Enhanced Ca2+ entry and Na+/Ca2+ exchanger activity in dendritic cells from AMP-activated protein kinase-deficient mice

FASEB Journal

Volumn 26, Issue 7, 2012, Pages 3049-3058

  Nurbaeva, Meerim K ^a   Schmid, Evi ^a   Szteyn, Kalina ^a   Yang, Wenting ^a   Viollet, Benoit ^b   Shumilina, Ekaterina ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b INSERM   (France)

Author keywords

AMPK; CRAC; Energy depletion; Migration; NCX; NKCX; Store operated calcium channel

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; FURA 2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOCHONDRIAL PROTEIN; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM CALCIUM EXCHANGE PROTEIN; STROMAL CELL DERIVED FACTOR 1; STROMAL INTERACTION MOLECULE 1; STROMAL INTERACTION MOLECULE 2; THAPSIGARGIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; FLUORESCENCE; MOUSE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING; WHOLE CELL; WILD TYPE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BASE SEQUENCE; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL MOVEMENT; CHEMOKINE CXCL12; DENDRITIC CELLS; DNA PRIMERS; MICE; MICE, KNOCKOUT; SODIUM-CALCIUM EXCHANGER;

MUS;

EID: 84863211075     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-204024     Document Type: Article

References (100)

1. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y. J., Pulendran, B., and Palucka, K. (2000) Immunobiology of dendritic cells. Annu. Rev. Immunol. 18, 767-811
2. den Haan, J. M., and Bevan, M. J. (2000) A novel helper role for CD4 T cells. Proc. Natl. Acad. Sci. U. S. A. 97, 12950-12952
3. Steinman, R. M., and Nussenzweig, M. C. (2002) Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. U. S. A. 99, 351-358 (Pubitemid 34060366)
4. Yamazaki, S., and Steinman, R. M. (2009) Dendritic cells as controllers of antigen-specific Foxp3(+) regulatory T cells. J. Dermatol. Sci. 54, 69-75
5. Connolly, S. F., and Kusner, D. J. (2007) The regulation of dendritic cell function by calcium-signaling and its inhibition by microbial pathogens. Immunol. Res. 39, 115-127 (Pubitemid 47574879)
6. Shumilina, E., Huber, S. M., and Lang, F. (2011) Ca2+signaling in the regulation of dendritic cell functions. Am. J. Physiol. Cell Physiol. 300, C1205-C1214
7. Salter, R. D., and Watkins, S. C. (2009) Dendritic cell altered states: what role for calcium? Immunol. Rev. 231, 278-288
8. Barbet, G., Demion, M., Moura, I. C., Serafini, N., Leger, T., Vrtovsnik, F., Monteiro, R. C., Guinamard, R., Kinet, J. P., and Launay, P. (2008) The calcium-activated nonselective cation channel TRPM4 is essential for the migration but not the maturation of dendritic cells. Nat. Immunol. 9, 1148-1156
9. Hsu, S., O'Connell, P. J., Klyachko, V. A., Badminton, M. N., Thomson, A. W., Jackson, M. B., Clapham, D. E., and Ahern, G. P. (2001) Fundamental Ca2+ signaling mechanisms in mouse dendritic cells: CRAC is the major Ca2+ entry pathway. J. Immunol. 166, 6126-6133 (Pubitemid 32440741)
10. Parekh, A. B., and Putney, J. W., Jr. (2005) Store-operated calcium channels. Physiol. Rev. 85, 757-810 (Pubitemid 40404641)
11. Prakriya, M., Feske, S., Gwack, Y., Srikanth, S., Rao, A., and Hogan, P. G. (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443, 230-233 (Pubitemid 44387613)
