DOI QR코드

DOI QR Code

Calcium Homeostasis and Regulation of Calbindin-D9k by Glucocorticoids and Vitamin D as Bioactive Molecules

  • Choi, Kyung-Chul (Laboratory of Veterinary Biochemistry and Immunology, College of Veterinary Medicine, Chungbuk National University) ;
  • Jeung, Eui-Bae (Laboratory of Veterinary Biochemistry and Molecular Biology, College of Veterinary Medicine, Chungbuk National University)
  • Published : 2009.04.30

Abstract

Calbindin-$D_{9k}$ (CaBP-9k), a cytosolic calcium-binding protein, is expressed in a variety of tissues, i.e., the duodenum, uterus, placenta, kidney and pituitary gland. Duodenal CaBP-9k is involved in intestinal calcium absorption, and is regulated at transcriptional and post-transcriptional levels by 1,25-dihydroxyvitamin D3, the hormonal form of vitamin D, and glucocorticoids (GCs). Uterine CaBP-9k has been implicated in the regulation of myometrial action(s) through modulation of intracellular calcium, and steroid hormones appear to be the main regulators in its uterine and placental regulation. Because phenotypes of CaBP-9k-null mice appear to be normal, other calcium-transporter genes may compensate for its gene deletion and physiological function in knockout mice. Previous studies indicate that CaBP-9k may be controlled in a tissue-specific fashion. In this review, we summarize the current information on calcium homeostasis related to CaBP-9k gene regulation by GCs, vitamin D and its receptors, and its molecular regulatory mechanism. In addition, we present related data from our current research.

Keywords

References

  1. Akhter, S., Kutuzova, G. D., Christakos, S. and DeLuca, H. F. (2007). Calbindin $D_{9k}$ is not required for 1,25-dihydroxyvitamin D3-mediated Ca2+ absorption in small intestine. Arch. Biochem. Biophys. 460, 227-232 https://doi.org/10.1016/j.abb.2006.12.005
  2. An, B. S., Choi, K. C., Hong, E. J., Jung, Y. W., Manabe, N. and Jeung, E. B. (2004). Differential transcriptional and translational regulations of calbindin-$D_{9k}$ by steroid hormones and their receptors in the uterus of immature mice. J. Reprod Dev. 50, 445-453 https://doi.org/10.1262/jrd.50.445
  3. An, B. S., Choi, K. C., Kang, S. K., Hwang, W. S. and Jeung, E. B. (2003). Novel Calbindin-D(9k) protein as a useful biomarker for environmental estrogenic compounds in the uterus of immature rats. Reprod Toxicol. 17, 311-319 https://doi.org/10.1016/S0890-6238(03)00003-0
  4. An, B. S., Choi, K. C., Kang, S. K., Lee, G. S., Hong, E. J., Hwang, W. S. and Jeung, E. B. (2003). Mouse calbindin-D (9k) gene expression in the uterus during late pregnancy and lactation. Mol. Cell Endocrinol. 205, 79-88 https://doi.org/10.1016/S0303-7207(03)00203-X
  5. An, B. S., Choi, K. C., Lee, G. S., Leung, P. C. and Jeung, E. B. (2004). Complex regulation of Calbindin-D(9k) in the mouse placenta and extra-embryonic membrane during mid-and late pregnancy. Mol. Cell Endocrinol. 214, 39-52 https://doi.org/10.1016/j.mce.2003.11.029
  6. Bacskai, B. J. and Friedman, P. A. (1990). Activation of latent Ca2+ channels in renal epithelial cells by parathyroid hormone. Nature 347, 388-391 https://doi.org/10.1038/347388a0
