Recent structural and functional insights into the family of sodium calcium exchangers

Genesis

Volumn 52, Issue 2, 2014, Pages 93-109

  Sharma, Vishal ^a,b   O'Halloran, Damien M ^a,b  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Antiporter; Caenorhabditis elegans; Calcium homeostasis; Sodium calcium exchange; Sodium calcium potassium exchange

Indexed keywords

ANTIPORTER; CAENORHABDITIS ELEGANS; CALCIUM HOMEOSTASIS; SODIUM CALCIUM EXCHANGE; SODIUM CALCIUM POTASSIUM EXCHANGE;

ANIMALS; CAENORHABDITIS ELEGANS; CALCIUM; CALCIUM SIGNALING; GENE EXPRESSION REGULATION; HUMANS; MITOCHONDRIA; MODELS, MOLECULAR; MULTIGENE FAMILY; PHYLOGENY; SODIUM-CALCIUM EXCHANGER;

EID: 84894237451     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22735     Document Type: Review

References (105)

1. Altimimi HF, Fung EH, Winkfein RJ, Schnetkamp PPM. 2010. Residues contributing to the na(+)-binding pocket of the SLC24 na(+)/ca(2+)-K(+) exchanger NCKX2. J Biol Chem 285:15245-15255.
2. Arnaudeau S, Kelley WL, Walsh Jr JV, Demaurex N. 2001. Mitochondria recycle ca(2+) to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J Biol Chem 276:29430-29439.
3. Baker PF, Blaustein MP, Hodgkin AL, Steinhardt RA. 1969. The influence of calcium on sodium efflux in squid axons. J Physiol. 200(2):431-458.
4. Begley JG, Duan W, Chan S, Duff K, Mattson MP. 1999. Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice. J Neurochem 72:1030-1039.
5. Bitsch A, Schuchardt J, Bunkowski S, Kuhlmann T, Bruck W. 2000. Acute axonal injury in multiple sclerosis. correlation with demyelination and inflammation. Brain 123(Pt 6):1174-1183.
6. Blaustein MP. 1968. Barbiturates block sodium and potassium conductance increases in voltage-clamped lobster axons. J Gen Physiol. 51(3):293-307.
7. Boscia F, D'Avanzo C, Pannaccione A, Secondo A, Casamassa A, et al. 2013. New roles of NCX in glial cells: Activation of microglia in ischemia and differentiation of oligodendrocytes. Adv Exp Med Biol 961:307-316.
8. Boscia F, D'Avanzo C, Pannaccione A, Secondo A, Casamassa A, et al. 2012. Silencing or knocking out the na(+)/ca(2+) exchanger-3 (NCX3) impairs oligodendrocyte differentiation. Cell Death Differ 19:562-572.
9. Boscia F, Gala R, Pannaccione A, Secondo A, Scorziello A, et al. 2009. NCX1 expression and functional activity increase in microglia invading the infarct core. Stroke 40:3608-3617.
10. Cai X, Lytton J. 2004a. The cation/ca(2+) exchanger superfamily: Phylogenetic analysis and structural implications. Mol Biol Evol 21:1692-1703.
11. Cai X, Lytton J. 2004b. Molecular cloning of a sixth member of the K+-dependent na+/Ca2+ exchanger gene family, NCKX6. J Biol Chem 279:5867-5876.
12. Candy SM, Szatkowski MS. 2000. Chronic hyperglycaemia increases neuronal sensitivity to high potassium in hippocampal slices from streptozotocin-treated diabetic rats. Neurosci Lett 279:105-108.
13. Canitano A, Papa M, Boscia F, Castaldo P, Sellitti S, et al 2002. Brain distribution of the na+/Ca2+ exchanger-encoding genes NCX1, NCX2, and NCX3 and their related proteins in the central nervous system. Ann N Y Acad Sci 976:394-404.
14. Carafoli E, Tiozzo R, Lugli G, Crovetti F, Kratzing C. 1974. The release of calcium from heart mitochondria by sodium. J Mol Cell Cardiol 6:361-371.
