Na+/Ca2+ exchangers: Three mammalian gene families control Ca2+ transport

Biochemical Journal

Volumn 406, Issue 3, 2007, Pages 365-382

  Lytton, Jonathan ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Calcium transport; Excitation contraction coupling; Melanosome biogenesis; Renal calcium reabsorption; Signal transduction; Sodium calcium exchanger; Synaptic plasticity

Indexed keywords

BRAIN; CELL MEMBRANES; PLASTICITY; SIGNAL TRANSDUCTION; SKIN; SODIUM; TISSUE;

CALCIUM TRANSPORT; EXCITATION-CONTRACTION COUPLING; MELANOSOME BIOGENESIS; RENAL CALCIUM REABSORPTION; SYNAPTIC PLASTICITY;

GENES;

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); SODIUM CALCIUM EXCHANGE PROTEIN; CALCIUM; POTASSIUM; SLC38A3 PROTEIN, HUMAN; SLC8A2 PROTEIN, MOUSE; SODIUM; SODIUM CALCIUM EXCHANGER 1; SODIUM-CALCIUM EXCHANGER 1; UNCLASSIFIED DRUG;

BIOGENESIS; CALCIUM ABSORPTION; CALCIUM TRANSPORT; CATION EXCHANGE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CYTOPLASM; EXCITATION CONTRACTION COUPLING; INTRACELLULAR SPACE; MELANOSOME; MULTIGENE FAMILY; NERVE CELL PLASTICITY; NONHUMAN; PHOTORECEPTOR; PIGMENT EPITHELIUM; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SKIN; SKIN PIGMENTATION; SODIUM CALCIUM EXCHANGE; TISSUE DISTRIBUTION; ANIMAL; BRAIN; CALCIUM SIGNALING; HEART MUSCLE; HUMAN; KIDNEY; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE;

MAMMALIA;

ANIMALS; BRAIN; CALCIUM; CALCIUM SIGNALING; HUMANS; KIDNEY; MULTIGENE FAMILY; MUSCLE, SKELETAL; MYOCARDIUM; POTASSIUM; SODIUM; SODIUM-CALCIUM EXCHANGER;

EID: 34548714102     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070619     Document Type: Review

References (229)

1. Berridge, M. J., Lipp, P. and Bootman, M. D. (2000) The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11-21
2. Berridge, M. J., Bootman, M. D. and Roderick, H. L. (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529
3. 2+ clearance mechanism in axon terminals of rat neurohypophysis. J. Neurosci. 22, 6891-6899
4. 2+ clearance at the calyx of Held. J. Neurosci. 25, 6057-6065
5. Wanaverbecq, N., Marsh, S. J., Al-Qatari, M. and Brown, D. A. (2003) 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
6. 2+ exchanger knockout mice: plasticity of cardiac excitation-contraction coupling. Ann. N.Y. Acad. Sci. 1099, 270-275
7. 2+ exchanger 2. Neuron 38, 965-976
8. 2+-exchanger 2, NCKX2, in motor learning and memory. J. Biol. Chem. 281, 6273-6282
9. Blaustein, M. P. and Lederer, W. J. (1999) Sodium/calcium exchange: its physiological implications. Physiol. Rev. 79, 763-854
10. Nicoll, D. A., Longoni, S. and Philipson, K. D. (1990) Molecular cloning and functional expression or the cardiac Na,Ca-exchanger. Science 250, 562-565
11. Schnetkamp, P. P. M. (1986) Sodium-calcium exchange in the outer segments of bovine rod photoreceptors. J. Physiol. 373, 25-45
12. Cervetto, L., Lagnado, L., Perry, R. J., Robinson, D. W. and McNaughton, P. A. (1989) Extrusion of calcium from rod outer segments is driven by both sodium and potassium gradients. Nature 337, 740-743
13. +. Am. J. Physiol. Cell Physiol. 257, C153-C157
14. Cook, N. J. and Kaupp, U. B. (1988) Solubilization, purification, and reconstitution of the sodium-calcium exchanger from bovine retinal rod outer segments. J. Biol. Chem. 263, 11382-11388
15. Reiländer, H., Achilles, A., Friedel, U., Maul, G., Lottspeich, F. and Cook, N. J. (1992) Primary structure and functional expression of the Na/Ca,K-exchanger from bovine rod photoreceptors. EMBO J. 11, 1689-1695
16. Schwarz, E. M. and Benzer, S. (1997) Calx, a sodium-calcium exchanger gene of Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 94, 10249-10254
17. 2+ exchanger superfamily: phylogenetic analysis and structural implications. Mol. Biol. Evol. 21, 1692-1703
18. Ren, Q., Chen, K. and Paulsen, I. T. (2007) TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels. Nucleic Acids Res. 35, D274-D279
19. Li, Z., Matsuoka, S., Hryshko, L. V., Nicoll, D. A., Bersohn, M. M., Burke, E. P., Lifton, R. P. and Philipson, K. D. (1994) Cloning of the NCX2 isoform of the plasma membrane Na-Ca exchanger. J. Biol. Chem. 269, 17434-17439
