Endoplasmic reticulum refilling and mitochondrial calcium extrusion promoted in neurons by NCX1 and NCX3 in ischemic preconditioning are determinant for neuroprotection

Cell Death and Differentiation

Volumn 21, Issue 7, 2014, Pages 1142-1149

  Sisalli, M J ^a   Secondo, A ^a   Esposito, A ^a   Valsecchi, V ^a   Savoia, C ^a   Di Renzo, G F ^a   Annunziato, L ^a   Scorziello, A ^a  

^a University School of Medicine Federico II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 7 CHLORO 5 (2 CHLOROPHENYL) 1,5 DIHYDRO 4,1 BENZOTHIAZEPIN 2(3H) ONE; 7 NITROINDAZOLE; CALCIUM; GLUCOSE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; OXYGEN; SMALL INTERFERING RNA; SODIUM CALCIUM EXCHANGE PROTEIN; WORTMANNIN; SLC8A3 PROTEIN, RAT; SODIUM-CALCIUM EXCHANGER 1;

ANIMAL CELL; ARTICLE; BRAIN CELL; BRAIN ISCHEMIA; CALCIUM HOMEOSTASIS; ENDOPLASMIC RETICULUM; IN VITRO STUDY; ISCHEMIC PRECONDITIONING; MICROFLUOROMETRY; MITOCHONDRION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REOXYGENATION; UPREGULATION; ANIMAL; APOPTOSIS; CALCIUM SIGNALING; CELL CULTURE; CELL HYPOXIA; CELL PROTECTION; CELL SURVIVAL; GENETICS; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL; PHYSIOLOGY; TRANSCRIPTION INITIATION; WISTAR RAT;

ANIMALS; APOPTOSIS; CALCIUM; CALCIUM SIGNALING; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; CYTOPROTECTION; ENDOPLASMIC RETICULUM; GLUCOSE; ISCHEMIC PRECONDITIONING; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NEURONS; NITRIC OXIDE; RATS, WISTAR; SODIUM-CALCIUM EXCHANGER; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84902241397     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.32     Document Type: Article

References (31)