15. Castaldo P, Cataldi M, Magi S, Lariccia V, Arcangeli S, et al. 2009. Role of the mitochondrial sodium/calcium exchanger in neuronal physiology and in the pathogenesis of neurological diseases. Prog Neurobiol 87:58-79.
16. Cervetto L, Lagnado L, Perry RJ, Robinson DW, McNaughton PA. 1989. Extrusion of calcium from rod outer segments is driven by both sodium and potassium gradients. Nature 337:740-743.
17. Chen G, Yang X, Alber S, Shusterman V, Salama G. 2011. Regional genomic regulation of cardiac sodium-calcium exchanger by oestrogen. J Physiol 589:1061-1080.
18. Cheng G, Hagen TP, Dawson ML, Barnes KV, Menick DR. 1999. The role of GATA, CArG, E-box, and a novel element in the regulation of cardiac expression of the na+-Ca2+ exchanger gene. J Biol Chem 274: 12819-12826.
19. Coates JC, de Bono M. 2002. Antagonistic pathways in neurons exposed to body fluid regulate social feeding in caenorhabditis elegans. Nature 419:925-929.
20. Contreras L, Satrústegui J. 2009. Calcium signaling in brain mitochondria: Interplay of malate aspartate NADH shuttle and calcium uniporter/mitochondrial dehydrogenase pathways. J Biol Chem 284:7091-7099.
21. Craner MJ, Newcombe J, Black JA, Hartle C, Cuzner ML, et al. 2004. Molecular changes in neurons in multiple sclerosis: Altered axonal expression of Nav1.2 and Nav1.6 sodium channels and na+/Ca2+ exchanger. Proc Natl Acad Sci USA 101:8168-8173.
22. Crompton M, Moser R, Ludi H, Carafoli E. 1978. The interrelations between the transport of sodium and calcium in mitochondria of various mammalian tissues. Eur J Biochem 82:25-31.
23. Daston GP, Naciff JM. 2005. 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.
24. Dong H, Light PE, French RJ, Lytton J. 2001. Electrophysiological characterization and ionic stoichiometry of the rat brain K(+)-dependent NA(+)/CA(2+) exchanger, NCKX2. J Biol Chem 276:25919-25928.
25. Dong H, Jiang Y, Triggle CR, Li X, Lytton J. 2006. 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.
26. Garcia-Chacon LE, Nguyen KT, David G, Barrett EF. 2006. Extrusion of Ca2+ from mouse motor terminal mitochondria via a na+-Ca2+ exchanger increases post-tetanic evoked release. J Physiol 574:663-675.
27. Giladi M, Khananshvili D. 2013. Molecular determinants of allosteric regulation in NCX proteins. Adv Exp Med Biol 961:35-48.
28. Giladi M, Boyman L, Mikhasenko H, Hiller R, Khananshvili D, 2010. Essential role of the CBD1-CBD2 linker in slow dissociation of Ca2+ from the regulatory two-domain tandem of NCX1. J Biol Chem 285:28117-28125.
29. Giladi M, Friedberg I, Fang X, Hiller R, Wang Y, et al. 2012. G503 is obligatory for coupling of regulatory domains in NCX proteins. Biochemistry 51:7313-7320.
30. Ginger RS, Askew SE, Ogborne RM, Wilson S, Ferdinando D, et al. 2008. SLC24A5 encodes a trans-golgi network protein with potassium-dependent sodium-calcium exchange activity that regulates human epidermal melanogenesis. J Biol Chem 283:5486-5495.
31. Gobbi P, Castaldo P, Minelli A, Salucci S, Magi S, et al. 2007. Mitochondrial localization of na+/Ca2+ exchangers NCX1-3 in neurons and astrocytes of adult rat brain in situ. Pharmacol Res 56:556-565.
32. Herchuelz A, Kamagate A, Ximenes H, Van Eylen F. 2007. Role of na/ca exchange and the plasma membrane Ca2+-ATPase in beta cell function and death. Ann NY Acad Sci 1099:456-467.
33. Hilge M, Aelen J, Vuister GW. 2006. Ca2+ regulation in the na+/Ca2+ exchanger involves two markedly different Ca2+ sensors. Mol Cell 22:15-25.