20. 2+ exchanger, NCX2. J. Biol. Chem. 271, 24914-24921
21. 2+ exchanger from Mozambique tilapia (Oreochromis mossambicus) reveal a teleost membrane transporter with mammalian temperature dependence. J. Biol. Chem. 280, 28903-28911
22. Tsoi, M., Rhee, K.-H., Bungard, D., Li, X.-F., Lee, S.-L., Auer, R. N. and Lytton, J. (1998) Molecular cloning of a novel potassium-dependent sodium-calcium exchanger from rat brain. J. Biol. Chem. 273, 4155-4162
23. Kraev, A., Quednau, B. D., Leach, S., Li, X. F., Dong, H., Winkfein, R., Perizzolo, M., Cai, X., Yang, R., Philipson, K. D. and Lytton, J. (2001) Molecular cloning of a third member of the potassium-dependent sodium-calcium exchanger gene family, NCKX3. J. Biol. Chem. 276, 23161-23172
24. Li, X. F., Kraev, A. S. and Lytton, J. (2002) Molecular cloning of a fourth member of the potassium-dependent sodium-caicium exchanger gene family, NCKX4. J. Biol. Chem. 277, 48410-48417
25. Lamason, R. L., Mohideen, M. A., Mest, J. R., Wong, A. C., Norton, H. L., Aros, M. C., Jurynec, M. J., Mao, X., Humphreville, V. R., Humbert, J. E. et al. (2005) SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310, 1782-1786
26. 2+ exchanger gene family, NCKX6. J. Biol. Chem. 279, 5867-5876
27. Palty, R., Ohana, E., Hershfinkel, M., Volokita, M., Elgazar, V., Beharier, O., Silverman, W. F., Argaman, M. and Sekler, I. (2004) Lithium-calcium exchange is mediated by a distinct potassium-independent sodium-calcium exchanger. J. Biol. Chem. 279, 25234-25240
28. 2+ exchanger. J. Biol. Chem. 271, 13385-13391
29. 2+ affinity. J. Biol. Chem. 275, 38571-38580
30. 2- exchanger. J. Biol. Chem. 280, 1061-1069
31. Nicoll, D. A., Ren, X., Ottolia, M., Phillips, M., Paredes, A. R., Abramson, J. and Philipson, K. D. (2007) What we know about the structure of NCX1 and how it relates to its function. Ann. N.Y. Acad. Sci. 1099, 1-6
32. Winkfein, R. J., Szerencsei, R. T., Kinjo, T. G., Kang, K., Perizzolo, M., Eisner, L. and Schnetkamp, P. P. (2003) Scanning mutagenesis of the α repeats and of the transmembrane acidic residues of the human retinal cone Na/Ca-K exchanger. Biochemistry 42, 543-552
33. + exchanger. Ann N.Y. Acad. Sci. 1099, 16-28
34. 2+ exchanger. J. Biol. Chem. 274, 910-917
35. 2+ exchanger. J. Biol. Chem. 276, 194-199
36. 2+ exchanger: proximity of transmembrane segments 1, 2, and 6. J. Biol. Chem. 281, 22808-22814
37. + exchanger α-repeats. Ann. N.Y. Acad. Sci. 1099, 34-39
38. Kinjo, T. G., Szerencsei, R. T., Winkfein, R. J., Kang, K. and Schnetkamp, P. P. (2003) Topology of the retinal cone NCKX2 Na/Ca-K exchanger. Biochemistry 42, 2485-2491
39. + exchanger. Biochemistry 44, 7787-7795
40. Rapp, M., Granseth, E., Seppala, S. and von Heijne, G. (2006) Identification and evolution of dual-topology membrane proteins. Nat. Struct. Mol. Biol. 13, 112-116
41. Rapp, M., Seppala, S., Granseth, E. and von Heijne, G. (2007) Emulating membrane protein evolution by rational design. Science 315, 1282-1284
42. Kofuji, P., Hadley, R. W., Kieval, R. S., Lederer, W. J. and Schulze, D. H. (1992) Expression of the Na-Ca exchanger in diverse tissues: a study using the cloned human cardiac Na-Ca exchanger. Am. J. Physiol. Cell Physiol. 263, C1241-C1249
43. Lee, S.-L., Yu, A. S. L. and Lytton, J. (1994) Tissue-specific expression of Na/Ca exchanger isoforms. J. Biol. Chem. 269, 14849-14852
44. Quednau, B. D., Nicoll, D. A. and Philipson, K. D. (2004) The sodium/calcium exchanger family-SLC8. Pflugers Arch. 447, 543-548
45. Kofuji, P., Lederer, W. J. and Schulze, D. H. (1994) Mutually exclusive and cassette exons underlie alternatively spliced isoforms of the Na/Ca exchanger. J. Biol. Chem. 269, 5145-5149
46. Barnes, K. V., Cheng, G., Dawson, M. M. and Menick, D. R. (1997) Cloning of cardiac, kidney, and brain promoters of the feline ncx1 gene. J. Biol. Chem 272, 11510-11517
47. 2+ exchanger gene. Am. J. Physiol. Heart Circ. Physiol. 274, H217-H232
48. 2+ exchanger isoforms NCX1, NCX2, and NCX3 in rat. Am. J. Physiol. Cell Physiol. 272, C1250-C1261