12. Putney, J. W., Jr. (2007) New molecular players in capacitative Ca2+ entry. J. Cell Sci. 120, 1959-1965
13. Vig, M., Peinelt, C., Beck, A., Koomoa, D. L., Rabah, D., Koblan-Huberson, M., Kraft, S., Turner, H., Fleig, A., Penner, R., and Kinet, J. P. (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312, 1220-1223 (Pubitemid 43801149)
14. Fahrner, M., Muik, M., Derler, I., Schindl, R., Fritsch, R., Frischauf, I., and Romanin, C. (2009) Mechanistic view on domains mediating STIM1-Orai coupling. Immunol. Rev. 231, 99-112
15. Peinelt, C., Vig, M., Koomoa, D. L., Beck, A., Nadler, M. J., Koblan-Huberson, M., Lis, A., Fleig, A., Penner, R., and Kinet, J. P. (2006) Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat. Cell Biol. 8, 771-773
16. Penna, A., Demuro, A., Yeromin, A. V., Zhang, S. L., Safrina, O., Parker, I., and Cahalan, M. D. (2008) The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers. Nature 456, 116-120
17. Smyth, J. T., Hwang, S. Y., Tomita, T., DeHaven, W. I., Mercer, J. C., and Putney, J. W. (2010) Activation and regulation of store-operated calcium entry. J. Cell. Mol. Med. 14, 2337-2349
18. Zhang, S. L., Yu, Y., Roos, J., Kozak, J. A., Deerinck, T. J., Ellisman, M. H., Stauderman, K. A., and Cahalan, M. D. (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437, 902-905 (Pubitemid 41486767)
19. Feske, S. (2007) Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol. 7, 690-702
20. Gwack, Y., Sharma, S., Nardone, J., Tanasa, B., Iuga, A., Srikanth, S., Okamura, H., Bolton, D., Feske, S., Hogan, P. G., and Rao, A. (2006) A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 441, 646-650 (Pubitemid 43927297)
21. Peel, S. E., Liu, B., and Hall, I. P. (2008) ORAI and store-operated calcium influx in human airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 38, 744-749 (Pubitemid 351841577)
22. Shin, D. M., and Muallem, S. (2008) Skeletal muscle dressed in SOCs. Nat. Cell Biol. 10, 639-641 (Pubitemid 351772929)
23. Bandyopadhyay, B. C., Pingle, S. C., and Ahern, G. P. (2011) Store-operated Ca(2)+ signaling in dendritic cells occurs independently of STIM1. J. Leukoc. Biol. 89, 57-62
24. 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 (Pubitemid 36773404)
25. Berridge, M. J. (2006) Calcium microdomains: organization and function. Cell Calcium 40, 405-412
26. Clapham, D. E. (2007) Calcium signaling. Cell 131, 1047-1058
27. Visser, F., and Lytton, J. (2007) K+-dependent Na+/Ca2+exchangers: key contributors to Ca2+ signaling. Physiology (Bethesda) 22, 185-192
28. Visser, F., Valsecchi, V., Annunziato, L., and 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
29. Blaustein, M. P., and Lederer, W. J. (1999) Sodium/calcium exchange: its physiological implications. Physiol. Rev. 79, 763-854 (Pubitemid 29330173)
30. Lytton, J. (2007) Na+/Ca2+ exchangers: three mammalian gene families control Ca2+ transport. Biochem. J. 406, 365-382
31. Herchuelz, A., Kamagate, A., Ximenes, H., and Van Eylen, F. (2007) Role of Na/Ca exchange and the plasma membrane Ca2+-ATPase in beta cell function and death. Ann. N. Y. Acad. Sci. 1099, 456-467 (Pubitemid 47092611)
