Active vitamin d deficiency mediated by extracellular calcium and phosphorus results in male infertility in young mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 308, Issue 1, 2015, Pages E51-E60

  Sun, Weiwei ^a   Chen, Lulu ^a   Zhang, Wei ^a   Wang, Rong ^a   Goltzman, David ^b   Miao, Dengshun ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Male infertility; Spermatogenesis; Vitamin D

Indexed keywords

25 HYDROXYVITAMIN D; 25 HYDROXYVITAMIN D 1 ALPHA HYDROXYLASE; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; CALCIUM; CASPASE 3; CYCLIN DEPENDENT KINASE 2; CYCLIN E; ESTRADIOL; FOLLITROPIN; LUTEINIZING HORMONE; PHOSPHORUS; PROTEIN BAX; PROTEIN BCL XL; PROTEIN P21; PROTEIN P53; TESTOSTERONE; TESTOSTERONE 17BETA DEHYDROGENASE; UNCLASSIFIED DRUG; CALCIDIOL 1 MONOOXYGENASE; CALCITRIOL; CALCIUM INTAKE; MINERAL; PHOSPHATE INTAKE;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CALCIUM BLOOD LEVEL; CALCIUM CELL LEVEL; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR CALCIUM; FEMALE; HISTOPATHOLOGY; HORMONE BLOOD LEVEL; HYPERGONADOTROPIC HYPOGONADISM; HYPOCALCEMIA; HYPOPHOSPHATEMIA; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MALE; MALE INFERTILITY; MOUSE; NONHUMAN; PHENOTYPE; PHOSPHATE BLOOD LEVEL; PROTEIN EXPRESSION; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; UPREGULATION; VITAMIN D DEFICIENCY; ANIMAL; BLOOD; CALCIUM INTAKE; COMPLICATION; DIET; FAMILIAL HYPOPHOSPHATEMIC RICKETS; GENETICS; INFERTILITY, MALE; KNOCKOUT MOUSE; METABOLISM; PHOSPHATE INTAKE;

25-HYDROXYVITAMIN D3 1-ALPHA-HYDROXYLASE; ANIMALS; CALCITRIOL; CALCIUM; CALCIUM, DIETARY; DIET; FAMILIAL HYPOPHOSPHATEMIC RICKETS; FEMALE; INFERTILITY, MALE; MALE; MICE; MICE, KNOCKOUT; MINERALS; PHOSPHORUS; PHOSPHORUS, DIETARY; VITAMIN D DEFICIENCY;

EID: 84919442065     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00076.2014     Document Type: Article

References (40)

