Endoplasmic reticulum potassium-hydrogen exchanger and small conductance calcium-activated potassium channel activities are essential for ER calcium uptake in neurons and cardiomyocytes

Journal of Cell Science

Volumn 125, Issue 3, 2012, Pages 625-633

  Kuum, Malle ^a,b,c   Veksler, Vladimir ^b,c   Liiv, Joanna ^a   Ventura Clapier, Renee ^b,c   Kaasik, Allen ^a  

^a Faculty of Medicine   (Estonia)

^b INSERM   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Counterion fluxes; Endoplasmic reticulum; LETM1; SK ca channels

Indexed keywords

CALCIUM; DEQUALINIUM; LEUCINE ZIPPER EF HAND CONTAINING TRANSMEMBRANE PROTEIN 1; MEMBRANE PROTEIN; NIGERICIN; POTASSIUM; POTASSIUM PROTON EXCHANGE PROTEIN; PROPRANOLOL; QUININE; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; SODIUM; TETRYLAMMONIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL IMMORTALIZATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FLUORESCENCE MICROSCOPE; HEART MUSCLE CELL; HYPOTHALAMUS; MOUSE; NERVE CELL; NONHUMAN; POTASSIUM TRANSPORT; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

ANIMALS; CALCIUM; CELLS, CULTURED; ENDOPLASMIC RETICULUM; ION TRANSPORT; MICE; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; NEURONS; NIGERICIN; POTASSIUM-HYDROGEN ANTIPORTERS; PROPRANOLOL; RATS; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS;

RATTUS;

EID: 84858114931     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.090126     Document Type: Article

References (44)

