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Expression and Regulation of Sodium/Calcium Exchangers, NCX and NCKX, in Reproductive Tissues: Do They Play a Critical Role in Calcium Transport for Reproduction and Development?

  • Hyun Yang
  • Kyung-Chul Choi
  • Eui-Man Jung
  • Beum-Soo An
  • Sang-Hwan Hyun
  • Eui-Bae JeungEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 961)

Abstract

Plasma membrane sodium/calcium (Na+/Ca2+) exchangers are an important component of intracellular calcium [Ca2+]i homeostasis and electrical conduction. Na+/Ca2+ exchangers, NCX and NCKX, play a critical role in the transport of one [Ca2+]i and potassium ion across the cell membrane in exchange for four extracellular sodium ions [Na+]e. Mammalian plasma membrane Na+/Ca2+ exchange proteins are divided into two families: one in which Ca2+ flux is dependent only on sodium (NCX1–3) and another in which Ca2+ flux is also dependent on potassium (NCKX1–4). Both molecules are capable of forward- and reverse-mode exchange. In cells and tissues, Na+/Ca2+ (and K+) gradients localize to the cell membrane; thus, the exchangers transport ions across a membrane potential. Uterine NCKX3 has been shown to be involved in the regulation of endometrial receptivity by [Ca2+]i. In the uterus and placenta, NCKX3 expression is regulated by the sex steroid hormone estrogen (E2) and hypoxia stress, respectively. In this chapter, we described the expression and regulation of these proteins for reproductive functions in various tissues including uterus, placenta, and kidney of humans and rodents. Evidence to date suggests that NCKX3 and NCX1 may be regulated in a tissue-specific manner. In addition, we focused on the molecular mechanism involved in the regulation of NCKX3 and NCX1 in mammals, based upon our recent results and those of others.

Keywords

Calcium transport Uterus • Placenta NCKX NCX 

Notes

Acknowledgment

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MEST) (No. 2011–0017948).

References

  1. E. Aneiros, S. Philipp, A. Lis, M. Freichel, A. Cavalie, Modulation of Ca2+ signaling by Na+/Ca2+ exchangers in mast cells. J. Immunol. 174, 119–130 (2005)PubMedGoogle Scholar
  2. L.M. Askie, L. Duley, D.J. Henderson-Smart, L.A. Stewart, Antiplatelet agents for prevention of pre-eclampsia: a meta-analysis of individual patient data. Lancet 369, 1791–1798 (2007)PubMedCrossRefGoogle Scholar
  3. J.M. Belizan, J. Villar, L. Gonzalez, L. Campodonico, E. Bergel, Calcium supplementation to prevent hypertensive disorders of pregnancy. N. Engl. J. Med. 325, 1399–1405 (1991)PubMedCrossRefGoogle Scholar
  4. L. Belkacemi, L. Simoneau, J. Lafond, Calcium-binding proteins: distribution and implication in mammalian placenta. Endocrine 19, 57–64 (2002)PubMedCrossRefGoogle Scholar
  5. L. Belkacemi, I. Bedard, L. Simoneau, J. Lafond, Calcium channels, transporters and exchangers in placenta: a review. Cell Calcium 37, 1–8 (2005)PubMedCrossRefGoogle Scholar
  6. M.J. Berridge, Capacitative calcium entry. Biochem. J. 312, 1–11 (1995)PubMedGoogle Scholar
  7. R.J. Bindels, Calcium handling by the mammalian kidney. J. Exp. Biol. 184, 89–104 (1993)PubMedGoogle Scholar
  8. M.P. Blaustein, W.J. Lederer, Sodium/calcium exchange: its physiological implications. Physiol. Rev. 79, 763–854 (1999)PubMedGoogle Scholar