  7. Barley, N. F., Prathalingam, S. R., Zhi, P., Legon, S., Howard, A. and Walters, J. R. (1999). Factors involved in the duodenal expression of the human calbindin-D9k gene. Biochem. J. 341(Pt 3), 491-500 https://doi.org/10.1042/0264-6021:3410491
  8. Beaulieu, J. F. and Calvert, R. (1985). Influences of dexamethasone on the maturation of fetal mouse intestinal mucosa in organ culture. Comp. Biochem. Physiol. A. 82, 91-95 https://doi.org/10.1016/0300-9629(85)90709-1
  9. Benn, B. S., Ajibade, D., Porta, A., Dhawan, P., Hediger, M., Peng, J. B., Jiang, Y., Oh, G. T., Jeung, E. B., Lieben, L., Bouillon, R., Carmeliet, G. and Christakos, S. (2008). Active intestinal calcium transport in the absence of transient receptor potential vanilloid type 6 and calbindin-D9k. Endocrinology 149, 3196-3205 https://doi.org/10.1210/en.2007-1655
  10. Bindels, R. J. (1993). Calcium handling by the mammalian kidney. J. Exp. Biol. 184, 89-104
  11. Brown, A. J., Krits, I. and Armbrecht, H. J. (2005). Effect of age, vitamin D, and calcium on the regulation of rat intestinal epithelial calcium channels. Arch. Biochem. Biophys. 437, 51-58 https://doi.org/10.1016/j.abb.2005.02.007
  12. Chailley-Heu, B., Rambaud, C., Barlier-Mur, A. M., Galateau-Salle, F., Perret, C., Capron, F. and Lacaze-Masmonteil, T. (2001). A model of pulmonary adenocarcinoma in transgenic mice expressing the simian virus 40 T antigen driven by the rat Calbindin-D9K (CaBP9K) promoter. J. Pathol. 195, 482-489 https://doi.org/10.1002/path.960
  13. Choi, K. C. and Jeung, E. B. (2008). Molecular mechanism of regulation of the calcium-binding protein calbindin-D9k, and its physiological role(s) in mammals: a review of current research. J. Cell Mol. Med. 12, 409-420 https://doi.org/10.1111/j.1582-4934.2007.00209.x
  14. Choi, K. C., Leung, P. C. and Jeung, E. B. (2005). Biology and physiology of Calbindin-D9k in female reproductive tissues: involvement of steroids and endocrine disruptors. Reprod Biol. Endocrinol. 3, 66 https://doi.org/10.1186/1477-7827-3-66
  15. Cole, M. A., Kim, P. J., Kalman, B. A. and Spencer, R. L. (2000). Dexamethasone suppression of corticosteroid secretion: evaluation of the site of action by receptor measures and functional studies. Psychoneuroendocrinology 25, 151-167 https://doi.org/10.1016/S0306-4530(99)00045-1
  16. Cosman, F., Nieves, J., Herbert, J., Shen, V. and Lindsay, R. (1994). High-dose glucocorticoids in multiple sclerosis patients exert direct effects on the kidney and skeleton. J. Bone Miner. Res. 9, 1097-1105 https://doi.org/10.1002/jbmr.5650090718
  17. Darwish, H., Krisinger, J., Furlow, J. D., Smith, C., Murdoch, F. E. and DeLuca, H. F. (1991). An estrogen-responsive element mediates the transcriptional regulation of calbindin D-9K gene in rat uterus. J. Biol. Chem. 266, 551-558
  18. Darwish, H. M. and DeLuca, H. F. (1992). Identification of a 1,25-dihydroxyvitamin D3-response element in the 5'-flanking region of the rat calbindin D-9k gene. Proc. Natl. Acad. Sci. USA. 89, 603-607 https://doi.org/10.1073/pnas.89.2.603
  19. Delorme, A. C., Danan, J. L., Acker, M. G., Ripoche, M. A. and Mathieu, H. (1983). In rat uterus 17 beta-estradiol stimulates a calcium-binding protein similar to the duodenal vitamin D-dependent calcium-binding protein. Endocrinology 113, 1340-1347 https://doi.org/10.1210/endo-113-4-1340
