confirm the validity of the antibodies. Testicular tissue from Casrfl/fl and Casrfl/fl; iVasa-Cre mice with knockdown of Casr. CaSR monomers and dimers should be detected at 140-160 and 260-300 kDa (arrows), respectively (Graca et al. 2016).
    • Supplementary Table 1 - Primer sequences used for gene expression analyses.
    • Supplementary Table 2 - Information on antibodies used for immunohistochemistry. Abbreviations: CIT: citrate buffer 10mM pH 6.0; TEG: Tris 10 mM, EGTA 0.5 mM, pH 8.5; MWO: microwave oven; PC: pressure cocker.

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Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© Society for Endocrinology 2021
Page(s):
16
Article Type:
Research Article
Received Date:
13 Sep 2021
Accepted Date:
05 Oct 2021
Print Publication Date:
01 Dec 2021
Online Publication Date:
05 Nov 2021
Keywords:
vitamin D; calcium; fertility; reproduction; testis; CaSR

  • Benn BS, Ajibade D, Porta A, Dhawan P, Hediger M, Peng JB, Jiang Y, Oh GT, Jeung EB & Lieben L et al.2008 Active intestinal calcium transport in the absence of transient receptor potential vanilloid type 6 and calbindin-D 9k. Endocrinology 149 3196–3205. (https://doi.org/10.1210/en.2007-1655)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Blomberg Jensen M 2014 Vitamin D and male reproduction. Nature Reviews: Endocrinology 10 175–186. (https://doi.org/10.1038/nrendo.2013.262)

  • Blomberg Jensen M, Nielsen JE, Jørgensen A, Rajpert-De Meyts E, Kristensen DM, Jørgensen N, Skakkebaek NE, Juul A & Leffers H 2010 Vitamin D receptor and vitamin D metabolizing enzymes are expressed in the human male reproductive tract. Human Reproduction 25 1303–1311. (https://doi.org/10.1093/humrep/deq024)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Blomberg Jensen M, Lieben L, Nielsen JE, Willems A, Jørgensen A, Juul A, Toppari J, Carmeliet G & Rajpert-De Meyts E 2013 Characterization of the testicular, epididymal and endocrine phenotypes in the Leuven Vdr-deficient mouse model: targeting estrogen signalling. Molecular and Cellular Endocrinology 377 93–102. (https://doi.org/10.1016/j.mce.2013.06.036)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Blomberg Jensen M, Lawaetz JG, Andersson AM, Petersen JH, Nordkap L, Bang AK, Ekbom P, Joensen UN, Prætorius L & Lundstrøm P et al.2016 Vitamin D deficiency and low ionized calcium are linked with semen quality and sex steroid levels in infertile men. Human Reproduction 31 1875–1885. (https://doi.org/10.1093/humrep/dew152)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Blomberg Jensen M, Lawaetz JG, Petersen JH, Juul A & Jørgensen N 2018 Effects of vitamin D supplementation on semen quality, reproductive hormones, and live birth rate: a randomized clinical trial. Journal of Clinical Endocrinology and Metabolism 103 870–881. (https://doi.org/10.1210/jc.2017-01656)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Blomberg Jensen M, Andreassen CH, Jørgensen A, Nielsen JE, Mortensen LJ, Boisen IM, Schwarz P, Toppari J, Baron R & Lanske B et al.2021 RANKL regulates male reproductive function. Nature Communications 12 1–15. (https://doi.org/10.1038/s41467-021-22734-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Boisen IM, Bøllehuus Hansen L, Mortensen LJ, Lanske B, Juul A & Blomberg Jensen M 2017 Possible influence of vitamin D on male reproduction. Journal of Steroid Biochemistry and Molecular Biology 173 215–222. (https://doi.org/10.1016/j.jsbmb.2016.09.023)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Boisen IM, Rehfeld A, Mos I, Poulsen NN, Nielsen JE, Schwarz P, Rejnmark L, Dissing S, Bach-Mortensen P & Juul A et al.2021 The calcium-sensing receptor is essential for calcium and bicarbonate sensitivity in human spermatozoa. Journal of Clinical Endocrinology and Metabolism 106 e1775–e1792. (https://doi.org/10.1210/clinem/dgaa937)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bouillon R, Carmeliet G, Verlinden L, Van Etten E, Verstuyf A, Luderer HF, Lieben L, Mathieu C, Demay M & Etten E 2008 Vitamin D and human health: lessons from vitamin D receptor null mice. Endocrine Reviews 29 726–776. (https://doi.org/10.1210/er.2008-0004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Brown AJ, Zhong M, Finch J, Ritter C, McCracken R, Morrissey