  9. J.F. Boggess, C. Zhou, V.L. Bae-Jump, P.A. Gehrig, Y.E. Whang, Estrogen-receptor-dependent regulation of telomerase activity in human endometrial cancer cell lines. Gynecol. Oncol. 103, 417–424 (2006)PubMedCrossRefGoogle Scholar
  10. X. Cai, J. Lytton, Molecular cloning of a sixth member of the K+-dependent Na+/Ca2+ exchanger gene family, NCKX6. J. Biol. Chem. 279, 5867–5876 (2004)PubMedCrossRefGoogle Scholar
  11. D.D. Carson, I. Bagchi, S.K. Dey, A.C. Enders, A.T. Fazleabas, B.A. Lessey, K. Yoshinaga, Embryo implantation. Dev. Biol. 223, 217–237 (2000)PubMedCrossRefGoogle Scholar
  12. L. Cervetto, L. Lagnado, R.J. Perry, D.W. Robinson, P.A. McNaughton, Extrusion of calcium from rod outer segments is driven by both sodium and potassium gradients. Nature 337, 740–743 (1989)PubMedCrossRefGoogle Scholar
  13. O. Chernysh, M. Condrescu, J.P. Reeves, Sodium-dependent inactivation of sodium/calcium exchange in transfected Chinese hamster ovary cells. Am. J. Physiol. Cell Physiol. 295, C872–C882 (2008)PubMedCrossRefGoogle Scholar
  14. K.C. Choi, E.B. Jeung, 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 (2008)PubMedCrossRefGoogle Scholar
  15. S. Choudhary, A. Kumar, R.K. Kale, L.G. Raisz, C.C. Pilbeam, Extracellular calcium induces COX-2 in osteoblasts via a PKA pathway. Biochem. Biophys. Res. Commun. 322, 395–402 (2004)PubMedCrossRefGoogle Scholar
  16. S. Christakos, P. Dhawan, B. Benn, A. Porta, M. Hediger, G.T. Oh, E.B. Jeung, Y. Zhong, D. Ajibade, K. Dhawan, S. Joshi, Vitamin D: molecular mechanism of action. Ann. N. Y. Acad. Sci. 1116, 340–348 (2007)PubMedCrossRefGoogle Scholar
  17. D.E. Clapham, Intracellular calcium. Replenishing the stores. Nature 375, 634–635 (1995)PubMedCrossRefGoogle Scholar
  18. N.J. Cook, U.B. Kaupp, Solubilization, purification, and reconstitution of the sodium-calcium exchanger from bovine retinal rod outer segments. J. Biol. Chem. 263, 11382–11388 (1988)PubMedGoogle Scholar
  19. G.P. Daston, J.M. Naciff, Gene expression changes related to growth and differentiation in the fetal and juvenile reproductive system of the female rat: evaluation of microarray results. Reprod. Toxicol. 19, 381–394 (2005)PubMedCrossRefGoogle Scholar
  20. R.J. Diepens, E. den Dekker, M. Bens, A.F. Weidema, A. Vandewalle, R.J. Bindels, J.G. Hoenderop, Characterization of a murine renal distal convoluted tubule cell line for the study of transcellular calcium transport. Am. J. Physiol. Renal Physiol. 286, F483–F489 (2004)PubMedCrossRefGoogle Scholar
  21. H. Dong, Y. Jiang, C.R. Triggle, X. Li, J. Lytton, Novel role for K+-dependent Na+/Ca2+ exchangers in regulation of cytoplasmic free Ca2+ and contractility in arterial smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 291, H1226–H1235 (2006)PubMedCrossRefGoogle Scholar
  22. P.A. Friedman, F.A. Gesek, Stimulation of calcium transport by amiloride in mouse distal convoluted tubule cells. Kidney Int. 48, 1427–1434 (1995)PubMedCrossRefGoogle Scholar
  23. R.D. Geisert, R.H. Renegar, W.W. Thatcher, R.M. Roberts, F.W. Bazer, Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Biol. Reprod. 27, 925–939 (1982)PubMedCrossRefGoogle Scholar