32. Staiano, R. I., Granata, F., Secondo, A., Petraroli, A., Loffredo, S., Frattini, A., Annunziato, L., Marone, G., and Triggiani, M. (2009) Expression and function of Na+/Ca2+ exchangers 1 and 3 in human macrophages and monocytes. Eur. J. Immunol. 39, 1405-1418
33. Shumilina, E., Xuan, N. T., Matzner, N., Bhandaru, M., Zemtsova, I. M., and Lang, F. (2010) Regulation of calcium signaling in dendritic cells by 1,25-dihydroxyvitamin D3. FASEB J. 24, 1989-1996
34. Heise, N., Shumilina, E., Nurbaeva, M. K., Schmid, E., Szteyn, K., Yang, W., Xuan, N. T., Wang, K., Zemtsova, I. M., Duszenko, M., and Lang, F. (2011) Effect of dexamethasone on Na+/ Ca2+ exchanger in dendritic cells. Am. J. Physiol. Cell Physiol. 300, C1306-C1313
35. Mungai, P. T., Waypa, G. B., Jairaman, A., Prakriya, M., Dokic, D., Ball, M. K., and Schumacker, P. T. (2011) Hypoxia triggers AMPK activation through reactive oxygen species-mediated activation of calcium release-activated calcium channels. Mol. Cell. Biol. 31, 3531-3545
36. Bair, A. M., Thippegowda, P. B., Freichel, M., Cheng, N., Ye, R. D., Vogel, S. M., Yu, Y., Flockerzi, V., Malik, A. B., and Tiruppathi, C. (2009) Ca2+ entry via TRPC channels is necessary for thrombin-induced NF-kappaB activation in endothelial cells through AMP-activated protein kinase and protein kinase Cdelta. J. Biol. Chem. 284, 563-574
37. Towler, M. C., and Hardie, D. G. (2007) AMP-activated protein kinase in metabolic control and insulin signaling. Circ. Res. 100, 328-341
38. Zhang, F., Dey, D., Branstrom, R., Forsberg, L., Lu, M., Zhang, Q., and Sjoholm, A. (2009) BLX-1002, a novel thiazolidinedione with no PPAR affinity, stimulates AMP-activated protein kinase activity, raises cytosolic Ca2+, and enhances glucose-stimulated insulin secretion in a PI3K-dependent manner. Am. J. Physiol. Cell Physiol. 296, C346-C354
39. Hurley, R. L., Anderson, K. A., Franzone, J. M., Kemp, B. E., Means, A. R., and Witters, L. A. (2005) The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J. Biol. Chem. 280, 29060-29066 (Pubitemid 41161355)
40. Woods, A., Johnstone, S. R., Dickerson, K., Leiper, F. C., Fryer, L. G., Neumann, D., Schlattner, U., Wallimann, T., Carlson, M., and Carling, D. (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr. Biol. 13, 2004-2008 (Pubitemid 37425212)
41. Steinberg, G. R., and Kemp, B. E. (2009) AMPK in health and disease. Physiol. Rev. 89, 1025-1078
42. Winder, W. W., and Thomson, D. M. (2007) Cellular energy sensing and signaling by AMP-activated protein kinase. Cell Biochem. Biophys. 47, 332-347 (Pubitemid 47339850)
43. Hardie, D. G. (2008) AMPK: a key regulator of energy balance in the single cell and the whole organism. Int. J. Obes. (Lond.) 32(Suppl. 4), S7-S12
44. Tamas, P., Hawley, S. A., Clarke, R. G., Mustard, K. J., Green, K., Hardie, D. G., and Cantrell, D. A. (2006) Regulation of the energy sensor AMP-activated protein kinase by antigen receptor and Ca2+ in T lymphocytes. J. Exp. Med. 203, 1665-1670 (Pubitemid 44036271)
45. Park, S., Scheffler, T. L., Gunawan, A. M., Shi, H., Zeng, C., Hannon, K. M., Grant, A. L., and Gerrard, D. E. (2009) Chronic elevated calcium blocks AMPK-induced GLUT-4 expression in skeletal muscle. Am. J. Physiol. Cell Physiol. 296, C106-C115