J & Slatopolsky E 1996 Rat calcium-sensing receptor is regulated by vitamin D but not by calcium. American Journal of Physiology 270 F454–F460. (https://doi.org/10.1152/ajprenal.1996.270.3.F454)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Canaff L & Hendy GN 2002 Human calcium-sensing receptor gene. Vitamin D response elements in promoters P1 and P2 confer transcriptional responsiveness to 1,25-dihydroxyvitamin D. Journal of Biological Chemistry 277 30337–30350. (https://doi.org/10.1074/jbc.M201804200)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dimke H, Desai P, Borovac J, Lau A, Pan W & Alexander RT 2013 Activation of the Ca2+-sensing receptor increases renal claudin-14 expression and urinary Ca2+ excretion. American Journal of Physiology: Renal Physiology 304 F761–F769. (https://doi.org/10.1152/ajprenal.00263.2012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Erben RG, Soegiarto DW, Weber K, Zeitz U, Lieberherr M, Gniadecki R, Möller G, Adamski J & Balling R 2002 Deletion of deoxyribonucleic acid binding domain of the vitamin D receptor abrogates genomic and nongenomic functions of vitamin D. Molecular Endocrinology 16 1524–1537. (https://doi.org/10.1210/mend.16.7.0866)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Graca JAZ, Schepelmann M, Brennan SC, Reens J, Chang W, Yan P, Toka H, Riccardi D & Price SA 2016 Comparative expression of the extracellular calcium-sensing receptor in the mouse, rat, and human kidney. American Journal of Physiology: Renal Physiology 310 F518–F533. (https://doi.org/10.1152/ajprenal.00208.2015)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hansen LB, Rehfeld A, De NR, Nielsen JE, Iversen H, Boisen IM, Mortensen LJ, Lanske B, Almstrup K & Carlsen E et al.2016 Selection of high quality spermatozoa may be promoted by activated vitamin D in the woman. Journal of Clinical Endocrinology and Metabolism 102 950–961. (https://doi.org/10.1210/jc.2016-3008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hendy GN, Canaff L & Cole DEC 2013 The CASR gene: alternative splicing and transcriptional control, and calcium-sensing receptor (CaSR) protein: structure and ligand binding sites. Best Practice and Research: Clinical Endocrinology and Metabolism 27 285–301. (https://doi.org/10.1016/j.beem.2013.02.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ho C, Conner DA, Pollak MR, Ladd DJ, Kifor O, Warren HB, Brown EM, Seidman JG & Seidman CE 1995 A mouse model of human familial hypocalciuric hypercalcemia and neonatal severe hyperparathyroidism. Nature Genetics 11 389–394. (https://doi.org/10.1038/ng1295-389)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hoenderop JGJ, Nilius B & Bindels RJM 2005 Calcium absorption across epithelia. Physiological Reviews 85 373–422. (https://doi.org/10.1152/physrev.00003.2004)

  • Hofmann MC, Narisawa S, Hess RA & Millán JL 1992 Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Experimental Cell Research 201 417–435. (https://doi.org/10.1016/0014-4827(9290291-F)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jenkins AD, Lechene CP & Howards SS 1980 Concentrations of seven elements in the intraluminal fluids of the rat seminiferous tubules, rete testis, and epididymis. Biology of Reproduction 23 981–987. (https://doi.org/10.1095/biolreprod23.5.981)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jenkins AD, Lechene CP & Howards SS 1983 The effect of estrogen administration in vivo on the elemental composition of the intraluminal fluids of the seminiferous tubules, rete testis, and epididymis of the rat. Journal of Andrology 4 272–275. (https://doi.org/10.1002/j.1939-4640.1983.tb02366.