49. 2+ exchanger transcripts and proteins in rat brain regions. J. Comp. Neurol. 461, 31-48
50. Durkin, J. T., Ahrens, D. C., Pan, Y. C. E. and Reeves, J. P. (1991) Purification and amino-terminal sequence of the bovine cardiac sodium-calcium exchanger: evidence for the presence of a signal sequence. Arch. Biochem. Biophys. 290, 369-375
51. 2+ exchanger gene (RBE-1) is not mandatory for functional expression. J. Biol. Chem. 270, 19120-19127
52. Loo, T. W., Ho, C. and Clarke, D. M. (1995) Expression of a functionally active human renal sodium-calcium exchanger lacking a signal sequence. J. Biol. Chem. 270, 19345-19350
53. 2+ exchanger is not required for functional membrane integration. Biochem. Biophys. Res. Commun. 212, 968-974
54. 2+ exchanger. Biochim. Biophys. Acta 1151, 35-42
55. 2+ exchanger. Biochim. Biophys. Acta 1371, 40-52
56. Secondo, A., Staiano, R. I., Scorziello, A., Sirabella, R., Boscia, F., Adornetto, A., Valsecchi, V., Molinaro, P., Canzoniero, L. M., Di Renzo, G. and Annunziato, L. (2007) BHK cells transfected with NCX3 are more resistant to hypoxia followed by reoxygenation than those transfected with NCX1 and NCX2: possible relationship with mitochondrial membrane potential, Cell Calcium, doi:10.1016/j.ceca.2007.01.006
57. Huang, Y., Lemieux, M. J., Song, J., Auer, M. and Wang, D. N. (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301, 616-620
58. Li, Z., Nicoll, D. A., Collins, A., Hilgemann, D. W., Filoteo, A. G., Penniston, J. T., Weiss, J. N., Tomich, J. M. and Philipson, K. D. (1991) Identification of a peptide inhibitor of the cardiac sarcolemmal Na,Ca-exchanger. J. Biol. Chem. 266, 1014-1020
59. 2+ sensors. Mol. Cell 22, 15-25
60. 2+ binding motif. J. Biol. Chem. 281, 21577-21581
61. 2+ exchanger (NCX1, NCX2, NCX3). Am J. Physiol. Cell Physiol. 274, C415-C423
62. Reeves, J. P. and Sutko, J. L. (1980) Sodium-calcium exchange activity generates a current in cardiac membrane vesicles. Science 208, 1461-1464
63. Kimura, J., Miyamae, S. and Noma, A. (1987) Identification of sodium-calcium exchange current in single ventricular cells of guinea-pig. J. Physiol. 384, 199-222
64. 2+ exchange in inside-out patches excised from guinea-pig ventricular myocytes. J. Physiol. 523, 339-351
65. 2+ exchanger NCX1.1 measured in transfected HEK cells. Biophys. J. 82, 1943-1952
66. 2+ exchanger. Nature 427, 544-548
67. Reeves, J. P. and Sutko, J. L. (1983) Competitive interactions of sodium and calcium with the sodium-calcium exchange system of cardiac sarcolemmal vesicles. J. Biol. Chem. 258, 3178-3182
68. Bers, D. M. (2002) Cardiac excitation-contraction coupling. Nature 415, 198-205
69. Lederer, W. J., Niggli, E. and Hadley, R. W. (1990) Sodium-calcium exchange in excitable cells: fuzzy space. Science 248, 283
70. Lencesova, L., O'Neill, A., Resneck, W. G., Bloch, R. J. and Blaustein, M. P. (2004) Plasma membrane-cytoskeleton-endoplasmic reticulum complexes in neurons and astrocytes. J. Biol. Chem. 279, 2885-2893
71. Schulze, D. H., Muqhal, M., Lederer, W. J. and Ruknudin, A. M. (2003) Sodium/calcium exchanger (NCX1) macromolecular complex. J. Biol. Chem. 278, 28849-28855
72. Mohler, P. J., Splawski, I., Napolitano, C., Bottelli, G., Sharpe, L., Timothy, K., Priori, S. G., Keating, M. T. and Bennett, V. (2004) A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. Proc. Natl. Acad. Sci. U.S.A. 101, 9137-9142
73. 2+ exchange current density in cardiac myocytes from rabbits and guinea pigs during postnatal development. Am. J. Physiol. 268, H1714-H1722
74. Boerth, S. R., Zimmer, D. B. and Artman, M. (1994) Steady-state mRNA levels of the sarcolemmal Na-Ca exchanger peak near birth in developing rabbit and rat hearts. Circ. Res. 74, 354-359
75. 2+ exchange protein in developing rabbit myocytes. Am. J. Physiol. Cell Physiol. 268, C1126-C1132
76. 2+ exchange activity in neonatal rabbit ventricular myocytes. Am. J. Physiol. Cell Physiol. 288, C195-C203