34. Hilge M, Aelen J, Foarce A, Perrakis A, Vuister GW. 2009. Ca2+ regulation in the na+/Ca2+ exchanger features a dual electrostatic switch mechanism. Proc Natl Acad Sci USA 106:14333-14338.
35. Hilgemann DW, Nicoll DA, Philipson KD. 1991. Charge movement during na+ translocation by native and cloned cardiac na+/Ca2+ exchanger. Nature 352:715-718.
36. Ichas F, Mazat JP. 1998. From calcium signaling to cell death: Two conformations for the mitochondrial permeability transition pore. switching from low- to high-conductance state. Biochim Biophys Acta 1366:33-50.
37. Jeon D, Yang YM, Jeong MJ, Philipson KD, Rhim H, et al. 2003. Enhanced learning and memory in mice lacking na+/Ca2+ exchanger 2. Neuron 38:965-976.
38. Jung DW, Baysal K, Brierley GP. 1995. The sodium-calcium antiport of heart mitochondria is not electroneutral. J Biol Chem 270:672-678.
39. Kang K, Schnetkamp PPM. 2003. Signal sequence cleavage and plasma membrane targeting of the retinal rod NCKX1 and cone NCKX2 na+/Ca2+-K+ exchangers. Biochemistry 42:9438-9445.
40. Kang K, Kinjo TG, Szerencsei RT, Schnetkamp PPM. 2005a. Residues contributing to the Ca2+ and K+ binding pocket of the NCKX2 na+/Ca2+-K+ exchanger. J Biol Chem 280:6823-6833.
41. Kang K, Shibukawa Y, Szerencsei RT, Schnetkamp PPM. 2005b. Substitution of a single residue, Asp575, renders the NCKX2 K+-dependent na+/Ca2+ exchanger independent of K+. J Biol Chem 280:6834-6839.
42. Kang TM, Hilgemann DW. 2004. Multiple transport modes of the cardiac na+/Ca2+ exchanger. Nature 427:544-548.
43. Kim B, Matsuoka S. 2008. Cytoplasmic na+-dependent modulation of mitochondrial Ca2+ via electrogenic mitochondrial na+-Ca2+ exchange. J Physiol 586:1683-1697.
44. Kim B, Takeuchi A, Koga O, Hikida M, Matsuoka S. 2012. Pivotal role of mitochondrial na(+)(-)ca(2)(+) exchange in antigen receptor mediated ca(2)(+) signalling in DT40 and A20 B lymphocytes. J Physiol 590:459-474.
45. Kinjo TG, Szerencsei RT, Winkfein RJ, Kang K, Schnetkamp PPM. 2003. Topology of the retinal cone NCKX2 na/ca-K exchanger. Biochemistry 42:2485-2491.
46. Kofuji P, Lederer WJ, Schulze DH. 1994. Mutually exclusive and cassette exons underlie alternatively spliced isoforms of the na/ca exchanger. J Biol Chem 269:5145-5149.
47. Kovacs R, Kardos J, Heinemann U, Kann O. 2005. Mitochondrial calcium ion and membrane potential transients follow the pattern of epileptiform discharges in hippocampal slice cultures. J Neurosci 25:4260-4269.
48. Kovacs R, Schuchmann S, Gabriel S, Kann O, Kardos J. et al. 2002. Free radical-mediated cell damage after experimental status epilepticus in hippocampal slice cultures. J Neurophysiol 88:2909-2918.
49. Kraev A, Quednau BD, Leach S, Li XF, Dong H, et al. 2001. Molecular cloning of a third member of the potassium-dependent sodium-calcium exchanger gene family, NCKX3. J Biol Chem 276:23161-23172.
50. Lamason RL, Mohideen MPK, Mest JR, Wong AC, Norton HL, et al. 2005. SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310:1782-1786.
51. Ledeen RW, Wu G. 2007. Sodium-calcium exchangers in the nucleus: An unexpected locus and an unusual regulatory mechanism. Ann NY Acad Sci 1099:494-506.
52. Lee KH, Lee JS, Lee D, Seog DH, Lytton J, et al. 2012. KIF21A-mediated axonal transport and selective endocytosis underlie the polarized targeting of NCKX2. J Neurosci 32:4102-4117.