46. Walker, J., Jijon, H. B., Diaz, H., Salehi, P., Churchill, T., and Madsen, K. L. (2005) 5-aminoimidazole-4-carboxamide riboside (AICAR) enhances GLUT2-dependent jejunal glucose transport: a possible role for AMPK. Biochem. J. 385, 485-491 (Pubitemid 40173969)
47. Sopjani, M., Bhavsar, S. K., Fraser, S., Kemp, B. E., Foller, M., and Lang, F. (2010) Regulation of Na+-coupled glucose carrier SGLT1 by AMP-activated protein kinase. Mol. Membr. Biol. 27, 137-144
48. Sopjani, M., Alesutan, I., Dermaku-Sopjani, M., Fraser, S., Kemp, B. E., Foller, M., and Lang, F. (2010) Down-regulation of Na+-coupled glutamate transporter EAAT3 and EAAT4 by AMP-activated protein kinase. J. Neurochem. 113, 1426-1435
49. Rotte, A., Pasham, V., Eichenmuller, M., Bhandaru, M., Foller, M., and Lang, F. (2010) Upregulation of Na+/H+ exchanger by the AMP-activated protein kinase. Biochem. Biophys. Res. Commun. 398, 677-682
50. Gusarova, G. A., Trejo, H. E., Dada, L. A., Briva, A., Welch, L. C., Hamanaka, R. B., Mutlu, G. M., Chandel, N. S., Prakriya, M., and Sznajder, J. I. (2011) Hypoxia leads to Na,K-ATPase downregulation via Ca(2+) release-activated Ca(2+) channels and AMPK activation. Mol. Cell. Biol. 31, 3546-3556
51. Albert, A. P., Woollhead, A. M., Mace, O. J., and Baines, D. L. (2008) AICAR decreases the activity of two distinct amiloride-sensitive Na+-permeable channels in H441 human lung epithelial cell monolayers. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L837-L848
52. Alesutan, I., Munoz, C., Sopjani, M., Dermaku-Sopjani, M., Michael, D., Fraser, S., Kemp, B. E., Seebohm, G., Foller, M., and Lang, F. (2011) Inhibition of Kir2.1 (KCNJ2) by the AMP-activated protein kinase. Biochem. Biophys. Res. Commun. 408, 505-510
53. Alesutan, I., Foller, M., Sopjani, M., Dermaku-Sopjani, M., Zelenak, C., Frohlich, H., Velic, A., Fraser, S., Kemp, B. E., Seebohm, G., Volkl, H., and Lang, F. (2011) Inhibition of the heterotetrameric K+ channel KCNQ1/KCNE1 by the AMP-activated protein kinase. Mol. Membr. Biol. 28, 79-89
54. Alesutan, I., Sopjani, M., Munoz, C., Fraser, S., Kemp, B. E., Foller, M., and Lang, F. (2011) Inhibition of connexin 26 by the AMP-activated protein kinase. J. Membr. Biol. 240, 151-158
55. Almaca, J., Kongsuphol, P., Hieke, B., Ousingsawat, J., Viollet, B., Schreiber, R., Amaral, M. D., and Kunzelmann, K. (2009) AMPK controls epithelial Na(+) channels through Nedd4-2 and causes an epithelial phenotype when mutated. Pflügers Arch. 458, 713-721
56. Alzamora, R., Gong, F., Rondanino, C., Lee, J. K., Smolak, C., Pastor-Soler, N. M., and Hallows, K. R. (2010) AMP-activated protein kinase inhibits KCNQ1 channels through regulation of the ubiquitin ligase Nedd4-2 in renal epithelial cells. Am. J. Physiol. Renal Physiol. 299, F1308-F1319
57. Andersen, M. N., Krzystanek, K., Jespersen, T., Olesen, S. P., and Rasmussen, H. B. (2011) AMP-activated protein kinase down-regulates Kv7.1 cell surface expression. Traffic 13, 143-156
58. Dallas, M. L., Scragg, J. L., and Peers, C. (2009) Inhibition of L-type Ca(2+) channels by carbon monoxide. Adv. Exp. Med. Biol. 648, 89-95
59. Dallas, M. L., Scragg, J. L., Wyatt, C. N., Ross, F., Hardie, D. G., Evans, A. M., and Peers, C. (2009) Modulation of O(2) sensitive K (+) channels by AMP-activated protein kinase. Adv. Exp. Med. Biol. 648, 57-63