77. Tibbits, G. F., Xu, L. and Sedarat, F. (2002) Ontogeny of excitation-contraction coupling in the mammalian heart. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 132, 691-698
78. Kent, R. L., Rozich, J. D., McCollam, P. L., McDermott, D. E., Thacher, U. F., Menich, D. R., McDermott, P. J. and Cooper IV, G. (1993) Rapid expression of the Na,Ca-exchanger in response to cardiac pressure overload. Am. J. Physiol. 263, H1024-H1029
79. Studer, R., Reinecke, H., Bilger, J., Eschenhagen, T., Bonm, M., Hasenfuss, G., Just, H., Holtz, J. and Drexler, H. (1994) Gene expression of the cardiac Na-Ca exchanger in end-stage human heart failure. Circ. Res. 75, 443-453
80. Menick, D. R., Renaud, L., Buchholz, A., Muller, J. G., Zhou, H., Kappler, C. S., Kubalak, S. W., Conway, S. J. and Xu, L. (2007) Regulation of Ncx1 gene expression in the normal and hypertrophic heart. Ann. N.Y. Acad. Sci. 1099, 195-203
81. Xu, L., Renaud, L., Muller, J. G., Baicu, C. F., Bonnema, D. D., Zhou, H., Kappler, C. S., Kubalak, S. W., Zile, M. R., Conway, S. J. and Menick, D. R. (2006) Regulation of Ncx1 expression: identification of regulatory elements mediating cardiac-specific expression and up-regulation. J. Biol. Chem. 281, 34430-34440
82. 2+ exchanger isoforms in developing cerebellar neurons. J. Biol. Chem. 275, 20903-20910
83. 2+ homeostasis and viability in cerebellar neurons. J. Neurosci. 25, 10822-10830
84. Blaustein, M. P., DiPolo, R. and Reeves, J. P. (eds) (1991) Sodium-Calcium Exchange: Proceedings of the Second International Conference. Ann. N.Y. Acad. Sci. 639, 1-671
85. Matsuoka, S. and Hilgemann, D. W. (1992) Steady-state and dynamic properties of cardiac sodium-calcium exchange: ion and voltage dependencies of the transport cycle. J. Gen. Physiol. 100, 963-1001
86. DiPolo, R. and Beauge, L. (2006) Sodium/calcium exchanger: influence of metabolic regulation on ion carrier interactions. Physiol. Rev. 86, 155-203
87. DiPolo, R. (1979) Calcium influx in internally dialyzed squid giant axons. J. Gen. Physiol. 73, 91-113
88. Hilgemann, D. W. (1989) Giant excised cardiac sarcolemmal membrane patches: sodium and sodium-calcium exchange currents. Pflugers Arch. 415, 247-249
89. 2+ exchange in giant excised sarcolemmal membrane patches. Nature 344, 242-245
90. Chernysh, O., Condrescu, M. and Reeves, J. P. (2004) Calcium-dependent regulation of calcium efflux by the cardiac sodium/calcium exchanger. Am. J. Physiol. Cell Physiol. 287, C797-C806
91. 2+ exchanger detected by FRET. Biophys. J. 87, 899-906
92. Levitsky, D. O., Nicoll, D. A. and Philipson, K. D. (1994) Identification of the high affinity Ca-binding domain of the cardiac Na-Ca exchanger. J. Biol. Chem. 269, 22847-22852
93. 2+-binding domain. J. Gen. Physiol. 105, 403-420
94. 2+. J. Gen. Physiol. 108, 67-74
95. 2+ exchanger from Drosophila: mutagenesis of ionic regulatory sites. J. Biol. Chem. 273, 12981-12987
96. Hilgemann, D. W., Matsuoka, S., Nagel, G. A. and Collins, A. (1992) Steady-state and dynamic properties of cardiac sodium-calcium exchange: sodium-dependent inactivation. J. Gen. Physiol. 100, 905-932
97. 2+ exchanger by the endogenous XIP region. J. Gen. Physiol. 109, 273-286
98. Hilgemann, D. W., Collins, A. and Matsuoka, S. (1992) Steady-state and dynamic properties of cardiac sodium-calcium exchange: secondary modulation by cytoplasmic calcium and ATP. J. Gen. Physiol. 100, 933-961
99. 2. Science 273, 956-959
100. 2 with the XIP region of the cardiac Na/Ca exchanger. Am. J. Physiol. Cell Physiol. 278, C661-C666
101. 2+ exchanger to α-linolenic acid. Cardiovasc. Res. 73, 395-403
102. Condrescu, M. and Reeves, J. P. (2001) Inhibition of sodium-calcium exchange by ceramide and sphingosine. J. Biol. Chem. 276, 4046-4054
103. 2+ exchange activity of cardiac sarcolemma in reconstituted vesicles. Biochim. Biophys. Acta 937, 258-268
104. 2+ exchange currents in HEK293t cells. Biochem. Biophys. Res. Commun. 321, 116-123
105. Riedel, M. J., Baczko, I., Searle, G. J., Webster, N., Fercho, M., Jones, L., Lang, J., Lytton, J., Dyck, J. R. and Light, P. E. (2006) Metabolic regulation of sodium-calcium exchange by intracellular acyl CoAs. EMBO J. 25, 4605-4614