  24. A. Halhali, A.R. Tovar, N. Torres, H. Bourges, M. Garabedian, F. Larrea, 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, 1828–1833 (2000)PubMedCrossRefGoogle Scholar
  25. E.P. Hill, L.D. Longo, Dynamics of maternal-fetal nutrient transfer. Fed. Proc. 39, 239–244 (1980)PubMedGoogle Scholar
  26. J.G. Hoenderop, P.H. Willems, R.J. Bindels, Toward a comprehensive molecular model of active calcium reabsorption. Am. J. Physiol. Renal Physiol. 278, F352–F360 (2000)PubMedGoogle Scholar
  27. J.G. Hoenderop, O. Dardenne, M. Van Abel, A.W. Van Der Kemp, C.H. Van Os, R. St Arnaud, R.J. Bindels, 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 (2002a)PubMedCrossRefGoogle Scholar
  28. J.G. Hoenderop, B. Nilius, R.J. Bindels, Molecular mechanism of active Ca2+ reabsorption in the distal nephron. Annu. Rev. Physiol. 64, 529–549 (2002b)PubMedCrossRefGoogle Scholar
  29. G.J. Hofmeyr, L. Duley, A. Atallah, Dietary calcium supplementation for prevention of pre-eclampsia and related problems: a systematic review and commentary. BJOG 114, 933–943 (2007)PubMedCrossRefGoogle Scholar
  30. E.J. Hong, K.C. Choi, E.B. Jeung, Induction of calbindin-D9k messenger RNA and protein by maternal exposure to alkylphenols during late pregnancy in maternal and neonatal uteri of rats. Biol. Reprod. 71, 669–675 (2004)PubMedCrossRefGoogle Scholar
  31. D. Jeon, Y.M. Yang, M.J. Jeong, K.D. Philipson, H. Rhim, H.S. Shin, Enhanced learning and memory in mice lacking Na+/Ca2+ exchanger 2. Neuron 38, 965–976 (2003)PubMedCrossRefGoogle Scholar
  32. S.G. Kamath, C.H. Smith, Na+/Ca2+ exchange, Ca2+ binding, and electrogenic Ca2+ transport in plasma membranes of human placental syncytiotrophoblast. Pediatr. Res. 36, 461–467 (1994)PubMedCrossRefGoogle Scholar
  33. R.C. Khanal, I. Nemere, Endocrine regulation of calcium transport in epithelia. Clin. Exp. Pharmacol. Physiol. 35, 1277–1287 (2008)PubMedCrossRefGoogle Scholar
  34. L. Kiedrowski, High activity of K+-dependent plasmalemmal Na+/Ca2+ exchangers in hippocampal CA1 neurons. Neuroreport 15, 2113–2116 (2004)PubMedCrossRefGoogle Scholar
  35. L. Kiedrowski, A. Czyz, X.F. Li, J. Lytton, Preferential expression of plasmalemmal K-dependent Na+/Ca2+ exchangers in neurons versus astrocytes. Neuroreport 13, 1529–1532 (2002)PubMedCrossRefGoogle Scholar
  36. L. Kiedrowski, A. Czyz, G. Baranauskas, X.F. Li, J. Lytton, Differential contribution of plasmalemmal Na/Ca exchange isoforms to sodium-dependent calcium influx and NMDA excitotoxicity in depolarized neurons. J. Neurochem. 90, 117–128 (2004)PubMedCrossRefGoogle Scholar
  37. M.H. Kim, N. Korogod, R. Schneggenburger, W.K. Ho, S.H. Lee, Interplay between Na+/Ca2+ exchangers and mitochondria in Ca2+ clearance at the calyx of Held. J. Neurosci. 25, 6057–6065 (2005)PubMedCrossRefGoogle Scholar
  38. J.C. Kingdom, P. Kaufmann, Oxygen and placental vascular development. Adv. Exp. Med. Biol. 474, 259–275 (1999)PubMedCrossRefGoogle Scholar
  39. S.N. Kip, N.W. Gray, A. Burette, A. Canbay, R.J. Weinberg, E.E. Strehler, Changes in the expression of plasma membrane calcium extrusion systems during the maturation of hippocampal neurons. Hippocampus 16, 20–34 (2006)PubMedCrossRefGoogle Scholar
  40. P. Kofuji, R.W. Hadley, R.S. Kieval, W.J. Lederer, D.H. Schulze, Expression of the Na-Ca exchanger in diverse tissues: a study using the cloned human cardiac Na-Ca exchanger. Am. J. Physiol. 263, C1241–C1249 (1992)PubMedGoogle Scholar