  20. Farman, N., Oblin, M. E., Lombes, M., Delahaye, F., Westphal, H. M., Bonvalet, J. P. and Gasc, J. M. (1991). Immunolocalization of gluco- and mineralocorticoid receptors in rabbit kidney. Am. J. Physiol. 260, C226-233 https://doi.org/10.1152/ajpcell.1991.260.2.C226
  21. Frick, K. K. and Bushinsky, D. A. (2003). Molecular mechanisms of primary hypercalciuria. J. Am. Soc. Nephrol. 14, 1082-1095 https://doi.org/10.1097/01.ASN.0000062960.26868.17
  22. Fukugawa, M. and Kurokawa, K. (2002). Calcium homeostasis and imbalance. Nephron. 92(Suppl 1), 41-45 https://doi.org/10.1159/000065376
  23. Gkika, D., Hsu, Y. J., van der Kemp, A. W., Christakos, S., Bindels, R. J. and Hoenderop, J. G. (2006). Critical role of the epithelial Ca2+ channel TRPV5 in active Ca2+ reabsorption as revealed by TRPV5/calbindin-D28K knockout mice. J. Am. Soc. Nephrol. 17, 3020-3027 https://doi.org/10.1681/ASN.2006060676
  24. Hoenderop, J. G., Dardenne, O., Van Abel, M., Van Der Kemp, A. W., Van Os, C. H., St-Arnaud, R. and Bindels, R. J. (2002). Modulation of renal Ca2+ transport protein genes by dietary Ca2+ and 1,25-dihydroxyvitamin D3 in 25-hydroxyvitamin D3-1alpha-hydroxylase knockout mice. Faseb J. 16, 1398-1406 https://doi.org/10.1096/fj.02-0225com
  25. Hoenderop, J. G., Nilius, B. and Bindels, R. J. (2002). Molecular mechanism of active Ca2+ reabsorption in the distal nephron. Annu. Rev. Physiol. 64, 529-549 https://doi.org/10.1146/annurev.physiol.64.081501.155921
  26. Hong, E. J., Choi, K. C. and Jeung, E. B. (2003). Maternal-fetal transfer of endocrine disruptors in the induction of Calbindin-D9k mRNA and protein during pregnancy in rat model. Mol. Cell Endocrinol. 212, 63-72 https://doi.org/10.1016/j.mce.2003.08.011
  27. Hong, E. J., Choi, K. C., Jung, Y. W., Leung, P. C. and Jeung, E. B. (2004). Transfer of maternally injected endocrine disruptors through breast milk during lactation induces neonatal Calbindin-D9k in the rat model. Reprod. Toxicol. 18, 661-668 https://doi.org/10.1016/j.reprotox.2004.03.005
  28. Hurwitz, S. (1996). Homeostatic control of plasma calcium concentration. Crit. Rev. Biochem. Mol. Biol. 31, 41-100 https://doi.org/10.3109/10409239609110575
  29. Huybers, S., Naber, T. H., Bindels, R. J. and Hoenderop, J. G. (2007). Prednisolone-induced Ca2+ malabsorption is caused by diminished expression of the epithelial Ca2+ channel TRPV6. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G92-97 https://doi.org/10.1152/ajpgi.00317.2006
  30. Juppner, H., Abou-Samra, A. B., Freeman, M., Kong, X. F., Schipani, E., Richards, J., Kolakowski, L. F., Jr., Hock, J., Potts, J. T. Jr., Kronenberg, H. M., Harald, J., Abdul-badi, A., Mason, F., Xiang, F. K., Ernestina, S., Jennifer, R., Lee, F. K. Jr., Janet, H., John, T., PoTrs, Jr., Henry, M. K., Gino, V. S. (1991). A G protein-linked receptor for parathyroid hormone and parathyroid hormone-related peptide. Science 254, 1024- 1026 https://doi.org/10.1126/science.1658941
  31. Kim, H. J., Lee, G. S., Ji, Y. K., Choi, K. C. and Jeung, E. B. (2006). Differential expression of uterine calcium transporter 1 and plasma membrane Ca2+ ATPase 1b during rat estrous cycle. Am. J. Physiol. Endocrinol. Metab. 291, E234-241 https://doi.org/10.1152/ajpendo.00434.2005