106. 2+ exchanger in the guinea-pig. J. Physiol. 480, 9-20
107. 2+ exchanger. J. Gen. Physiol. 114, 701-711
108. 2+ exchanger (NCX1) isoforms. J. Biol. Chem. 277, 33957-33962
109. Reeves, J. P., Condrescu, M., Urbanczyk, J. and Chernysh, O. (2007) New modes of exchanger regulation: physiological implications. Ann. N.Y. Acad. Sci. 1099, 64-77
110. Frank, J. S., Mottino, G., Reid, D., Molday, R. S. and Philipson, K. D. (1992) Distribution of the Na-Ca exchange protein in mammalian cardiac myocytes: an immunofluorescence and immunocolloidal gold-labeling study. J. Cell Biol. 117, 337-345
111. + pump and sarcoplasmic reticulum in smooth muscle. Nature 365, 657-660
112. 2+ exchanger in rabbit kidney. Am. J. Physiol. Renal Physiol. 265, F327-F332
113. 2+ exchanger binds to the cytoskeletal protein ankyrin. J. Biol. Chem. 268, 11489-11491
114. 3 receptor in a cardiac T-tubule/SR microdomain. PLoS Biol. 3, e423
115. Cunha, S. R., Bhasin, N. and Mohler, P. J. (2007) Targeting and stability of Na/Ca exchanger 1 in cardiomyocytes reguires direct interaction with the membrane adaptor ankyrin-B. J. Biol. Chem. 282, 4875-4883
116. Condrescu, M., Gardner, J. P., Chernaya, G., Aceto, J. F., Kroupis, C. and Reeves, J. P. (1995) ATP-dependent regulation of sodium-calcium exchange in Chinese hamster ovary cells transfected with the bovine cardiac sodium-calcium exchanger. J. Biol. Chem. 270, 9137-9146
117. 2+ exchanger. Am. J. Physiol. Cell Physiol. 290, C691-C701
118. Razani, B., Woodman, S. E. and Lisanti, M. P. (2002) Caveolae: from cell biology to animal physiology. Pharmacol. Rev. 54, 431-467
119. Williams, T. M. and Lisanti, M. P. (2004) The caveolin genes: from cell biology to medicine. Ann. Med. 36, 584-595
120. 2+-dependent signal transduction. Traffic 4, 717-723
121. Gratton, J. P., Bernatchez, P. and Sessa, W. C. (2004) Caveolae and caveolins in the cardiovascular system. Circ. Res. 94, 1408-1417
122. Woodman, S. E., Park, D. S., Cohen, A. W., Cheung, M. W., Chandra, M., Shirani, J., Tang, B., Jelicks, L. A., Kitsis, R. N., Christ, G. J. et al. (2002) Caveolin-3 knock-out mice develop a progressive cardiomyopathy and show hyperactivation of the p42/44 MAPK cascade. J. Biol. Chem. 277, 38988-38997
123. Scriven, D. R., Klimek, A., Asghari, P., Bellve, K. and Moore, E. D. (2005) Caveolin-3 is adjacent to a group of extradyadic ryanodine receptors. Biophys. J. 89, 1893-1901
124. Bossuyt, J., Taylor, B. E., James-Kracke, M. and Hale, C. C. (2002) Evidence for cardiac sodium-calcium exchanger association with caveolin-3. FEBS Lett. 511, 113-117
125. 2+ exchanger and caveolin-3 in non-failing and failing human heart. J. Mol. Cell. Cardiol. 40, 47-55
126. Cavalli, A., Eghbali, M., Minosyan, T. Y., Stefani, E. and Philipson, K. D. (2007) Localization of sarcolemmal proteins to lipid rafts in the myocardium, Cell Calcium 42, 313-322
127. 2+ exchanger 1 association with caveolin-1 and -2 in C6 glioma cells. IUBMB Life 56, 621-627
128. 2+ exchanger by phospholemman. Ann N.Y. Acad. Sci. 1099, 119-134
129. Garty, H. and Karlish, S. J. (2006) Role of FXYD proteins in ion transport. Annu. Rev. Physiol. 68, 431-459
130. 2+ exchange in adult rat cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 288, H2342-H2354
131. 2+ exchanger. J. Biol. Chem. 281, 32004-32014
132. 2+ exchanger: role of phosphorylation. J. Biol. Chem. 281, 7784-7792
133. 2+ exchange. Am. J. Physiol. Heart Circ. Physiol. 291, H2199-H2209
134. Crambert, G., Fuzesi, M., Garty, H., Karlish, S. and Geering, K. (2002) Phospholemman (FXYD1) associates with Na,K-ATPase and regulates its transport properties. Proc. Natl. Acad. Sci. U.S.A. 99, 11476-11481
135. 2+ exchange in phenylephrine-treated hypertrophic cardiomyocytes. J. Biol. Chem. 280, 5764-5772
136. 2+ exchangers with the 14-3-3 proteins. J. Biol. Chem. 281, 19645-19654
137. Bridges, D. and Moorhead, G. B. (2005) 14-3-3 proteins: a number of functions for a numbered protein. Science STKE 2005, re10
138. 2+ exchange current recorded from guinea-pig ventricular myocytes. Cell Calcium 29, 347-358