  41. T.H. Koo, H. Yang, B.S. An, K.C. Choi, S.H. Hyun, E.B. Jeung, Calcium transport genes are differently regulated in maternal and fetal placenta in the knockout mice of calbindin-D(9k) and -D(28k). Mol Reprod Dev. 79(5), 346–355 (2012)Google Scholar
  42. C.S. Kovacs, H.M. Kronenberg, Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr. Rev. 18, 832–872 (1997)PubMedCrossRefGoogle Scholar
  43. A. Kraev, B.D. Quednau, S. Leach, X.F. Li, H. Dong, R. Winkfein, M. Perizzolo, X. Cai, R. Yang, K.D. Philipson, J. Lytton, Molecular cloning of a third member of the potassium-dependent sodium-calcium exchanger gene family, NCKX3. J. Biol. Chem. 276, 23161–23172 (2001)PubMedCrossRefGoogle Scholar
  44. J. Lafond, M. Leclerc, M.G. Brunette, Characterization of calcium transport by basal plasma membranes from human placental syncytiotrophoblast. J. Cell. Physiol. 148, 17–23 (1991)PubMedCrossRefGoogle Scholar
  45. R.L. Lamason, M.A. Mohideen, J.R. Mest, A.C. Wong, H.L. Norton, M.C. Aros, M.J. Jurynec, X. Mao, V.R. Humphreville, J.E. Humbert, S. Sinha, J.L. Moore, P. Jagadeeswaran, W. Zhao, G. Ning, I. Makalowska, P.M. McKeigue, D. O’Donnell, R. Kittles, E.J. Parra, N.J. Mangini, D.J. Grunwald, M.D. Shriver, V.A. Canfield, K.C. Cheng, SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310, 1782–1786 (2005)PubMedCrossRefGoogle Scholar
  46. G.S. Lee, E.B. Jeung, Uterine TRPV6 expression during the estrous cycle and pregnancy in a mouse model. Am. J. Physiol. Endocrinol. Metab. 293, E132–E138 (2007)PubMedCrossRefGoogle Scholar
  47. H.C. Lee, B.K. Lum, Protective action of calcium entry blockers in endotoxin shock. Circ. Shock 18, 193–203 (1986)PubMedGoogle Scholar
  48. S.H. Lee, M.H. Kim, K.H. Park, Y.E. Earm, W.K. Ho, K+-dependent Na+/Ca2+ exchange is a major Ca2+ clearance mechanism in axon terminals of rat neurohypophysis. J. Neurosci. 22, 6891–6899 (2002)PubMedGoogle Scholar
  49. G.S. Lee, K.Y. Lee, K.C. Choi, Y.H. Ryu, S.G. Paik, G.T. Oh, E.B. Jeung, 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 (2007)PubMedCrossRefGoogle Scholar
  50. R.J. Levine, J.C. Hauth, L.B. Curet, B.M. Sibai, P.M. Catalano, C.D. Morris, R. DerSimonian, J.R. Esterlitz, E.G. Raymond, D.E. Bild, J.D. Clemens, J.A. Cutler, Trial of calcium to prevent preeclampsia. N. Engl. J. Med. 337, 69–76 (1997)PubMedCrossRefGoogle Scholar
  51. X.F. Li, A.S. Kraev, J. Lytton, Molecular cloning of a fourth member of the potassium-dependent sodium-calcium exchanger gene family, NCKX4. J. Biol. Chem. 277, 48410–48417 (2002)PubMedCrossRefGoogle Scholar
  52. X.F. Li, L. Kiedrowski, F. Tremblay, F.R. Fernandez, M. Perizzolo, R.J. Winkfein, R.W. Turner, J.S. Bains, D.E. Rancourt, J. Lytton, Importance of K+-dependent Na+/Ca2+-exchanger 2, NCKX2, in motor learning and memory. J. Biol. Chem. 281, 6273–6282 (2006)PubMedCrossRefGoogle Scholar
  53. S. Longoni, E. Carafoli, Identification of the Na+/Ca2+ exchanger of calf heart sarcolemma with the help of specific antibodies. Biochem. Biophys. Res. Commun. 145, 1059–1063 (1987)PubMedCrossRefGoogle Scholar