  32. Kim, M. H., Lee, G. S., Jung, E. M., Choi, K. C., Oh, G. T. and Jeung, E. B. (2009). Dexamethasone differentially regulates renal and duodenal calcium-processing genes in calbindin-D9k and -D28k knockout mice. Exp. Physiol. 94, 138-151 https://doi.org/10.1113/expphysiol.2008.044339
  33. Kutuzova, G. D., Akhter, S., Christakos, S., Vanhooke, J., Kimmel-Jehan, C. and Deluca, H. F. (2006). Calbindin D(9k) knockout mice are indistinguishable from wild-type mice in phenotype and serum calcium level. Proc. Natl. Acad. Sci. USA. 103, 12377-12381 https://doi.org/10.1073/pnas.0605252103
  34. Kutuzova, G. D., Sundersingh, F., Vaughan, J., Tadi, B. P., Ansay, S. E., Christakos, S. and Deluca, H. F. (2008). TRPV6 is not required for 1alpha,25-dihydroxyvitamin D3-induced intestinal calcium absorption in vivo. Proc. Natl. Acad. Sci. USA. 105, 19655-19659 https://doi.org/10.1073/pnas.0810761105
  35. Kwiecinksi, G. G., Petrie, G. I. and DeLuca, H. F. (1989). 1,25-Dihydroxyvitamin D3 restores fertility of vitamin D-deficient female rats. Am. J. Physiol. 256, E483-487
  36. L'Horset, F., Blin, C., Colnot, S., Lambert, M., Thomasset, M. and Perret, C. (1994). Calbindin-D9k gene expression in the uterus: study of the two messenger ribonucleic acid species and analysis of an imperfect estrogen-responsive element. Endocrinology 134, 11-18 https://doi.org/10.1210/en.134.1.11
  37. Lambers, T. T., Mahieu, F., Oancea, E., Hoofd, L., de Lange, F., Mensenkamp, A. R., Voets, T., Nilius, B., Clapham, D. E., Hoenderop, J. G. and Bindels, R. J. (2006). Calbindin-D28K dynamically controls TRPV5-mediated Ca2+ transport. Embo. J. 25, 2978-2988 https://doi.org/10.1038/sj.emboj.7601186
  38. Lee, G. S., Choi, K. C. and Jeung, E. B. (2006). Glucocorticoids differentially regulate expression of duodenal and renal calbindin-D9k through glucocorticoid receptor-mediated pathway in mouse model. Am. J. Physiol. Endocrinol. Metab. 290, E299-307 https://doi.org/10.1152/ajpendo.00232.2005
  39. Lee, G. S., Choi, K. C., Kim, H. J. and Jeung, E. B. (2004). Effect of genistein as a selective estrogen receptor beta agonist on the expression of Calbindin-D9k in the uterus of immature rats. Toxicol. Sci. 82, 451-457 https://doi.org/10.1093/toxsci/kfh296
  40. Lee, G. S., Kim, H. J., Jung, Y. W., Choi, K. C. and Jeung, E. B. (2005). Estrogen receptor alpha pathway is involved in the regulation of Calbindin-D9k in the uterus of immature rats. Toxicol. Sci. 84, 270-277 https://doi.org/10.1093/toxsci/kfi072
  41. Lee, G. S., Lee, K. Y., Choi, K. C., Ryu, Y. H., Paik, S. G., Oh, G. T. and Jeung, E. B. (2007). Phenotype of a calbindin-d9k gene knockout is compensated for by the induction of other calcium transporter genes in a mouse model. J. Bone Miner. Res. 22, 1968-1978 https://doi.org/10.1359/jbmr.070801
  42. Lee, K. Y., Oh, G. T., Kang, J. H., Shin, S. M., Heo, B. E., Yun, Y. W., Paik, S. G., Krisinger, J., Leung, P. C. and Jeung, E. B. (2003). Transcriptional regulation of the mouse calbindin-D9k gene by the ovarian sex hormone. Mol. Cells. 16, 48-53