1. Almon E, Goldfinger N, Kapon A, Schwartz D, Levine AJ, Rotter V. Testicular tissue-specific expression of the p53 suppressor gene. Dev Biol 156: 107–116, 1993.
2. Aquila S, Guido C, Middea E, Perrotta I, Bruno R, Pellegrino M, Andò S. Human male gamete endocrinology: 1alpha, 25-dihydroxyvitamin D3 (1,25(OH)2D3) regulates different aspects of human sperm biology and metabolism. Reprod Biol Endocrinol 7: 140, 2009.
3. Arnoult C, Cardullo RA, Lemos JR, Florman HM. Activation of mouse sperm T-type Ca2_ channels by adhesion to the egg zona pellucida. Proc Natl Acad Sci USA 93: 13004–13009, 1996.
4. Bao GC, Wang JG, Jong A. Increased p21 expression and complex formation with cyclin E/CDK2 in retinoid-induced pre-B lymphoma cell apoptosis. FEBS Lett 580: 3687–3693, 2006.
5. Blomberg Jensen M, Nielsen JE, Jorgensen A, Rajpert-De Meyts E, Kristensen DM, Jorgensen N, Skakkebaek NE, Juul A, Leffers H. Vitamin D receptor and vitamin D metabolizing enzymes are expressed in the human male reproductive tract. Hum Reprod 25: 1303–1311, 2010.
6. Bouillon R, Carmeliet G, Verlinden L, van Etten E, Verstuyf A, Luderer HF, Lieben L, Mathieu C, Demay M. Vitamin D and human health: lessons from vitamin D receptor null mice. Endocr Rev 29: 726–776, 2008.
7. Coqueret O. New roles for p21 and p27 cell-cycle inhibitors: A function for each cell compartment? Trends Cell Biol 13: 65–70, 2003.
8. Costello S, Michelangeli F, Nash K, Lefievre L, Morris J, Machado-Oliveira G, Barratt C, Kirkman-Brown J, Publicover S. Ca2_-stores in sperm: their identities and functions. Reproduction 138: 425–437, 2009.
9. Dardenne O, Prud’homme J, Arabian A, Glorieux FH, St-Arnaud R. Targeted inactivation of the 25-hydroxyvitamin D(3)-1(alpha)-hydroxylase gene (CYP27B1) creates an animal model of pseudovitamin D-deficiency rickets. Endocrinology 142: 3135–3141, 2001.
10. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 75: 817–825, 1993.
11. Espinosa F, López-González I, Serrano CJ, Gasque G, delaVega-Beltrán JL, Treviño CL, Darszon A. Anion channel blockers differentially affect T-type Ca(2_) currents of mouse spermatogenic cells, alpha1E currents expressed in Xenopus oocytes and the sperm acrosome reaction. Dev Genet 25: 103–114, 1999.
12. Fujisawa M, Shirakawa T, Fujioka H, Gotoh A, Okada H, Arakawa S, Kamidono S. Adenovirus-mediated p53 gene transfer to rat testis impairs spermatogenesis. Arch Androl 46: 223–231, 2001.
13. Furuchi T, Masuko K, Nishimune Y, Obinata M, Matsui Y. Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia. Development 122: 1703–1709, 1996.
14. Goodwin LO, Leeds NB, Hurley I, Mandel FS, Pergolizzi RG, Benoff S. Isolation and characterization of the primary structure of testis-specific L-type calcium channel: implications for contraception. Mol Hum Reprod 3: 255–268, 1997.
15. Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805–816, 1993.
16. Herrick SB, Schweissinger DL, Kim S., Bayan KR, Mann S, Cardullo RA. The acrosomal vesicle of mouse sperm is a calcium store. J Cell Physiol 202: 663–671, 2005.
17. Hirai T, Tsujimura A, Ueda T, Fujita K, Matsuoka Y, Takao T, Miyagawa Y, Koike N, Okuyama A. Effect of 1,25-dihydroxyvitamin d on testicular morphology and gene expression in experimental cryptorchid mouse: testis specific cDNA microarray analysis and potential implication in male infertility. J Urol 181: 1487–1492, 2009.
18. Johnson LE, DeLuca HF. Vitamin D receptor null mutant mice fed high levels of calcium are fertile. J Nutr 131: 1787–1791, 2001.
19. Kinuta K, Tanaka H, Moriwake T, Aya K, Kato S, Seino Y. Vitamin D is an important factor in estrogen biosynthesis of both female and male gonads. Endocrinology 141: 1317–1324, 2000.
20. Kwiecinski GG, Petrie GI, DeLuca HF. Vitamin D is necessary for reproductive functions of the male rat. J Nutr 119: 741–744, 1989.