60. Evans, A. M., Hardie, D. G., Peers, C., Wyatt, C. N., Viollet, B., Kumar, P., Dallas, M. L., Ross, F., Ikematsu, N., Jordan, H. L., Barr, B. L., Rafferty, J. N., and Ogunbayo, O. (2009) Ion channel regulation by AMPK: the route of hypoxia-response coupling in the carotid body and pulmonary artery. Ann. N. Y. Acad. Sci. 1177, 89-100
61. Hirschler-Laszkiewicz, I., Tong, Q., Waybill, K., Conrad, K., Keefer, K., Zhang, W., Chen, S. J., Cheung, J. Y., and Miller, B. A. (2011) The transient receptor potential (TRP) channel TRPC3 TRP domain and AMP-activated protein kinase binding site are required for TRPC3 activation by erythropoietin. J. Biol. Chem. 286, 30636-30646
62. Kreneisz, O., Benoit, J. P., Bayliss, D. A., and Mulkey, D. K. (2009) AMP-activated protein kinase inhibits TREK channels. J. Physiol. 587, 5819-5830
63. Lim, A., Park, S. H., Sohn, J. W., Jeon, J. H., Park, J. H., Song, D. K., Lee, S. H., and Ho, W. K. (2009) Glucose deprivation regulates KATP channel trafficking via AMP-activated protein kinase in pancreatic beta-cells. Diabetes 58, 2813-2819
64. Mace, O. J., Woollhead, A. M., and Baines, D. L. (2008) AICAR activates AMPK and alters PIP2 association with the epithelial sodium channel ENaC to inhibit Na+ transport in H441 lung epithelial cells. J. Physiol. 586, 4541-4557
65. Myerburg, M. M., King, J. D., Jr., Oyster, N. M., Fitch, A. C., Magill, A., Baty, C. J., Watkins, S. C., Kolls, J. K., Pilewski, J. M., and Hallows, K. R. (2010) AMPK agonists ameliorate sodium and fluid transport and inflammation in cystic fibrosis airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 42, 676-684
66. Ross, F. A., Rafferty, J. N., Dallas, M. L., Ogunbayo, O., Ikematsu, N., McClafferty, H., Tian, L., Widmer, H., Rowe, I. C., Wyatt, C. N., Shipston, M. J., Peers, C., Hardie, D. G., and Evans, A. M. (2011) Selective expression in carotid body type I cells of a single splice variant of the large conductance calcium- and voltage-activated potassium channel confers regulation by AMP-activated protein kinase. J. Biol. Chem. 286, 11929-11936
67. Sidani, S., Kopic, S., Socrates, T., Kirchhoff, P., Foller, M., Murek, M., Capasso, A., and Geibel, J. P. (2009) AMP-activated protein kinase: a physiological off switch for murine gastric acid secretion. Pflügers Arch. 459, 39-46
68. Tang, C., To, W. K., Meng, F., Wang, Y., and Gu, Y. (2010) A role for receptor-operated Ca2+ entry in human pulmonary artery smooth muscle cells in response to hypoxia. Physiol. Res. 59, 909-918
69. Turrell, H. E., Rodrigo, G. C., Norman, R. I., Dickens, M., and Standen, N. B. (2011) Phenylephrine preconditioning involves modulation of cardiac sarcolemmal K(ATP) current by PKC delta, AMPK and p38 MAPK. J. Mol. Cell Cardiol. 51, 370-380
70. Yoshida, H., Bao, L., Kefaloyianni, E., Taskin, E., Okorie, U., Hong, M., Dhar-Chowdhury, P., Kaneko, M., and Coetzee, W. A. (2011) AMP-activated protein kinase connects cellular energy metabolism to K(ATP) channel function. J. Mol. Cell. Cardiol. 52, 410-418
71. Viollet, B., Andreelli, F., Jorgensen, S. B., Perrin, C., Flamez, D., Mu, J., Wojtaszewski, J. F., Schuit, F. C., Birnbaum, M., Richter, E., Burcelin, R., and Vaulont, S. (2003) Physiological role of AMP-activated protein kinase (AMPK): insights from knockout mouse models. Biochem. Soc. Trans. 31, 216-219 (Pubitemid 36241431)