  43. Li, H. and Christakos, S. (1991). Differential regulation by 1,25-dihydroxyvitamin D3 of calbindin-D9k and calbindin-D28k gene expression in mouse kidney. Endocrinology 128, 2844-2852 https://doi.org/10.1210/endo-128-6-2844
  44. Li, Y. C., Bolt, M. J., Cao, L. P. and Sitrin, M. D. (2001). Effects of vitamin D receptor inactivation on the expression of calbindins and calcium metabolism. Am. J. Physiol. Endocrinol. Metab. 281, E558-564 https://doi.org/10.1152/ajpendo.2001.281.3.E558
  45. Lukert, B. P. and Raisz, L. G. (1990). Glucocorticoid-induced osteoporosis: pathogenesis and management. Ann. Intern. Med. 112, 352-364 https://doi.org/10.7326/0003-4819-112-5-352
  46. Luu, K. C., Nie, G. Y. and Salamonsen, L. A. (2004). Endometrial calbindins are critical for embryo implantation: evidence from in vivo use of morpholino antisense oligonucleotides. Proc. Natl. Acad. Sci. USA. 101, 8028-8033 https://doi.org/10.1073/pnas.0401069101
  47. McCuaig, K. A., Lee, H. S., Clarke, J. C., Assar, H., Horsford, J. and White, J. H. (1995). Parathyroid hormone/parathyroid hormone related peptide receptor gene transcripts are expressed from tissue-specific and ubiquitous promoters. Nucleic Acids Res. 23, 1948-1955 https://doi.org/10.1093/nar/23.11.1948
  48. McGowan, J. E., Sysyn, G., Petersson, K. H., Sadowska, G. B., Mishra, O. P., Delivoria-Papadopoulos, M. and Stonestreet, B. S. (2000). Effect of dexamethasone treatment on maturational changes in the NMDA receptor in sheep brain. J. Neurosci. 20, 7424-7429
  49. McLaughlin, F., Mackintosh, J., Hayes, B. P., McLaren, A., Uings, I. J., Salmon, P., Humphreys, J., Meldrum, E. and Farrow, S. N. (2002). Glucocorticoid-induced osteopenia in the mouse as assessed by histomorphometry, microcomputed tomography, and biochemical markers. Bone 30, 924-930 https://doi.org/10.1016/S8756-3282(02)00737-8
  50. Merot, J., Bidet, M., Gachot, B., Le Maout, S., Koechlin, N., Tauc, M. and Poujeol, P. (1989). Electrical properties of rabbit early distal convoluted tubule in primary culture. Am. J. Physiol. 257, F288-299
  51. Nagpal, S., Na, S. and Rathnachalam, R. (2005). Noncalcemic actions of vitamin D receptor ligands. Endocr Rev. 26, 662-6 https://doi.org/10.1210/er.2004-0002
  52. Nie, G., Findlay, J. K. and Salamonsen, L. A. (2005). Identification of novel endometrial targets for contraception. Contraception 71, 272-281 https://doi.org/10.1016/j.contraception.2004.12.019
  53. Nie, G. Y., Li, Y., Wang, J., Minoura, H., Findlay, J. K. and Sala monsen, L. A. (2000). Complex regulation of calciumbinding protein D9k (calbindin-D(9k)) in the mouse uterus during early pregnancy and at the site of embryo implantation. Biol. Reprod. 62, 27-36 https://doi.org/10.1095/biolreprod62.1.27
  54. Nijenhuis, T., Hoenderop, J. G. and Bindels, R. J. (2004). Downregulation of Ca(2+) and Mg(2+) transport proteins in the kidney explains tacrolimus (FK506)-induced hypercalciuria and hypomagnesemia. J. Am. Soc. Nephrol. 15, 549-557 https://doi.org/10.1097/01.ASN.0000113318.56023.B6
  55. Panda, D. K., Miao, D., Bolivar, I., Li, J., Huo, R., Hendy, G. N. and Goltzman, D. (2004). 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 https://doi.org/10.1074/jbc.M310271200