  54. K.C. Luu, G.Y. Nie, A. Hampton, G.Q. Fu, Y.X. Liu, L.A. Salamonsen, Endometrial expression of calbindin (CaBP)-d28k but not CaBP-d9k in primates implies evolutionary changes and functional redundancy of calbindins at implantation. Reproduction 128, 433–441 (2004)PubMedCrossRefGoogle Scholar
  55. J. Lytton, Na+/Ca2+ exchangers: three mammalian gene families control Ca2+ transport. Biochem. J. 406, 365–382 (2007)PubMedCrossRefGoogle Scholar
  56. J. Lytton, X.F. Li, H. Dong, A. Kraev, K+-dependent Na+/Ca2+ exchangers in the brain. Ann. N. Y. Acad. Sci. 976, 382–393 (2002)PubMedCrossRefGoogle Scholar
  57. A. Malassine, L. Cronier, Hormones and human trophoblast differentiation: a review. Endocrine 19, 3–11 (2002)PubMedCrossRefGoogle Scholar
  58. L. Marions, K.G. Danielsson, Expression of cyclo-oxygenase in human endometrium during the implantation period. Mol. Hum. Reprod. 5, 961–965 (1999)PubMedCrossRefGoogle Scholar
  59. R. Moreau, G. Daoud, A. Masse, L. Simoneau, J. Lafond, Expression and role of calcium-ATPase pump and sodium-calcium exchanger in differentiated trophoblasts from human term placenta. Mol. Reprod. Dev. 65, 283–288 (2003a)PubMedCrossRefGoogle Scholar
  60. R. Moreau, L. Simoneau, J. Lafond, Calcium fluxes in human trophoblast (BeWo) cells: calcium channels, calcium-ATPase, and sodium-calcium exchanger expression. Mol. Reprod. Dev. 64, 189–198 (2003b)PubMedCrossRefGoogle Scholar
  61. D.A. Nicoll, S. Longoni, K.D. Philipson, Molecular cloning and functional expression of the cardiac sarcolemmal Na+-Ca2+ exchanger. Science 250, 562–565 (1990)PubMedCrossRefGoogle Scholar
  62. D.A. Nicoll, B.D. Quednau, Z. Qui, Y.R. Xia, A.J. Lusis, K.D. Philipson, Cloning of a third mammalian Na+-Ca2+ exchanger, NCX3. J. Biol. Chem. 271, 24914–24921 (1996)PubMedCrossRefGoogle Scholar
  63. T. Nijenhuis, J.G. Hoenderop, A.W. van der Kemp, R.J. Bindels, Localization and regulation of the epithelial Ca2+ channel TRPV6 in the kidney. J. Am. Soc. Nephrol. 14, 2731–2740 (2003)PubMedCrossRefGoogle Scholar
  64. L.A. Opperman, T.J. Saunders, D.E. Bruns, J.C. Boyd, S.E. Mills, M.E. Bruns, Estrogen inhibits calbindin-D28k expression in mouse uterus. Endocrinology 130, 1728–1735 (1992)PubMedCrossRefGoogle Scholar
  65. R. Palty, E. Ohana, M. Hershfinkel, M. Volokita, V. Elgazar, O. Beharier, W.F. Silverman, M. Argaman, I. Sekler, Lithium-calcium exchange is mediated by a distinct potassium-independent sodium-calcium exchanger. J. Biol. Chem. 279, 25234–25240 (2004)PubMedCrossRefGoogle Scholar
  66. R.C. Peck, A.M. Lefer, Protective effect of nifedipine in the hypoxic perfused cat liver. Agents Actions 11, 421–424 (1981)PubMedCrossRefGoogle Scholar
  67. J.B. Peng, E.M. Brown, M.A. Hediger, Apical entry channels in calcium-transporting epithelia. News Physiol. Sci. 18, 158–163 (2003)PubMedGoogle Scholar
  68. R.M. Pitkin, Endocrine regulation of calcium homeostasis during pregnancy. Clin. Perinatol. 10, 575–592 (1983)PubMedGoogle Scholar
  69. C. Pott, S.A. Henderson, J.I. Goldhaber, K.D. Philipson, Na+/Ca2+ exchanger knockout mice: plasticity of cardiac excitation-contraction coupling. Ann. N. Y. Acad. Sci. 1099, 270–275 (2007)PubMedCrossRefGoogle Scholar
  70. A. Psychoyos, Hormonal control of uterine receptivity for nidation. J. Reprod. Fertil. 25(Suppl), 17–28 (1976)Google Scholar