1. Choubey, V., Safiulina, D., Vaarmann, A., Cagalinec, M., Wareski, P., Kuum, M., Zharkovsky, A. and Kaasik, A. (2011). Mutant A53T alpha-synuclein induces neuronal death by increasing mitochondrial autophagy. J. Biol. Chem. 286, 10814-10824.
2. Dimmer, K. S., Navoni, F., Casarin, A., Trevisson, E., Endele, S., Winterpacht, A., Salviati, L. and Scorrano, L. (2008). LETM1, deleted in Wolf-Hirschhorn syndrome is required for normal mitochondrial morphology and cellular viability. Hum. Mol. Genet. 17, 201-214.
3. Edwards, J. C. and Kahl, C. R. (2010). Chloride channels of intracellular membranes. FEBS Lett. 584, 2102-2111.
4. 2+)-binding protein, flanks the Wolf-Hirschhorn syndrome (WHS) critical region and is deleted in most WHS patients. Genomics 60, 218-225.
5. Faber, E. S. (2009). Functions and modulation of neuronal SK channels. Cell Biochem. Biophys. 55, 127-139.
6. Fakler, B. and Adelman, J. P. (2008). Control of K(Ca) channels by calcium nano/ microdomains. Neuron 59, 873-881.
7. Fernandez de Sevilla, D., Garduno, J., Galvan, E. and Buno, W. (2006). Calciumactivated afterhyperpolarizations regulate synchronization and timing of epileptiform bursts in hippocampal CA3 pyramidal neurons. J. Neurophysiol. 96, 3028-3041.
8. + exchange in mitochondrial membrane vesicles involves Yol027/Letm1 proteins. Biochim. Biophys. Acta 1711, 41-48.
9. Garduno, J., Galvan, E., Fernandez de Sevilla, D. and Buno, W. (2005). 1-Ethyl-2-benzimidazolinone (EBIO) suppresses epileptiform activity in in vitro hippocampus. Neuropharmacology 49, 376-388.
10. + antiporter ClC-7 is the primary chloride permeation pathway in lysosomes. Nature 453, 788-792.
11. 2+ handling in airway smooth muscle. Am. J. Physiol. Lung Cell Mol. Physiol. 290, L1146-L1153.
12. Jentsch, T. J. (2007). Chloride and the endosomal-lysosomal pathway: emerging roles of CLC chloride transporters. J. Physiol. 578, 633-640.
13. Joiner, W. J., Wang, L. Y., Tang, M. D. and Kaczmarek, L. K. (1997). hSK4, a member of a novel subfamily of calcium-activated potassium channels. Proc. Natl. Acad. Sci. USA 94, 11013-11018.
14. Kaasik, A., Joubert, F., Ventura-Clapier, R. and Veksler, V. (2004). A novel mechanism of regulation of cardiac contractility by mitochondrial functional state. FASEB J. 18, 1219-1227.
15. 2+ uptake and release by the sarcoplasmic reticulum of saponin permeabilized isolated smooth muscle cells. J. Gen. Physiol. 106, 467-484.
16. Kim, J. H., Johannes, L., Goud, B., Antony, C., Lingwood, C. A., Daneman, R. and Grinstein, S. (1998). Noninvasive measurement of the pH of the endoplasmic reticulum at rest and during calcium release. Proc. Natl. Acad. Sci. USA 95, 2997-3002.
17. Kneen, M., Farinas, J., Li, Y. and Verkman, A. S. (1998). Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys. J. 74, 1591-1599.
18. Koch, G. L., Macer, D. R. and Smith, M. J. (1987). Visualization of the intact endoplasmic reticulum by immunofluorescence with antibodies to the major ER glycoprotein, endoplasmin. J. Cell Sci. 87, 535-542.
19. 2+ loss in cardiac muscle: different efficiencies of different energy sources. Cardiovasc. Res. 83, 89-96.
20. Levy, D., Seigneuret, M., Bluzat, A. and Rigaud, J. L. (1990). Evidence for proton countertransport by the sarcoplasmic reticulum Ca2(+)-ATPase during calcium transport in reconstituted proteoliposomes with low ionic permeability. J. Biol. Chem. 265, 19524-19534.
21. Mancilla, E. and Rojas, E. (1990). Quinine blocks the high conductance, calciumactivated potassium channel in rat pancreatic beta-cells. FEBS Lett. 260, 105-108.
22. McQuibban, A. G., Joza, N., Megighian, A., Scorzeto, M., Zanini, D., Reipert, S., Richter, C., Schweyen, R. J. and Nowikovsky, K. (2010). A Drosophila mutant of LETM1, a candidate gene for seizures in Wolf-Hirschhorn syndrome. Hum. Mol. Genet. 19, 987-1000.
23. 2+ uptake by cardiac sarcoplasmic reticulum ATPase in situ strongly depends on bound creatine kinase. Pflugers Arch. 432, 904-912.
24. Miyazaki, E., Sakaguchi, M., Wakabayashi, S., Shigekawa, M. and Mihara, K. (2001). NHE6 protein possesses a signal peptide destined for endoplasmic reticulum membrane and localizes in secretory organelles of the cell. J. Biol. Chem. 276, 49221-49227.
25. Nowikovsky, K., Froschauer, E. M., Zsurka, G., Samaj, J., Reipert, S., Kolisek, M., Wiesenberger, G. and Schweyen, R. J. (2004). The LETM1/YOL027 gene family encodes a factor of the mitochondrial K+ homeostasis with a potential role in the Wolf-Hirschhorn syndrome. J. Biol. Chem. 279, 30307-30315.
26. Pal, S., Sombati, S., Limbrick, D. D., Jr and DeLorenzo, R. J. (1999). In vitro status epilepticus causes sustained elevation of intracellular calcium levels in hippocampal neurons. Brain Res. 851, 20-31.
27. 2+-activated K+ channels. J. Biol. Chem. 276, 9762-9769.
28. 2+) interaction with the ion-binding sites of the SR Ca-ATPase. Biophys. J. 82, 170-181.
29. Picollo, A. and Pusch, M. (2005). Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 436, 420-423.
30. Plans, V., Rickheit, G. and Jentsch, T. J. (2009). Physiological roles of CLC Cl(-)/ H(+) exchangers in renal proximal tubules. Pflugers Arch. 458, 23-37.
31. 2+ uptake by the smooth muscle sarcoplasmic reticulum. Biophys. J. 75, 1759-1766.
32. Raza, M., Pal, S., Rafiq, A. and DeLorenzo, R. J. (2001). Long-term alteration of calcium homeostatic mechanisms in the pilocarpine model of temporal lobe epilepsy. Brain Res. 903, 1-12.
33. Raza, M., Blair, R. E., Sombati, S., Carter, D. S., Deshpande, L. S. and DeLorenzo, R. J. (2004). Evidence that injury-induced changes in hippocampal neuronal calcium dynamics during epileptogenesis cause acquired epilepsy. Proc. Natl. Acad. Sci. USA 101, 17522-17527.
34. Safiulina, D., Veksler, V., Zharkovsky, A. and Kaasik, A. (2006). Loss of mitochondrial membrane potential is associated with increase in mitochondrial volume: physiological role in neurones. J. Cell. Physiol. 206, 347-353.
35. Scheel, O., Zdebik, A. A., Lourdel, S. and Jentsch, T. J. (2005). Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436, 424-427.
36. South, S. T., Bleyl, S. B. and Carey, J. C. (2007). Two unique patients with novel microdeletions in 4p16.3 that exclude the WHS critical regions: implications for critical region designation. Am. J. Med. Genet. A 143A, 2137-2142.
37. 2+ uptake. J. Biochem. 89, 1247-1252.
38. 2+ current in rat ventricular myocytes. Br. J. Pharmacol. 127, 65-74.
39. Wareski, P., Vaarmann, A., Choubey, V., Safiulina, D., Liiv, J., Kuum, M. and Kaasik, A. (2009). PGC-1{alpha} and PGC-1{beta} regulate mitochondrial density in neurons. J. Biol. Chem. 284, 21379-21385.
40. Wassler, M., Jonasson, I., Persson, R. and Fries, E. (1987). Differential permeabilization of membranes by saponin treatment of isolated rat hepatocytes. Release of secretory proteins. Biochem. J. 247, 407-415.
41. 2+ release. FEBS J. 273, 3585-3597.
42. 2+ pump in reconstituted proteoliposomes. Biophys. J. 64, 1232-1242.
43. +-channel subunits on the mitochondria and endoplasmic reticulum of rat cardiomyocytes. J. Histochem. Cytochem. 53, 1491-1500.
44. Zollino, M., Lecce, R., Fischetto, R., Murdolo, M., Faravelli, F., Selicorni, A., Butte, C., Memo, L., Capovilla, G. and Neri, G. (2003). Mapping the Wolf-Hirschhorn syndrome phenotype outside the currently accepted WHS critical region and defining a new critical region, WHSCR-2. Am. J. Hum. Genet. 72, 590-597.