139. Perchenet, L., Hinde, A. K., Patel, K. C., Hancox, J. C. and Levi, A. J. (2000) Stimulation of Na/Ca exchange by the β-adrenergic/protein kinase A pathway in guinea-pig ventricular myocytes at 37°C. Pflügers Arch. 439, 822-828
140. 2+ exchanger in failing pig myocytes. Circ. Res. 92, 897-903
141. 2+ exchanger NCX1 expressed in Xenopus oocytes. J. Physiol. 529, 599-610
142. Ginsburg, K. S. and Bers, D. M. (2005) Isoproterenol does not enhance Ca-dependent Na/Ca exchange current in intact rabbit ventricular myocytes. J. Mol. Cell. Cardiol. 39, 972-981
143. 2+ exchange current in guinea pig, mouse, and rat ventricular myocytes. Am. J. Physiol. Cell Physiol. 290, C601-C608
144. 2- exchange current in guinea pig, mouse, and rat ventricular myocytes". Am. J Physiol. Cell Physiol. 290, C1271
145. 2+ exchanger via protein kinase C. J. Biol. Chem. 271, 13609-13615
146. 2+ exchanger isoforms NCX1 and NCX3 does not require their direct phosphorylation. Biochemistry 37, 17230-17238
147. 2+ exchange as a drug target: insights from molecular pharmacology and genetic engineering. Ann. N.Y. Acad. Sci. 1099, 516-528
148. 2+ exchanger is essential for embryonic heart development in mice. Mol. Cells 10, 712-722
149. 2+ exchanger gene leads to cardiomyocyte apoptosis and defects in heartbeat. J. Biol. Chem. 275, 36991-36998
150. Koushik, S. V., Wang, J., Rogers, R., Moskophidis, D., Lambert, N. A., Creazzo, T. L. and Conway, S. J. (2001) Targeted inactivation of the sodium-calcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization. FASEB J. 15, 1209-1211
151. Reuter, H., Henderson, S. A., Han, T., Ross, R. S., Goldhaber, J. I. and
152. 2+ exchanger (NCX1) knock-out mouse by transgenic expression of NCX1. Exp. Mol. Med. 35, 125-135
153. 2+ exchange: cardiac-specific knockout of NCX1. Circ. Res. 95, 604-611
154. +-Ca2+ exchanger. Biophys. J. 92, 1431-1437
155. 2+ exchanger knockout mice. Am. J. Physiol. Cell Physiol. 292, C968-C973
156. 2+ exchange in the regulation of cardiac excitation-contraction coupling. Cardiovasc. Res. 67, 198-207
157. 2+ release in mouse heart. Biophys. J. 92, 624-628
158. Reuter, H. and Porzig, H. (1995) Localization and functional significance of the Na/Ca exchanger in presynaptic boutons of hippocampal cells in culture. Neuron 15, 1077-1084
159. 2+ exchanger protein isoforms, NCX1, NCX2, and NCX3 in cerebral cortex and hippocampus of adult rat. Cell Calcium 41, 221-234
160. 2+ exchanger in excitotoxicity. Cell 120, 275-285
161. Lorincz, A., Rozsa, B., Katona, G., Vizi, E. S. and Tamas, G. (2007) Differential distribution of NCX1 contributes to spine-dendrite compartmentalization in CA1 pyramidal cells. Proc. Natl. Acad. Sci. U.S.A. 104, 1033-1038
162. Burdakov, D., Liss, B. and Ashcroft, F. M. (2003) Orexin excites GABAergic neurons of the arcuate nucleus by activating the sodium-calcium exchanger. J. Neurosci. 23, 4951-4957
163. Eriksson, K. S., Sergeeva, O. A., Stevens, D. R. and Haas, H. L. (2002) Neurotransmitter-induced activation of sodium-calcium exchange causes neuronal excitation. Ann. N.Y. Acad. Sci. 976, 405-407
164. 2+- exchange. Neuropharmacology 40, 345-351
165. 2+ concentration increases in cultured rat forebrain neurons. Mol. Pharmacol. 53, 742-749
166. Sergeeva, O. A., Amberger, B. T., Vorobjev, V. S., Eriksson, K. S. and Haas, H. L. (2004) AMPA receptor properties and coexpression with sodium-calcium exchangers in rat hypothalamic neurons. Eur. J. Neurosci. 19, 957-965
167. 2+ exchanger and tissue-specific expression of isoforms. J. Biochem. (Tokyo) 114, 528-534
168. 2+ and contractility in arterial smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 291, H1226-H1235
169. 2+ mobilization. Am. J. Physiol. Lung Cell. Mol. Physiol. 292, L438-L447
170. 2+ entry via NCX reversal in ATP stimulated smooth muscle cells. Biochem. Biophys. Res. Commun. 352, 130-134
171. Hoenderop, J. G., Nilius, B. and Bindels, R. J. (2005) Calcium absorption across epithelia. Physiol. Rev. 85, 373-422