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kato S, Mano T, Kobayashi T, Yamazaki N, Himeno Y, Yamamoto K, Itoh M, Harada N & Nagasaka A 2002 A calcium-deficient diet caused decreased bone mineral density and secondary elevation of estrogen in aged male rats – effect of menatetrenone and elcatonin. Metabolism: Clinical and Experimental 51 1230–1234. (https://doi.org/10.1053/meta.2002.35178)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kinuta K, Tanaka H, Moriwake T, Aya K, Kato S & Seino Y 2000 Vitamin D is an important factor in estrogen biosynthesis of both female and male gonads. Endocrinology 141 1317–1324. (https://doi.org/10.1210/endo.141.4.7403)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kong W, Tong L, Zhang H, Cao Y, Wang G, Zhu J, Feng Z, Xue-Ying S, Tie-Hui Z & Lin-Lin Z 2015 The calcium-sensing receptor participates in testicular damage in streptozotocin-induced diabetic rats. Asian Journal of Andrologyournal of Andrology 17 1–6. (https://doi.org/10.4103/1008-682X.160885)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kremer R, Sebag M, Champigny C, Meerovitch K, Hendy GN, White J & Goltzman D 1996 Identification and characterization of 1,25-dihydroxyvitamin D3-responsive repressor sequences in the rat parathyroid hormone-related peptide gene. Journal of Biological Chemistry 271 16310–16316. (https://doi.org/10.1074/jbc.271.27.16310)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kutuzova GD & DeLuca HF 2004 Gene expression profiles in rat intestine identify pathways for 1,25-dihydroxyvitamin D3 stimulated calcium absorption and clarify its immunomodulatory properties. Archives of Biochemistry and Biophysics 432 152–166. (https://doi.org/10.1016/j.abb.2004.09.004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Li YC, Pirro AE, Amling M, Delling G, Baron R, Bronson R & Demay MB 1997 Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. PNAS 94 9831–9835. (https://doi.org/10.1073/pnas.94.18.9831)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Li X, Zheng W & Li YC 2003 Altered gene expression profile in the kidney of vitamin D receptor knockout mice. Journal of Cellular Biochemistry 89 709–719. (https://doi.org/10.1002/jcb.10547)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lieben L, Carmeliet G & Masuyama R 2011 Calcemic actions of vitamin D: effects on the intestine, kidney and bone. Best Practice and Research: Clinical Endocrinology and Metabolism 25 561–572. (https://doi.org/10.1016/j.beem.2011.05.008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Liu DY, Lopata A, Johnston WIH & Baker HWG 1988 A human sperm-zona pellucida binding test using oocytes that failed to fertilize in vitro. Fertility and Sterility 50 782–788. (https://doi.org/10.1016/S0015-0282(1660316-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Liu C, Liu Y, Larsen K, Hou YP & Callesen H 2018 Calcium-sensing receptor (CASR) is involved in porcine in vitro fertilisation and early embryo development. Reproduction, Fertility, and Development 30 391–398. (https://doi.org/10.1071/RD16338)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Loupy A, Ramakrishnan SK, Wootla B, Chambrey R, de la Faille R, Bourgeois S, Bruneval P, Mandet C, Christensen EI & Faure H et al.2012 PTH-independent regulation of blood calcium concentration by the calcium-sensing receptor. Journal of Clinical Investigation 122 3355–3367. (https://doi.org/10.1172/JCI57407)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Macías-García B, Rocha A & González-Fernández L 2016 Extracellular calcium regulates protein tyrosine phosphorylation through calcium-sensing receptor (CaSR) in stallion sperm. Molecular Reproduction and Development 83 236–245. (https://doi.org/10.1002/mrd.22615)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Macías‐García B, García‐Marín LJ, Bragado MJ & González‐Fernández L 2019 The calcium‐sensing receptor regulates protein tyrosine phosphorylation through PDK1 in boar spermatozoa. Molecular Reproduction and Development 86 751–761. (https://doi.org/10.1002/mrd.23160)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mendoza FJ, Perez-Marin CC, Garcia-Marin L, Madueno JA, Henley C, Aguilera-Tejero E & Rodriguez M 2012 Localization, distribution, and function of the calcium-sensing receptor in sperm. Journal of Andrology 33 96–104. (https://doi.org/10.2164/jandrol.110.011254)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Panda DK, Miao D, Tremblay ML, Sirois J, Farookhi R, Hendy GN & Goltzman D 2001 Targeted ablation of the 25-hydroxyvitamin D 1alpha-hydroxylase enzyme: evidence for skeletal, reproductive, and immune dysfunction. PNAS 98 7498–7503. (https://doi.org/10.1073/pnas.131029498)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sato T, Courbebaisse M, Ide N, Fan Y, Hanai JI, Kaludjerovic J, Densmore MJ, Yuan Q, Toka HR & Pollak MR et al.2017 Parathyroid