  56. Patschan, D., Loddenkemper, K. and Buttgereit, F. (2001). Molecular mechanisms of glucocorticoid-induced osteoporosis. Bone 29, 498-505 https://doi.org/10.1016/S8756-3282(01)00610-X
  57. Pausova, Z., Bourdon, J., Clayton, D., Mattei, M. G., Seldin, M. F., Janicic, N., Riviere, M., Szpirer, J., Levan, G., Szpirer, C., Zdenka, P., Johanne, B., Dale, C., Marie-Genevieve, M., Michael, F. S., Natasa, J., Michele, R., Josiane, S., Goran, L., Claude, S., David, G. and Geoffrey, N. H. (1994). Cloning of a parathyroid hormone/parathyroid hormone-related peptide receptor (PTHR) cDNA from a rat osteosarcoma (UMR 106) cell line: chromosomal assignment of the gene in the human, mouse, and rat genomes. Genomics 20, 20-26 https://doi.org/10.1006/geno.1994.1122
  58. Peng, J. B., Brown, E. M. and Hediger, M. A. (2003). Epithelial Ca2+ entry channels: transcellular Ca2+ transport and beyond. J. Physiol. 551, 729-740 https://doi.org/10.1113/jphysiol.2003.043349
  59. Peng, J. B., Chen, X. Z., Berger, U. V., Vassilev, P. M., Brown, E. M. and Hediger, M. A. (2000). A rat kidney-specific calcium transporter in the distal nephron. J. Biol. Chem. 275, 28186-28194
  60. Roche, C., Bellaton, C., Pansu, D., Miller, A. 3rd and Bronner, F. (1986). Localization of vitamin D-dependent active Ca2+ transport in rat duodenum and relation to CaBP. Am. J. Physiol. 251, G314-320
  61. Rouleau, M. F., Mitchell, J. and Goltzman, D. (1988). In vivo distribution of parathyroid hormone receptors in bone: evidence that a predominant osseous target cell is not the mature osteoblast. Endocrinology 123, 187-191 https://doi.org/10.1210/endo-123-1-187
  62. Schacke, H., Docke, W. D. and Asadullah, K. (2002). Mechanisms involved in the side effects of glucocorticoids. Pharmacol. Ther. 96, 23-43 https://doi.org/10.1016/S0163-7258(02)00297-8
  63. Sheppard, K. E., Li, K. X. and Autelitano, D. J. (1999). Corticosteroid receptors and 11beta-hydroxysteroid dehydrogenase isoforms in rat intestinal epithelia. Am. J. Physiol. 277, G541-547
  64. Shultz, T. D., Bollman, S. and Kumar, R. (1982). Decreased intestinal calcium absorption in vivo and normal brush border membrane vesicle calcium uptake in cortisol-treated chickens: evidence for dissociation of calcium absorption from brush border vesicle uptake. Proc. Natl. Acad. Sci. USA. 79, 3542-3546 https://doi.org/10.1073/pnas.79.11.3542
  65. Silvestrini, G., Ballanti, P., Patacchioli, F. R., Mocetti, P., Di Grezia, R., Wedard, B. M., Angelucci, L. and Bonucci, E. (2000). Evaluation of apoptosis and the glucocorticoid receptor in the cartilage growth plate and metaphyseal bone cells of rats after high-dose treatment with corticosterone Bone 26, 33-42 https://doi.org/10.1016/S8756-3282(99)00245-8
  66. Song, Y., Peng, X., Porta, A., Takanaga, H., Peng, J. B., Hediger, M. A., Fleet, J. C. and Christakos, S. (2003). Calcium transporter 1 and epithelial calcium channel messenger ribonucleic acid are differentially regulated by 1,25 dihydroxyvitamin D3 in the intestine and kidney of mice. Endocrinology 144, 3885-3894 https://doi.org/10.1210/en.2003-0314
  67. Tanabe, M., Matsumoto, T., Shibuya, K., Tateda, K., Miyazaki, S., Nakane, A., Iwakura, Y. and Yamaguchi, K. (2005). Compensatory response of IL-1 gene knockout mice after pulmonary infection with Klebsiella pneumoniae. J. Med. Microbiol. 54, 7-13 https://doi.org/10.1099/jmm.0.45736-0