172. Augustine, G. J., Santamaria, F. and Tanaka, K. (2003) Local calcium signaling in neurons. Neuron 40, 331-346
173. Malenka, R. C. and Bear, M. F. (2004) LTP and LTD: an embarrassment of riches. Neuron 44, 5-21
174. Sokolow, S., Manto, M., Gailly, P., Molgo, J., Vandebrouck, C., Vanderwinden, J. M., Herchuelz, A. and Schurmans, S. (2004) Impaired neuromuscular transmission and skeletal muscle fiber necrosis in mice lacking Na/Ca exchanger 3. J. Clin. Invest. 113, 265-273
175. Sipido, K. R., Bito, V., Antoons, G., Volders, P. G. and Vos, M. A. (2007) Na/Ca exchange and cardiac ventricular arrhythmias. Ann. N.Y. Acad. Sci. 1099, 339-348
176. Venetucci, L. A., Trafford, A. W., O'Neill, S. C. and Eisner, D. A. (2007) Na/Ca exchange: regulator of intracellular calcium and source of arrhythmias in the heart. Ann. N.Y. Acad. Sci. 1099, 315-325
177. Venetucci, L. A., Trafford, A. W. and Eisner, D. A. (2007) Increasing ryanodine receptor open probability alone does not produce arrhythmogenic calcium waves: threshold sarcoplasmic reticulum calcium content is required. Circ. Res. 100, 105-111
178. Sipido, K. R., Volders, P. G., Vos, M. A. and Verdonck, F. (2002) Altered Na/Ca exchange activity in cardiac hypertrophy and heart failure: a new target for therapy? Cardiovasc. Res, 53, 782-805
179. Sipido, K. R. (2006) Calcium overload, spontaneous calcium release, and ventricular arrhythmias. Heart Rhythm 3, 977-979
180. Hobai, I. A., Maack, C. and O'Rourke, B. (2004) Partial inhibition of sodium/calcium exchange restores cellular calcium handling in canine heart failure. Circ. Res. 95, 292-299
181. Murphy, E., Cross, H. and Steenbergen, C. (1999) Sodium regulation during ischemia versus reperfusion and its role in injury. Circ. Res. 84, 1469-1470
182. Lipton, P. (1999) Ischemic cell death in brain neurons. Physiol. Rev. 79, 1431-1568
183. Stys, P. K. (2005) General mechanisms of axonal damage and its prevention. J. Neurol. Sci. 233, 3-13
184. +. Mol. Pharmacol. 56, 619-632
185. 2+ exchange in spinal cord white matter injury at physiological temperature. J. Neurophysiol. 84, 1116-1119
186. Kiedrowski, L. (2007) NCX and NCKX operation in ischemic neurons. Ann. N.Y. Acad. Sci. 1099, 383-395
187. Pignataro, G., Gala, R., Cuomo, O., Tortiglione, A., Giaccio, L., Castaldo, P., Sirabella, R., Matrone, C., Canitano, A., Amoroso, S. et al. (2004) Two sodium/calcium exchanger gene products, NCX1 and NCX3, play a major role in the development of permanent focal cerebral ischemia. Stroke 35, 2566-2570
188. 2+ exchanger in cerebral ischemia induced by middle cerebral artery occlusion in male rats. Neuropharmacology 46, 439-448
189. Annunziato, L., Pignataro, G., Boscia, F., Sirabella, R., Formisano, L., Saggese, M., Cuomo, O., Gala, R., Secondo, A., Viggiano, D. et al. (2007) ncx1 ncx2, and ncx3 gene product expression and function in neuronal anoxia and brain ischemia. Ann. N.Y. Acad. Sci. 1099, 413-426
190. 2+ exchanger type-1 in vascular smooth muscle. Nat. Med. 10, 1193-1199
191. 2+ exchange inhibitors in attenuating ischemia-reperfusion injury. Can. J. Cardiol. 21, 509-516
192. Noble, D. and Blaustein, M. P. (2007) Directionality in drug action on sodium-calcium exchange. Ann. N.Y. Acad. Sci. 1099, 540-543
193. Schnetkamp, P. P. M. (1995) Calcium homeostasis in vertebrate retinal rod outer segments. Cell Calcium 18, 322-330
194. 2+ exchanger in human platelets. Am. J. Physiol. Heart Physiol. 277, H911-H917
195. 2+ exchangers in the brain. Ann. N.Y. Acad. Sci. 976, 382-393
196. Poon, S., Leach, S., Li, X. F., Tucker, J. E., Schnetkamp, P. P. M. and Lytton, J. (2000) Alternatively spliced isoforms of the rat eye sodium/calcium+potassium exchanger NCKX1. Am. J. Physiol. Cell Physiol. 278, C651-C660
197. Prinsen, C. F., Szerencsei, R. T. and Schnetkamp, P. P. M. (2000) Molecular cloning and functional expression of the potassium-dependent sodium-calcium exchanger from human and chicken retinal cone photoreceptors. J. Neurosci. 20, 1424-1434
198. 2+ exchanger in intact retinal cone photoreceptors. J. Gen. Physiol. 129, 1-16