53. Li W, Shariat-Madar Z, Powers M, Sun X, Lane RD, et al. 1992. Reconstitution, identification, purification, and immunological characterization of the 110-kDa na+/Ca2+ antiporter from beef heart mitochondria. J Biol Chem 267:17983-17989.
54. Li X, Kraev AS, Lytton J. 2002. Molecular cloning of a fourth member of the potassium-dependent sodium-calcium exchanger gene family, NCKX4. J Biol Chem 277:48410-48417.
55. Li X, Kiedrowski L, Tremblay F, Fernandez FR, Perizzolo M, et al. 2006. Importance of K+-dependent na+/Ca2+-exchanger 2, NCKX2, in motor learning and memory. J Biol Chem 281:6273-6282.
56. Li Z, Matsuoka S, Hryshko LV, Nicoll DA, Bersohn MM, et al. 1994. Cloning of the NCX2 isoform of the plasma membrane na(+)-Ca2+ exchanger. J Biol Chem 269:17434-17439.
57. Liao J, Li H, Zeng W, Sauer DB, Belmares R, et al. 2012. Structural insight into the ion-exchange mechanism of the sodium/calcium exchanger. Science 335:686-690.
58. Luther PW, Yip RK, Bloch RJ, Ambesi A, Lindenmayer GE, et al. 1992. Presynaptic localization of sodium/calcium exchangers in neuromuscular preparations. J Neurosci 12:4898-4904.
59. Lytton J, Li X, Dong H, Kraev A. 2002. K+-dependent na+/Ca2+ exchangers in the brain. Ann NY Acad Sci 976:382-393.
60. Ma H, Sumbilla CM, Farrance IKG, Klein MG, Inesi G. 2004. Cell-specific expression of SERCA, the exogenous Ca2+ transport ATPase, in cardiac myocytes. Am J Physiol Cell Physiol 286:C556-C564.
61. Mani SK, Egan EA, Addy BK, Grimm M, Kasiganesan H, et al. 2010. Beta-adrenergic receptor stimulated Ncx1 upregulation is mediated via a CaMKII/AP-1 signaling pathway in adult cardiomyocytes. J Mol Cell Cardiol 48:342-351.
62. Marks JD, Boriboun C, Wang J. 2005. Mitochondrial nitric oxide mediates decreased vulnerability of hippocampal neurons from immature animals to NMDA. J Neurosci 25:6561-6575.
63. Matsuoka S, Nicoll DA, He Z, Philipson KD. 1997. Regulation of cardiac na(+)-Ca2+ exchanger by the endogenous XIP region. J Gen Physiol 109:273-286.
64. Menick DR, Renaud L, Buchholz A, Muller JG, Zhou H, et al. 2007. Regulation of Ncx1 gene expression in the normal and hypertrophic heart. Ann NY Acad Sci 1099:195-203.
65. Molinaro P, Viggiano D, Nistico R, Sirabella R, Secondo A, et al. 2011. Na+ -Ca2+ exchanger (NCX3) knock-out mice display an impairment in hippocampal long-term potentiation and spatial learning and memory. J Neurosci 31:7312-7321.
66. Molinaro P, Cuomo O, Pignataro G, Boscia F, Sirabella R, et al. 2008. Targeted disruption of na+/Ca2+ exchanger 3 (NCX3) gene leads to a worsening of ischemic brain damage. J Neurosci 28:1179-1184.
67. Murata H, Hotta S, Sawada E, Yamamura H, Ohya S, et al. 2010. Cellular Ca2+ dynamics in urinary bladder smooth muscle from transgenic mice overexpressing na+-Ca2+ exchanger. J Pharmacol Sci 112:373-377.
68. Nicoll DA, Quednau BD, Qui Z, Xia YR, Lusis AJ, et al. 1996. Cloning of a third mammalian na+-Ca2+ exchanger, NCX3. J Biol Chem 271:24914-24921.
69. Niggli V, Sigel E, Carafoli E. 1982. The purified Ca2+ pump of human erythrocyte membranes catalyzes an electroneutral Ca2+-H+ exchange in reconstituted liposomal systems. J Biol Chem 257:2350-2356.