21. Lee PS, Buchan AM, Hsueh AJ, Yuen BH, Leung PC. Intracellular calcium mobilization in response to the activation of human wild-type and chimeric gonadotropin receptors. Endocrinology 143: 1732–1740, 2002.
22. Li YC, Pirro AE, Amling M, Delling G, Baron R, Bronson R, Demay MB. Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. Proc Natl Acad Sci USA 94: 9831–9835, 1997.
23. Lievano A, Santi CM, Serrano CJ, Trevino CL, Bellve AR, Hernandez-Cruz A, Darszon A. T-type Ca2_ channels and alpha1E expression in spermatogenic cells, and their possible relevance to the sperm acrosome reaction. FEBS Lett 388: 150–154, 1996.
24. Malloy PJ, Wang J, Srivastava T, Feldman D. Hereditary 1,25-dihydroxyvitamin D-resistant rickets with alopecia resulting from a novel missense mutation in the DNA-binding domain of the vitamin D receptor. Mol Genet Metab 99: 72–79, 2010.
25. Miao D, He B, Karaplis AC, Goltzman D. Parathyroid hormone is essential for normal fetal bone formation. J Clin Invest 109: 1173–1182, 2002.
26. Miller WL, Auchus RJ. The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr Rev 32: 81–151, 2011.
27. Panda DK, Miao D, Bolivar I, Li J, Huo R, Hendy GN, Goltzman D. Inactivation of the 25-hydroxyvitamin D 1alpha-hydroxylase and vitamin D receptor demonstrates independent and interdependent effects of calcium and vitamin D on skeletal and mineral homeostasis. J Biol Chem 279: 16754–16766, 2004.
28. Panda DK, Miao D, Tremblay ML, Sirois J, Farookhi R, Hendy GN, Goltzman D. Targeted ablation of the 25-hydroxyvitamin D 1alpha -hydroxylase enzyme: evidence for skeletal, reproductive, and immune dysfunction. Proc Natl Acad Sci USA 98: 7498–7503, 2001.
29. Pike JW, Zella LA, Meyer MB, Fretz JA, Kim S. Molecular actions of 1,25-dihydroxyvitamin D3 on genes involved in calcium homeostasis. J Bone Miner Res 22, Suppl 2: V16–V19, 2007.
30. Russell LD, Chiarini-Garcia H, Korsmeyer SJ, Knudson CM. Baxdependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol Reprod 66: 950–958, 2002.
31. Schwartz D, Goldfinger N, Rotter V. Expression of p53 protein in spermatogenesis is confined to the tetraploid pachytene primary spermatocytes. Oncogene 8: 1487–1494, 1993.
32. Shen C, Kuang Y, Liu J, Feng J, Chen X, Wu W, Chi J, Tang L, Wang Y, Fei J, Wang Z. Prss37 is required for male fertility in the mouse. Biol Reprod 88: 123, 2013.
33. Sood S, Reghunandanan R, Reghunandanan V, Marya RK, Singh PI. Effect of vitamin D repletion on testicular function in vitamin D-deficient rats. Ann Nutr Metab 39: 95–98, 1995.
34. Sun W, Xie H, Ji J, Zhou X, Goltzman D, Miao D. Defective female reproductive function in 1,25(OH)2D-deficient mice results from indirect effect mediated by extracellular calcium and/or phosphorus. Am J Physiol Endocrinol Metab 299: E928–E935, 2010.
35. Trussell JC. Male reproductive endocrinology: When to replace gonadotropins. Semin Reprod Med 31: 237–244, 2013.
36. Uhland AM, Kwiecinski GG, DeLuca HF. Normalization of serum calcium restores fertility in vitamin D-deficient male rats. J Nutr 122: 1338–1344, 1992.
37. Xue Y, Karaplis AC, Hendy GN, Goltzman D, Miao D. Genetic models show that parathyroid hormone and 1,25-dihydroxyvitamin D3 play distinct and synergistic roles in postnatal mineral ion homeostasis and skeletal development. Hum Mol Genet 14: 1515–1528, 2005.
38. Yin Y, DeWolf WC, Morgentaler A. Experimental cryptorchidism induces testicular germ cell apoptosis by p53-dependent and -independent pathways in mice. Biol Reprod 58: 492–496, 1998.
39. Yoshida M, Kawano N, Yoshida K. Control of sperm motility and fertility: diverse factors and common mechanisms. Cell Mol Life Sci 65: 3446–3457, 2008.
40. Yoshizawa T, Handa Y, Uematsu Y, Takeda S, Sekine K, Yoshihara Y, Kawakami T, Arioka K, Sato H, Uchiyama Y, Masushige S, Fukamizu A, Matsumoto T, Kato S. Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nat Genet 16: 391–396, 1997.