hormone controls paracellular Ca2+ transport in the thick ascending limb by regulating the tight-junction protein Claudin14. PNAS 114 E3344–E3353. (https://doi.org/10.1073/pnas.1616733114)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Singh R, Sengar GS, Singh U, Deb R, Junghare V, Hazra S, Kumar S, Tyagi S, Das AK & Raja TV et al.2018 Functional proteomic analysis of crossbred (Holstein Friesian × Sahiwal) Reproduction in Domestic Animals 53 588–608. (https://doi.org/10.1111/rda.13146)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Song Y, Kato S & Fleet JC 2003 Vitamin D receptor (VDR) knockout mice reveal VDR-independent regulation of intestinal calcium absorption and ECaC2 and calbindin D9k mRNA. Journal of Nutrition 133 374–380. (https://doi.org/10.1093/jn/133.2.374)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sun W, Chen L, Zhang W, Wang R, Goltzman D & Miao D 2015 Active vitamin D deficiency mediated by extracellular calcium and phosphorus results in male infertility in young mice. American Journal of Physiology: Endocrinology and Metabolism 308 E51–E62. (https://doi.org/10.1152/ajpendo.00076.2014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Toka HR, Al-Romaih K, Koshy JM, DiBartolo S, Kos CH, Quinn SJ, Curhan GC, Mount DB, Brown EM & Pollak MR 2012 Deficiency of the calcium-sensing receptor in the kidney causes parathyroid hormone–independent hypocalciuria. Journal of the American Society of Nephrology 23 1879–1890. (https://doi.org/10.1681/ASN.2012030323)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Usdin TB, Paciga M, Riordan T, Kuo J, Parmelee A, Petukova G, Camerini-Otero RD & Mezey E 2008 Tuberoinfundibular peptide of 39 residues is required for germ cell development. Endocrinology 149 4292–4300. (https://doi.org/10.1210/en.2008-0419)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Van Cromphaut SJ, Dewerchin M, Hoenderop JG, Stockmans I, Van Herck E, Kato S, Bindels RJ, Collen D, Carmeliet P & Bouillon R et al.2001 Duodenal calcium absorption in vitamin D receptor-knockout mice: functional and molecular aspects. PNAS 98 13324–13329. (https://doi.org/10.1073/pnas.231474698)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • 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. (https://doi.org/10.1359/jbmr.2003.18.10.1725)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Van Cromphaut SJ, Stockmans I, Torrekens S, Herck Van E, Carmeliet G & Bouillon R 2007 Duodenal calcium absorption in dexamethasone-treated mice: functional and molecular aspects. Archives of Biochemistry and Biophysics 460 300–305. (https://doi.org/10.1016/j.abb.2006.11.027)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • VanHouten J, Dann P, McGeoch G, Brown EM, Krapcho K, Neville M & Wysolmerski JJ 2004 The calcium-sensing receptor regulates mammary gland parathyroid hormone–related protein production and calcium transport. Journal of Clinical Investigation 113 598–608. (https://doi.org/10.1172/JCI18776)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wang YJ, Yan J, Yin F, Li L, Qin YG, Meng CY, Lu RF & Guo L 2017 Role of autophagy in cadmium-induced testicular injury. Human and Experimental Toxicology 36 1039–1048. (https://doi.org/10.1177/0960327116678300)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Weissgerber P, Kriebs U, Tsvilovskyy V, Olausson J, Kretz O, Stoerger C, Vennekens R, Wissenbach U, Middendorff R & Flockerzi V et al.2011 Male fertility depends on Ca2+ absorption by TRPV6 in epididymal epithelia. Science Signaling 4 ra27. (https://doi.org/10.1126/scisignal.2001791)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yao JJ, Bai S, Karnauskas AJ, Bushinsky DA & Favus MJ 2005 Regulation of renal calcium receptor gene expression by 1,25-dihydroxyvitamin D 3 in genetic hypercalciuric stone-forming rats. Journal of the American Society of Nephrology 16 1300–1308. (https://doi.org/10.1681/ASN.2004110991)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yoshizawa T, Handa Y, Uematsu Y, Takeda S, Sekine K, Yoshihara Y, Kawakami T, Arioka K, Sato H & Uchiyama Y et al.1997 Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nature Genetics 16 391–396. (https://doi.org/10.1038/ng0897-391)

    • PubMed
    • Search Google Scholar
    • Export Citation