70. Nishizawa T, Kita S, Maturana AD, Furuya N, Hirata K, et al. 2013. Structural basis for the counter-transport mechanism of a H+/Ca2+ exchanger. Science 341:168-172.
71. O'Rourke EJ, Soukas AA, Carr CE, Ruvkun G. 2009. C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell Metab 10:430-435.
72. Palty R, Ohana E, Hershfinkel M, Volokita M, Elgazar V, et al. 2004. Lithium-calcium exchange is mediated by a distinct potassium-independent sodium-calcium exchanger. J Biol Chem 279:25234-25240.
73. Palty R, Silverman WF, Hershfinkel M, Caporale T, Sensi SL, et al. 2010. NCLX is an essential component of mitochondrial na+/Ca2+ exchange. Proc Natl Acad Sci USA 107:436-441.
74. Pannaccione A, Secondo A, Molinaro P, D'Avanzo C, Cantile M, et al. 2012. A new concept: Aβ1-42 generates a hyperfunctional proteolytic NCX3 fragment that delays caspase-12 activation and neuronal death. J Neurosci 32:10609-10617.
75. Pignataro G, Boscia F, Esposito E, Sirabella R, Cuomo O, et al. 2012. NCX1 and NCX3: Two new effectors of delayed preconditioning in brain ischemia. Neurobiol Dis 45:616-623.
76. Pignataro G, Esposito E, Cuomo O, Sirabella R, Boscia F, et al. 2011. The NCX3 isoform of the na+/Ca2+ exchanger contributes to neuroprotection elicited by ischemic postconditioning. J Cereb Blood Flow Metab 31:362-370.
77. Quednau BD, Nicoll DA, Philipson KD. 1997. Tissue specificity and alternative splicing of the na+/Ca2+ exchanger isoforms NCX1, NCX2, and NCX3 in rat. Am J Physiol 272:C1250-C1261.
78. Raiteri L, Stigliani S, Zedda L, Raiteri M, Bonanno G. 2002. Multiple mechanisms of transmitter release evoked by "pathologically" elevated extracellular [K+]: Involvement of transporter reversal and mitochondrial calcium. J Neurochem 80:706-714.
79. Raiteri L, Zappettini S, Milanese M, Fedele E, Raiteri M, et al. 2007. Mechanisms of glutamate release elicited in rat cerebrocortical nerve endings by "pathologically" elevated extraterminal K+ concentrations. J Neurochem 103:952-961.
80. Reeves JP, Hale CC. 1984. The stoichiometry of the cardiac sodium-calcium exchange system. J Biol Chem 259:7733-7739.
81. Ren X, Philipson KD. 2013. The topology of the cardiac na(+)/ca(2)(+) exchanger, NCX1. J Mol Cell Cardiol 57:68-71.
82. Reyes RC, Verkhratsky A, Parpura V. 2012. Plasmalemmal na+/Ca2+ exchanger modulates Ca2+-dependent exocytotic release of glutamate from rat cortical astrocytes. ASN Neuro 4:.
83. Roberts DE, Matsuda T, Bose R. 2012. Molecular and functional characterization of the human platelet na(+) /ca(2+) exchangers. Br J Pharmacol 165:922-936.
84. Roome CJ, Power EM, Empson RM. 2013. Transient reversal of the sodium/calcium exchanger boosts presynaptic calcium and synaptic transmission at a cerebellar synapse. J Neurophysiol 109:1669-1680.
85. Sahin-Toth M, Nicoll DA, Frank JS, Philipson KD, Friedlander M. 1995. The cleaved N-terminal signal sequence of the cardiac na+-Ca2+ exchanger is not required for functional membrane integration. Biochem Biophys Res Commun 212:968-974.
86. Salamonsen LA, Nie G, Dimitriadis E, Robb L, Findlay JK. 2001. Genes involved in implantation. Reprod Fertil Dev 13:41-49.
87. Schulze DH, Polumuri SK, Gille T, Ruknudin A. 2002. Functional regulation of alternatively spliced na+/Ca2+ exchanger (NCX1) isoforms. Ann NY Acad Sci 976:187-196.