72. Matzner, N., Zemtsova, I. M., Nguyen, T. X., Duszenko, M., Shumilina, E., Lang, F. (2008) Ion channels modulating mouse dendritic cell functions. J. Immunol. 181, 6803-6809
73. Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391, 85-100 (Pubitemid 11012976)
74. Barry, P. H., and Lynch, J. W. (1991) Liquid junction potentials and small cell effects in patch-clamp analysis. J. Membr. Biol. 121, 101-117
75. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
76. Sag, D., Carling, D., Stout, R. D., and Suttles, J. (2008) Adenosine 5=-monophosphate-activated protein kinase promotes macrophage polarization to an anti-inflammatory functional phenotype. J. Immunol. 181, 8633-8641
77. Zanoni, I., Ostuni, R., Capuano, G., Collini, M., Caccia, M., Ronchi, A. E., Rocchetti, M., Mingozzi, F., Foti, M., Chirico, G., Costa, B., Zaza, A., Ricciardi-Castagnoli, P., and Granucci, F. (2009) CD14 regulates the dendritic cell life cycle after LPS exposure through NFAT activation. Nature 460, 264-268
78. Krawczyk, C. M., Holowka, T., Sun, J., Blagih, J., Amiel, E., DeBerardinis, R. J., Cross, J. R., Jung, E., Thompson, C. B., Jones, R. G., and Pearce, E. J. (2010) Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 115, 4742-4749
79. Sumoza-Toledo, A., Lange, I., Cortado, H., Bhagat, H., Mori, Y., Fleig, A., Penner, R., and Partida-Sanchez, S. (2011) Dendritic cell maturation and chemotaxis is regulated by TRPM2-mediated lysosomal Ca2+ release. FASEB J. 25, 3529-3542
80. Aneiros, E., Philipp, S., Lis, A., Freichel, M., and Cavalie, A. (2005) Modulation of Ca2+ signaling by Na+/Ca2+ exchangers in mast cells. J. Immunol. 174, 119-130
81. Baughman, J. M., Perocchi, F., Girgis, H. S., Plovanich, M., Belcher-Timme, C. A., Sancak, Y., Bao, X. R., Strittmatter, L., Goldberger, O., Bogorad, R. L., Koteliansky, V., and Mootha, V. K. (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341-345
82. De Stefani, D., Raffaello, A., Teardo, E., Szabo, I., and Rizzuto, R. (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336-340
83. Partida-Sanchez, S., Goodrich, S., Kusser, K., Oppenheimer, N., Randall, T. D., and Lund, F. E. (2004) Regulation of dendritic cell trafficking by the ADP-ribosyl cyclase CD38: impact on the development of humoral immunity. Immunity 20, 279-291 (Pubitemid 38388230)
84. Eylenstein, A., Gehring, E. M., Heise, N., Shumilina, E., Schmidt, S., Szteyn, K., Munzer, P., Nurbaeva, M. K., Eichenmuller, M., Tyan, L., Regel, I., Foller, M., Kuhl, D., Soboloff, J., Penner, R., and Lang, F. (2011) Stimulation of Ca2+-channel Orai1/STIM1 by serum- and glucocorticoid-inducible kinase 1 (SGK1). FASEB J. 25, 2012-2021
85. Bhalla, V., Oyster, N. M., Fitch, A. C., Wijngaarden, M. A., Neumann, D., Schlattner, U., Pearce, D., and Hallows, K. R. (2006) AMP-activated kinase inhibits the epithelial Na+ channel through functional regulation of the ubiquitin ligase Nedd4-2. J. Biol. Chem. 281, 26159-26169 (Pubitemid 44401823)
86. Carattino, M. D., Edinger, R. S., Grieser, H. J., Wise, R., Neumann, D., Schlattner, U., Johnson, J. P., Kleyman, T. R., and Hallows, K. R. (2005) Epithelial sodium channel inhibition by AMP-activated protein kinase in oocytes and polarized renal epithelial cells. J. Biol. Chem. 280, 17608-17616 (Pubitemid 41388995)