1. Pignataro G, Boscia F, Esposito E, Sirabella R, Cuomo O, Vinciguerra A et al. NCX1 and NCX3: two new effectors of delayed preconditioning in brain ischemia. Neurobiol Dis 2012; 45: 616-623.
2. Bojarski C, Meloni BP, Moore SR, Majda BT, Knuckey NW. Na+/Ca2+ exchanger subtype (NCX1, NCX2, NCX3) protein expression in the rat hippocampus following 3 min and 8min durations of global cerebral ischemia. Brain Res 2008; 1189: 198-202.
3. Mohammadi E, Bigdeli MR. Effects of preconditioning with normobaric hyperoxia on Na(+)/Ca(2)(+) exchanger in the rat brain. Neuroscience 2013; 237: 277-284.
4. Annunziato L, Pignataro G, Di Renzo GF. Pharmacology of brain Na+/Ca2+ exchanger: from molecular biology to therapeutic perspectives. Pharmacol Rev 2004; 56: 633-654.
5. Annunziato L, Pignataro G, Boscia F, Sirabella R, Formisano L, Saggese M et al. ncx1, ncx2, and ncx3 gene product expression and function in neuronal anoxia and brain ischemia. Ann N Y Acad Sc 2007; 1099: 413-426.
6. Sirabella R, Secondo A, Pannaccione A, Scorziello A, Valsecchi V, Adornetto A et al. Anoxia-induced NF-kappaB-dependent upregulation of NCX1 contributes to Ca2+ refilling into endoplasmic reticulum in cortical neurons. Stroke 2009; 40: 922-929.
7. Dawson VL, Dawson TM. Neuronal ischaemic preconditioning. Trends Pharmacol Sci 2000; 21: 423-424.
8. Scorziello A, Santillo M, Adornetto A, Dell'aversano C, Sirabella R, Damiano S et al. NO-induced neuroprotection in ischemic preconditioning stimulates mitochondrial Mn-SOD activity and expression via Ras/ERK1/2 pathway. J Neurochem 2007; 103: 1472-1480.
9. Scorziello A, Savoia C, Sisalli MJ, Adornetto A. Secondo A, Boscia F, et al. NCX3 regulates mitochondrial Ca2+ handling through the AKAP121-anchored signaling complex and prevents hypoxia-induced neuronal death. J Cell Sci 2013; 126(Pt 24): 5566-5577.
10. Dave KR, Saul I, Busto R, Ginsberg MD, Sick TJ, Perez-Pinzon MA. Ischemic preconditioning preserves mitochondrial function after global cerebral ischemia in rat hippocampus. J Cereb Blood Flow Metab 2001; 21: 1401-1410.
11. Zhang HX, Du GH, Zhang JT. Ischemic pre-conditioning preserves brain mitochondrial functions during the middle cerebral artery occlusion in rat. Neurol Res 2003; 25: 471-476.
12. Formisano L, Saggese M, Secondo A, Sirabella R, Vito P, Valsecchi V et al. The two isoforms of the Na+/Ca2+ exchanger, NCX1 and NCX3, constitute novel additional targets for the prosurvival action of Akt/protein kinase B pathway. Mol Pharmacol 2008; 73: 727-737.
13. Huang PL. Nitric oxide and cerebral ischemic preconditioning. Cell Calcium 2004; 36: 323-329.
14. Knepper BR, Kurylo DD. Effects of nitric oxide synthase inhibitor NG-nitro-L-arginine methyl ester on spatial and cued leaning. Neuroscience 1998; 83: 837-841.
15. Pignataro G, Esposito E, Sirabella R, Vinciguerra A, Cuomo O, Di Renzo G et al. nNOS and p-ERK involvement in the neuroprotection exerted by remote postconditioning in rats subjected to transient middle cerebral artery occlusion. Neurobiol Dis 2013; 54: 105-114.
16. Secondo A, Taglialatela M, Cataldi M, Giorgio G, Valore M, Di Renzo G et al. Pharmacological blockade of ERG K(+) channels and Ca(2+) influx through store-operated channels exerts opposite effects on intracellular Ca(2+) oscillations in pituitary GH(3) cells. Mol Pharmacol 2000; 58: 1115-1128.
17. Cox DA, Conforti L, Sperelakis N, Matlib MA. Selectivity of inhibition of Na(+)-Ca2+ exchange of heart mitochondria by benzothiazepine CGP-37157. J Cardiovasc Pharmacol 1993; 21: 595-599.
18. Secondo A, Molinaro P, Pannaccione A, Esposito A, Cantile M, Lippiello P et al. Nitric oxide stimulates NCX1 and NCX2 but inhibits NCX3 isoform by three distinct molecular determinants. Mol Pharmacol 2011; 79: 558-568.
19. Babcock DF, Herrington J, Goodwin PC, Park YB, Hille B. Mitochondrial participation in the intracellular Ca2+ network. J Cell Biol 1997; 136: 833-844.
20. Budd SL, Nicholls DG. Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem 1996; 67: 2282-2291.
21. Jouaville LS, Ichas F, Holmuhamedov EL, Camacho P, Lechleiter JD. Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature 1995; 377: 438-441.
22. Werth JL, Thayer SA. Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons. J Neurosci 1994; 14: 348-356.
23. Saris NE, Carafoli E. A historical review of cellular calcium handling, with emphasis on mitochondria. Biochem Biokhimiia 2005; 70: 187-194.
24. Denton RM, McCormack JG. On the role of the calcium transport cycle in heart and other mammalian mitochondria. FEBS Lett 1980; 119: 1-8.
25. Abramov AY, Scorziello A, Duchen MR. Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J Neurosci 2007; 27: 1129-1138.
26. Scorziello A, Pellegrini C, Forte L, Tortiglione A, Gioielli A, Iossa S et al. Differential vulnerability of cortical and cerebellar neurons in primary culture to oxygen glucose deprivation followed by reoxygenation. J Neurosci Res 2001; 63: 20-26.
27. Livigni A, Scorziello A, Agnese S, Adornetto A, Carlucci A, Garbi C et al. Mitochondrial AKAP121 links cAMP and src signaling to oxidative metabolism. Mol Biol Cell 2006; 17: 263-271.
28. Secondo A, Staiano RI, Scorziello A, Sirabella R, Boscia F, Adornetto A et al. 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 2007; 42: 521-535.
29. Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985; 260: 3440-3450.
30. Wei H, Leeds PR, Qian Y, Wei W, Chen R, Chuang D. beta-amyloid peptide-induced death of PC 12 cells and cerebellar granule cell neurons is inhibited by long-term lithium treatment. Eur J Pharmacol 2000; 392: 117-123.
31. Hansen MB, Nielsen SE, Berg K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J Immunol Methods 1989; 119: 203-210.