88. Scorziello A, Savoia C, Sisalli MJ, Adornetto A, Secondo A, et al. 2013. NCX3 regulates mitochondrial calcium handling through AKAP121-anchored signaling complex and prevents hypoxia-induced cell death. J. Cell. Sci.
89. Sharma V, He C, Sacca-Schaeffer J, Brzozowski E, Herranz DM, et al. 2013. Insight into the family of na+/Ca2+ exchangers of caenorhabditis elegans. Genetics.
90. Sheng JZ, Prinsen CF, Clark RB, Giles WR, Schnetkamp PP. 2000. Na(+)-ca(2+)-K(+) currents measured in insect cells transfected with the retinal cone or rod na(+)-ca(2+)-K(+) exchanger cDNA. Biophys J 79:1945-1953.
91. Sirabella R, Secondo A, Pannaccione A, Molinaro P, Formisano L, et al. 2012. ERK1/2, p38, and JNK regulate the expression and the activity of the three isoforms of the na+ /Ca2+ exchanger, NCX1, NCX2, and NCX3, in neuronal PC12 cells. J Neurochem 122:911-922.
92. Sirabella R, Secondo A, Pannaccione A, Scorziello A, Valsecchi V, et al. 2009. Anoxia-induced NF-kappaB-dependent upregulation of NCX1 contributes to Ca2+ refilling into endoplasmic reticulum in cortical neurons. Stroke 40:922-929.
93. Sokolow S, Luu SH, Headley AJ, Hanson AY, Kim T, et al. 2011. High levels of synaptosomal na+-Ca2+ exchangers (NCX1, NCX2, NCX3) co-localized with amyloid-beta in human cerebral cortex affected by alzheimer's disease. Cell Calcium 49:208-216.
94. Tang Y, Zucker RS. 1997. Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron 18:483-491.
95. Tritsch E, Mallat Y, Lefebvre F, Diguet N, Escoubet B, et al. 2013. An SRF/miR-1 axis regulates NCX1 and annexin A5 protein levels in the normal and failing heart. Cardiovasc Res 98:372-380.
96. Valsecchi V, Pignataro G, Del Prete A, Sirabella R, Matrone C, et al. 2011. NCX1 is a novel target gene for hypoxia-inducible factor-1 in ischemic brain preconditioning. Stroke 42:754-763.
97. Visser F, Valsecchi V, Annunziato L, Lytton J. 2007. Exchangers NCKX2, NCKX3, and NCKX4: Identification of thr-551 as a key residue in defining the apparent K(+) affinity of NCKX2. J Biol Chem 282:4453-4462.
98. Waight AB, Pedersen BP, Schlessinger A, Bonomi M, Chau BH. et al. 2013. Structural basis for alternating access of a eukaryotic calcium/proton exchanger. Nature 499:107-110.
99. Wang T, Xu H, Oberwinkler J, Gu Y, Hardie RC. et al. 2005. Light activation, adaptation, and cell survival functions of the na+/Ca2+ exchanger CalX. Neuron 45:367-378.
100. Winkfein RJ, Szerencsei RT, Kinjo TG, Kang K, Perizzolo M. et al. 2003. Scanning mutagenesis of the alpha repeats and of the transmembrane acidic residues of the human retinal cone na/ca-K exchanger. Biochemistry 42:543-552.
101. Wu A, Derrico CA, Hatem L, Colvin RA. 1997. Alzheimer's amyloid-beta peptide inhibits sodium/calcium exchange measured in rat and human brain plasma membrane vesicles. Neuroscience 80:675-684.
102. Wu G, Lu ZH, Ledeen RW. 1995. GM1 ganglioside in the nuclear membrane modulates nuclear calcium homeostasis during neurite outgrowth. J Neurochem 65:1419-1422.
103. Xu L, Renaud L, Muller JG, Baicu CF, Bonnema DD, et al. 2006. Regulation of Ncx1 expression. identification of regulatory elements mediating cardiac-specific expression and up-regulation. J Biol Chem 281:34430-34440.
104. Yang H, Kim TH, Lee HH, Choi KC, Jeung EB. 2011 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.
105. Yang H, Yoo Y, Jung E, Choi K, Jeung E. 2010 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.