  68. Uhland, A. M., Kwiecinski, G. G. and DeLuca, H. F. (1992). Normalization of serum calcium restores fertility in vitamin D-deficient male rats. J. Nutr. 122, 1338-1344 https://doi.org/10.1093/jn/122.6.1338
  69. van Abel, M., Hoenderop, J. G. and Bindels, R. J. (2005). The epithelial calcium channels TRPV5 and TRPV6: regulation and implications for disease. Naunyn Schmiedebergs Arch. Pharmacol. 371, 295-306 https://doi.org/10.1007/s00210-005-1021-2
  70. Van Cromphaut, S. J., Dewerchin, M., Hoenderop, J. G., Stockmans, I., Van Herck, E., Kato, S., Bindels, R. J., Collen, D., Carmeliet, P., Bouillon, R. and Carmeliet, G. (2001). Duodenal calcium absorption in vitamin D receptor-knockout mice: functional and molecular aspects. Proc. Natl. Acad. Sci. USA. 98, 13324-13329 https://doi.org/10.1073/pnas.231474698
  71. Van Cromphaut, S. J., Rummens, K., Stockmans, I., Van Herck, E., Dijcks, F. A., Ederveen, A. G., Carmeliet, P., Verhaeghe, J., Bouillon, R. and Carmeliet, G. (2003). Intestinal calcium transporter genes are upregulated by estrogens and the reproductive cycle through vitamin D receptor-independent mechanisms. J. Bone Miner. Res. 18, 1725-1736 https://doi.org/10.1359/jbmr.2003.18.10.1725
  72. Walters, J. R., Howard, A., Lowery, L. J., Mawer, E. B. and Legon, S. (1999). Expression of genes involved in calcium absorption in human duodenum. Eur. J. Clin. Invest. 29, 214-219 https://doi.org/10.1046/j.1365-2362.1999.00439.x
  73. Wasserman, R. H. and Fullmer, C. S. (1989). On the molecular mechanism of intestinal calcium transport. Adv. Exp. Med. Biol. 249, 45-65 https://doi.org/10.1007/978-1-4684-9111-1_5
  74. Wasserman, R. H. and Fullmer, C. S. (1995). Vitamin D and intestinal calcium transport: facts, speculations and hypotheses. J. Nutr. 125, 1971S-1979S https://doi.org/10.1093/jn/125.suppl_7.1971S
  75. Wertheimer, E., Spravchikov, N., Trebicz, M., Gartsbein, M., Accili, D., Avinoah, I., Nofeh-Moses, S., Sizyakov, G. and Tennenbaum, T. (2001). The regulation of skin proliferation and differentiation in the IR null mouse: implications for skin complications of diabetes. Endocrinology 142, 1234-1241 https://doi.org/10.1210/en.142.3.1234
  76. Xu, J., Chang, V., Joseph, S. B., Trujillo, C., Bassilian, S., Saad, M. F., Lee, W. N. and Kurland, I. J. (2004). Peroxisomal proliferator-activated receptor alpha deficiency diminishes insulin-responsiveness of gluconeogenic/glycolytic/pentose gene expression and substrate cycle flux. Endocrinology 145, 1087-1095 https://doi.org/10.1210/en.2003-1173
  77. Zheng, W., Xie, Y., Li, G., Kong, J., Feng, J. Q. and Li, Y. C. (2004). Critical role of calbindin-D28k in calcium homeostasis revealed by mice lacking both vitamin D receptor and calbindin-D28k. J. Biol. Chem. 279, 52406-52413 https://doi.org/10.1074/jbc.M405562200
  78. Ziegler, R. and Kasperk, C. (1998). Glucocorticoid-induced osteoporosis: prevention and treatment. Steroids 63, 344-348 https://doi.org/10.1016/S0039-128X(98)00022-1

Cited by

  1. Assessment of biochemical and immunohistochemical changes in buffalo-cows with reproductive disorders vol.29, pp.3, 2009, https://doi.org/10.1007/s00580-020-03109-9