  71. A. Psychoyos, Uterine receptivity for nidation. Ann. N. Y. Acad. Sci. 476, 36–42 (1986)PubMedCrossRefGoogle Scholar
  72. B.D. Quednau, D.A. Nicoll, K.D. Philipson, Tissue specificity and alternative splicing of the Na+/Ca2+ exchanger isoforms NCX1, NCX2, and NCX3 in rat. Am. J. Physiol. 272, C1250–C1261 (1997)PubMedGoogle Scholar
  73. H. Rasmussen, The calcium messenger system (2). N. Engl. J. Med. 314, 1164–1170 (1986)PubMedCrossRefGoogle Scholar
  74. C.W. Redman, I.L. Sargent, Placental stress and pre-eclampsia: a revised view. Placenta 30(Suppl A), S38–S42 (2009)PubMedCrossRefGoogle Scholar
  75. H. Reilander, A. Achilles, U. Friedel, G. Maul, F. Lottspeich, N.J. Cook, Primary structure and functional expression of the Na/Ca, K-exchanger from bovine rod photoreceptors. EMBO J. 11, 1689–1695 (1992)PubMedGoogle Scholar
  76. N.J. Robinson, M. Wareing, N.K. Hudson, R.T. Blankley, P.N. Baker, J.D. Aplin, I.P. Crocker, Oxygen and the liberation of placental factors responsible for vascular compromise. Lab. Invest. 88, 293–305 (2008)PubMedCrossRefGoogle Scholar
  77. L.A. Salamonsen, G. Nie, E. Dimitriadis, L. Robb, J.K. Findlay, Genes involved in implantation. Reprod. Fertil. Dev. 13, 41–49 (2001)PubMedCrossRefGoogle Scholar
  78. B.M. Sanborn, Relationship of ion channel activity to control of myometrial calcium. J. Soc. Gynecol. Investig. 7, 4–11 (2000)PubMedCrossRefGoogle Scholar
  79. S. Schlafke, A.C. Enders, Cellular basis of interaction between trophoblast and uterus at implantation. Biol. Reprod. 12, 41–65 (1975)PubMedCrossRefGoogle Scholar
  80. P.P. Schnetkamp, Sodium-calcium exchange in the outer segments of bovine rod photoreceptors. J. Physiol. 373, 25–45 (1986)PubMedGoogle Scholar
  81. P.P. Schnetkamp, Calcium homeostasis in vertebrate retinal rod outer segments. Cell Calcium 18, 322–330 (1995)PubMedCrossRefGoogle Scholar
  82. P.P. Schnetkamp, D.K. Basu, R.T. Szerencsei, Na+-Ca2+ exchange in bovine rod outer segments requires and transports K+. Am. J. Physiol. 257, C153–C157 (1989)PubMedGoogle Scholar
  83. E.W. Seely, R.J. Wood, E.M. Brown, S.W. Graves, Lower serum ionized calcium and abnormal calciotropic hormone levels in preeclampsia. J. Clin. Endocrinol. Metab. 74, 1436–1440 (1992)PubMedCrossRefGoogle Scholar
  84. K.A. Seta, Y. Yuan, Z. Spicer, G. Lu, J. Bedard, T.K. Ferguson, P. Pathrose, A. Cole-Strauss, A. Kaufhold, D.E. Millhorn, The role of calcium in hypoxia-induced signal transduction and gene expression. Cell Calcium 36, 331–340 (2004)PubMedCrossRefGoogle Scholar
  85. A. Sharkey, Cytokines and implantation. Rev. Reprod. 3, 52–61 (1998)PubMedCrossRefGoogle Scholar
  86. B. Sibai, G. Dekker, M. Kupferminc, Pre-eclampsia. Lancet 365, 785–799 (2005)PubMedGoogle Scholar
  87. J. Stulc, B. Stulcova, C.P. Sibley, Evidence for active maternal-fetal transport of Na+ across the placenta of the anaesthetized rat. J. Physiol. 470, 637–649 (1993)PubMedGoogle Scholar
  88. J. Stulc, B. Stulcova, M. Smid, I. Sach, Parallel mechanisms of Ca++ transfer across the perfused human ­placental cotyledon. Am. J. Obstet. Gynecol. 170, 162–167 (1994)PubMedCrossRefGoogle Scholar
  89. G.A. Surveyor, A.K. Wilson, D.R. Brigstock, Localization of connective tissue growth factor during the period of embryo implantation in the mouse. Biol. Reprod. 59, 1207–1213 (1998)PubMedCrossRefGoogle Scholar