87. Reppel, M., Fleischmann, B. K., Reuter, H., Pillekamp, F., Schunkert, H., and Hescheler, J. (2007) Regulation of Na+/ Ca2+ exchange current in the normal and failing heart. Ann. N. Y. Acad. Sci. 1099, 361-372 (Pubitemid 47092628)
88. 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 (Pubitemid 47092629)
89. 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 (Pubitemid 47092597)
90. Canitano, A., Papa, M., Boscia, F., Castaldo, P., Sellitti, S., Taglialatela, M., and Annunziato, L. (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 (Pubitemid 36126921)
91. Schmitt, R., Ellison, D. H., Farman, N., Rossier, B. C., Reilly, R. F., Reeves, W. B., Oberbaumer, I., Tapp, R., and Bachmann, S. (1999) Developmental expression of sodium entry pathways in rat nephron. Am. J. Physiol. 276, F367-F381 (Pubitemid 29157529)
92. Kimura, M., Jeanclos, E. M., Donnelly, R. J., Lytton, J., Reeves, J. P., and Aviv, A. (1999) Physiological and molecular characterization of the Na+/Ca2+ exchanger in human platelets. Am. J. Physiol. 277, H911-H917 (Pubitemid 29459603)
93. Balasubramanyam, M., Rohowsky-Kochan, C., Reeves, J. P., and Gardner, J. P. (1994) Na+/Ca2+ exchange-mediated calcium entry in human lymphocytes. J. Clin. Invest. 94, 2002-2008
94. Tintinger, G. R., and Anderson, R. (2004) Counteracting effects of NADPH oxidase and the Na+/Ca2+ exchanger on membrane repolarisation and store-operated uptake of Ca2+by chemoattractant-activated human neutrophils. Biochem. Pharmacol. 67, 2263-2271 (Pubitemid 38639934)
95. Rumpel, E., Pilatus, U., Mayer, A., and Pecht, I. (2000) Na(+)-dependent Ca(2+) transport modulates the secretory response to the Fcepsilon receptor stimulus of mast cells. Biophys. J. 79, 2975-2986
96. Koski, G. K., Schwartz, G. N., Weng, D. E., Czerniecki, B. J., Carter, C., Gress, R. E., and Cohen, P. A. (1999) Calcium mobilization in human myeloid cells results in acquisition of individual dendritic cell-like characteristics through discrete signaling pathways. J. Immunol. 163, 82-92 (Pubitemid 29295828)
97. Partida-Sanchez, S., Gasser, A., Fliegert, R., Siebrands, C. C., Dammermann, W., Shi, G., Mousseau, B. J., Sumoza-Toledo, A., Bhagat, H., Walseth, T. F., Guse, A. H., and Lund, F. E. (2007) Chemotaxis of mouse bone marrow neutrophils and dendritic cells is controlled by adp-ribose, the major product generated by the CD38 enzyme reaction. J. Immunol. 179, 7827-7839
98. Rubartelli, A., Poggi, A., and Zocchi, M. R. (1997) The selective engulfment of apoptotic bodies by dendritic cells is mediated by the alpha(v)beta3 integrin and requires intracellular and extracellular calcium. Eur. J. Immunol. 27, 1893-1900 (Pubitemid 27346003)
99. Xuan, N. T., Shumilina, E., Matzner, N., Zemtsova, I. M., Biedermann, T., Goetz, F., and Lang, F. (2009) Ca2+-dependent functions in peptidoglycan- stimulated mouse dendritic cells. Cell. Physiol. Biochem. 24, 167-176
100. Dreval, V., Dieterich, P., Stock, C., and Schwab, A. (2005) The role of Ca2+ transport across the plasma membrane for cell migration. Cell. Physiol. Biochem. 16, 119-126 (Pubitemid 41197095)