199. Sharon, D., Yamamoto, H., McGee, T. L., Rabe, V., Szerencsei, R. T., Winkfein, R. J., Prinsen, C. F., Barnes, C. S., Andreasson, S., Fishman, G. A. et al. (2002) Mutated alleles of the rod and cone Na-Ca+K-exchanger genes in patients with retinal diseases. Invest. Ophthalmol. Visual Sci. 43, 1971-1979
200. + exchangers. Biochemistry 42, 9438-9445
201. 2+ exchanger, NCKX2. J. Biol. Chem. 277, 48923-48930
202. + exchanger. J. Biol. Chem. 280, 6823-6833
203. +. J. Biol. Chem. 280, 6834-6839
204. + affinity of NCKX2. J. Biol. Chem. 282, 4453-4462
205. +-binding site. Ann. N.Y. Acad. Sci. 1099, 166-170
206. + exchanger family: vision and beyond. Pflügers Arch. 447, 683-688
207. Kaupp, U. B. and Seifert, R. (2002) Cyclic nucleotide-gated ion channels. Physiol. Rev. 82, 769-824
208. Schwarzer, A., Schauf, H. and Bauer, P. J. (2000) Binding of the cGMP-gated channel to the Na/Ca-K exchanger in rod photoreceptors. J. Biol. Chem. 275, 13448-13454
209. + exchanger oligomers with cGMP-gated channel subunits as probed with heterologously expressed cDNAs. Biochemistry 42, 4593-4600
210. Yoo, S. S., Leach, S. and Lytton, J. (2002) Studies on the oligomeric state of the sodium/calcium+potassium exchanger NCKX2. Ann. N.Y. Acad. Sci. 976, 94-96
211. + exchanger NCKX2. J. Biol. Chem. 282, 3720-3729
212. Lee, J. Y., Visser, F., Lee, J. S., Lee, K. H., Soh, J. W., Ho, W. K., Lytton, J. and Lee, S. H. (2006) Protein kinase C-dependent enhancement of activity of rat brain NCKX2 heterologously expressed in HEK293 cells. J. Biol. Chem. 281, 39205-39216
213. Lan, J. Y., Skeberdis, V. A., Jover, T., Grooms, S. Y., Lin, Y., Araneda, R. C., Zheng, X., Bennett, M. V. and Zukin, R. S. (2001) Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci. 4, 382-390
214. 2+ sensor for vesicle fusion. Nature 435, 497-501
215. Fain, G. L., Matthews, H. R., Cornwall, M. C. and Koutalos, Y. (2001) Adaptation in vertebrate photoreceptors. Physiol. Rev. 81, 117-151
216. 2+ exchangers in the rat supraoptic magnocellular neuron is polarized to axon terminals. J. Neurosci. 23, 11673-11680
217. 2+ exchangers in hippocampal CA1 neurons. NeuroReport 15, 2113-2116
218. Chi, A., Valencia, J. C., Hu, Z. Z., Watabe, H., Yamaguchi, H., Mangini, N. J., Huang, H., Canfield, V. A., Cheng, K. C., Yang, F. et al. (2006) Proteomic and bioinformatic characterization of the biogenesis and function of melanosomes. J. Proteome Res. 5, 3135-3144
219. Pyrski, M., Koo, J. H., Polumuri, S. K., Ruknudin, A. M., Margolis, J. W., Schulze, D. H. and Margolis, F. L. (2007) Sodium/calcium exchanger expression in the mouse and rat olfactory systems. J. Comp. Neurol. 501, 944-958
220. 2+ exchange in type I vestibular sensory cells of guinea-pig. Eur. J. Neurosci. 11, 1955-1959
221. 2+ low in sea urchin spermatozoa. Proc. Natl. Acad. Sci. U.S.A. 99, 6743-6748
222. Hansen, A. J. and Zeuthen, T. (1981) Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. Acta Physiol. Scand. 113, 437-445
223. Kiedrowski, L., Czyz, A., Baranauskas, G., Li, X. F. and Lytton, J. (2004) Differential contribution of plasmalemmal Na/Ca exchange isoforms to sodium-dependent calcium influx and NMDA excitotoxicity in depolarized neurons. J. Neurochem. 90, 117-128
224. Cuomo, O., Pignataro, G., Gala, R., Boscia, F., Tortiglione, A., Molinaro, P., Di Renzo, G., Lytton, J. and Annunziato, L. (2007) Involvement of the potassium-dependent sodium/calcium exchanger gene product NCKX2 in the brain insult induced by permanent focal cerebral ischemia. Ann. N.Y. Acad. Sci. 1099, 486-489
225. 2+ exchanger isoform lacking the six C-terminal transmembrane segments. Eur. J. Biochem. 239, 897-904
226. Li, X. F. and Lytton, J. (1999) A circularized sodium-calcium exchanger exon 2 transcript. J. Biol. Chem. 274, 8153-8160
227. 2+ exchanger, NCLX, oligomerize to form a functional exchanger. Biochemistry 45, 11856-11866
228. 2+ exchanger-related Escherichia coli protein YrbG have opposite membrane topologies. J. Biol. Chem. 276, 18905-18907
229. 2+-ATPase in Cell Function: Fifth International Conference. Ann. N.Y. Acad. Sci. 1099, xv-547