  90. M. Tsoi, K.H. Rhee, D. Bungard, X.F. Li, S.L. Lee, R.N. Auer, J. Lytton, Molecular cloning of a novel potassium-dependent sodium-calcium exchanger from rat brain. J. Biol. Chem. 273, 4155–4162 (1998)PubMedCrossRefGoogle Scholar
  91. S.J. Van Cromphaut, M. Dewerchin, J.G. Hoenderop, I. Stockmans, E. Van Herck, S. Kato, R.J. Bindels, D. Collen, P. Carmeliet, R. Bouillon, G. Carmeliet, Duodenal calcium absorption in vitamin D receptor-knockout mice: functional and molecular aspects. Proc. Natl. Acad. Sci. U. S. A. 98, 13324–13329 (2001)PubMedCrossRefGoogle Scholar
  92. S.J. Van Cromphaut, K. Rummens, I. Stockmans, E. Van Herck, F.A. Dijcks, A.G. Ederveen, P. Carmeliet, J. Verhaeghe, R. Bouillon, G. Carmeliet, 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 (2003)PubMedCrossRefGoogle Scholar
  93. N. Wanaverbecq, S.J. Marsh, M. Al-Qatari, D.A. Brown, The plasma membrane calcium-ATPase as a major mechanism for intracellular calcium regulation in neurones from the rat superior cervical ganglion. J. Physiol. 550, 83–101 (2003)PubMedCrossRefGoogle Scholar
  94. J.M. Williams, D.R. Abramovich, C.G. Dacke, T.M. Mayhew, K.R. Page, Inhibitor action on placental calcium transport. Calcif. Tissue Int. 48, 7–12 (1991)PubMedCrossRefGoogle Scholar
  95. S. Wray, K. Jones, S. Kupittayanant, Y. Li, A. Matthew, E. Monir-Bishty, K. Noble, S.J. Pierce, S. Quenby, A.V. Shmygol, Calcium signaling and uterine contractility. J. Soc. Gynecol. Investig. 10, 252–264 (2003)PubMedCrossRefGoogle Scholar
  96. H. Yang, T.H. Kim, B.S. An, K.C. Choi, H.H. Lee, J.M. Kim, E.B. Jeung, Differential expression of calcium transport channels in placenta primary cells and tissues derived from preeclamptic placenta. Mol Cell Endocrinol (in submission)Google Scholar
  97. H. Yang, G.S. Lee, Y.M. Yoo, K.C. Choi, E.B. Jeung, Sodium/potassium/calcium exchanger 3 is regulated by the steroid hormones estrogen and progesterone in the uterus of mice during the estrous cycle. Biochem. Biophys. Res. Commun. 385, 279–283 (2009)PubMedCrossRefGoogle Scholar
  98. H. Yang, Y.M. Yoo, E.M. Jung, K.C. Choi, E.B. Jeung, Uterine expression of sodium/potassium/calcium exchanger 3 and its regulation by sex-steroid hormones during the estrous cycle of rats. Mol. Reprod. Dev. 77, 971–977 (2010)PubMedCrossRefGoogle Scholar
  99. H. Yang, T.H. Kim, H.H. Lee, K.C. Choi, E.B. Jeung, Distinct expression of the calcium exchangers, NCKX3 and NCX1, and their regulation by steroid in the human endometrium during the menstrual cycle. Reprod. Sci. 18, 577–585 (2011)PubMedCrossRefGoogle Scholar
  100. K. Yoshinaga, Uterine receptivity for blastocyst implantation. Ann. N. Y. Acad. Sci. 541, 424–431 (1988)PubMedCrossRefGoogle Scholar
  101. W. Zheng, Y. Xie, G. Li, J. Kong, J.Q. Feng, Y.C. Li, 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 (2004)PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Hyun Yang
    • 1
  • Kyung-Chul Choi
    • 1
  • Eui-Man Jung
    • 1
  • Beum-Soo An
    • 1
  • Sang-Hwan Hyun
    • 1
  • Eui-Bae Jeung
    • 1
    Email author
  1. 1.Laboratory of Veterinary Biochemistry and Molecular Biology, College of Veterinary MedicineChungbuk National UniversityCheongjuRepublic of Korea

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