Bioenergetic analysis of cerebellar granule neurons undergoing apoptosis by potassium/serum deprivation

Cell Death and Differentiation

Volumn 13, Issue 9, 2006, Pages 1595-1610

  Jekabsons, M B ^a,b   Nicholls, D G ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; HYDROETHIDINE; OXYGEN; POTASSIUM ION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOENERGY; BRAIN NERVE CELL; CELL FUNCTION; CEREBELLUM; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOPLASM; GRANULE CELL; HIPPOCAMPUS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; POTASSIUM DEFICIENCY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; RESPIRATORY CHAIN; SERUM; STEADY STATE;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; CALCIUM; CELL RESPIRATION; CELLS, CULTURED; CEREBELLUM; CULTURE MEDIA, SERUM-FREE; ENERGY METABOLISM; HIPPOCAMPUS; MITOCHONDRIA; NEURONS; POTASSIUM; RATS; SUPEROXIDES;

EID: 33747149006     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401851     Document Type: Article

References (49)

1. + channels. J. Biol. Chem. 278: 32068-32076
2. 2+ channels. J. Bioenerg. Biomembr. 35: 621-637
3. + channels: Role in apoptosis and tumorigenesis 8. Pflugers Arch. 448: 261-273
4. Atlante A, Gagliardi S, Marra E and Calissano P (1998) Neuronal apoptosis in rats is accompanied by rapid impairment of cellular respiration and is prevented by scavengers of reactive oxygen species. Neurosci. Lett. 245: 127-130
5. Bobba A, Atlante A, Giannattasio S, Sgaramella G, Calissano P and Marra E (1999) Early release and subsequent caspase-mediated degradation of cytochrome c in apoptotic cerebellar granule cells. FEBS Lett. 457: 126-130
6. Linseman DA, Phelps RA, Bouchard RJ, Le SS, Laessig TA, McClure ML and Heidenreich KA (2002) Insulin-like growth factor-1 blocks Bcl-2 interacting mediator of cell death (Bim) induction and intrinsic death signaling in cerebellar granule neurons 13. J. Neurosci. 22: 9287-9297
7. Miller TM, Moulder KL, Knudson CM, Creedon DJ, Deshmukh M, Korsmeyer SJ and Johnson Jr EM (1997) Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspase-independent pathway to cell death. J. Cell Biol. 139: 205-217
8. Polster BM and Fiskum G (2004) Mitochondrial mechanisms of neural cell apoptosis. J. Neurochem. 90: 1281-1289
9. Jekabsons MB and Nicholls DG (2004) In situ respiration and bioenergetic status of mitochondria in primary cerebellar granule neuronal cultures exposed continuously to glutamate. J. Biol. Chem. 279: 32989-33000
10. Gonzalvez F, Pariselli F, Dupaigne P, Budihardjo I, Lutter M, Antonsson B, Diolez P, Manon S, Martinou JC, Goubern M, Wang X, Bernard S and Petit PX (2005) tBid interaction with cardiolipin primarily orchestrates mitochondrial dysfunctions and subsequently activates Bax and Bak. Cell Death Differ. 12: 614-626
11. Rostovtseva TK, Antonsson B, Suzuki M, Youle RJ, Colombini M and Bezrukov SM (2004) Bid, but not Bax, regulates VDAC channels. J. Biol. Chem. 279: 13575-13583
12. Vander Heiden MG, Chandel NS, Li XX, Schumacker PT, Colombini M and Thompson CB (2000) Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival. Proc. Natl. Acad. Sci. USA 97: 4666-4671
13. Hammerman PS, Fox CJ and Thompson CB (2004) Beginnings of a signal-transduction pathway for bioenergetic control of cell survival. Trends Biochem. Sci. 29: 586-592
14. Vesce S, Jekabsons MB, Johnson-Cadwell LI and Nicholls DG (2005) Neuronal glutathione depletion increases vulnerability to glutamate by restricting mitochondrial ATP export. J. Biol. Chem. 280: 38720-38728
15. Scott ID and Nicholls DG (1980) Energy transduction in intact synaptosomes: Influence of plasma- membrane depolarization on the respiration and membrane potential of internal mitochondria determined in situ. Biochem. J. 186: 21-33
16. Atchison WD, Luke VS, Narahashi T and Vogel SM (1986) Nerve membrane sodium channels as the target site of brevetoxins at neuromuscular junctions. Br. J. Pharmacol. 89: 731-738
17. Campbell DT (1992) Large and small vertebrate sensory neurons express different Na and K channel subtypes. Proc. Natl. Acad. Sci. USA 89: 9569-9573
18. Leppanen L and Stys PK (1997) Ion transport and membrane potential in CNS myelinated axons I. Normoxic conditions. J. Neurophysiol. 78: 2086-2094
19. Valencia A and Morán J (2001) Role of oxidative stress in the apoptotic cell death of cultured cerebellar granule neurons. J. Neurosci. Res. 64: 284-297
20. Korshunov SS, Skulachev VP and Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 416: 15-18
21. Starkov AA, Polster BM and Fiskum G (2002) Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J. Neurochem. 83: 220-228
22. Lambert AJ and Brand MD (2004) Superoxide production by NADH: Ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane. Biochem. J. 382: 511-517
23. Nicotera P and Leist M (1997) Energy supply and the shape of death in neurons and lymphoid cells. Cell Death Differ. 4: 435-442
24. Castiglione M, Spinsanti P, Iacovelli L, Lenti L, Martini F, Gradini R, Gerevini VD, Caricasole A, Caruso A, De Maria R, Nicoletti F and Melchiorri D (2004) Activation of Fas receptor is required for the increased formation of the disialoganglioside GD3 in cultured cerebellar granule cells committed to apoptotic death. Neuroscience 126: 889-898
25. Harris C, Maroney AC and Johnson Jr EM (2002) Identification of JNK-dependent and -independent components of cerebellar granule neuron apoptosis. J. Neurochem. 83: 992-1001
26. McGinnis KM, Gnegy ME and Wang KK (1999) Endogenous Bax translocation in SH-SY5Y human neuroblastoma cells and cerebellar granule neurons undergoing apoptosis. J. Neurochem. 72: 1899-1906
27. Linseman DA, Butts BD, Precht TA, Phelps RA, Le SS, Laessig TA, Bouchard RJ, Florez-McClure ML and Heidenreich KA (2004) Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J. Neurosci. 24: 9993-10002
28. Alavez S, Pedroza D and Morán J (2003) Mechanisms of cell death by deprivation of depolarizing conditions during cerebellar granule neurons maturation. Neurochem. Int. 43: 581-590
29. Schulz JB, Weller M and Klockgether T (1996) Potassium deprivation-induced apoptosis of cerebellar granule neurons: A sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. J. Neurosci. 16: 4696-4706
30. Tanabe H, Eguchi Y, Shimizu S, Martinou JC and Tsujimoto Y (1998) Death-signalling cascade in mouse cerebellar granule neurons. Eur. J. Neurosci. 10: 1403-1411
31. Atlante A, Giannattasio S, Bobba A, Gagliardi S, Petragallo V, Calissano P, Marra E and Passarella S (2005) An increase in the ATP levels occurs in cerebellar granule cells en route to apoptosis in which ATP derives from both oxidative phosphorylation and anaerobic glycolysis. Biochim. Biophys. Acta 1708: 50-62
32. Martin-Romero FJ, Garcia-Martin E and Gutierrez-Merino C (2002) Inhibition of oxidative stress produced by plasma membrane NADH oxidase delays low-potassium-induced apoptosis of cerebellar granule cells. J. Neurochem. 82: 705-715
33. Atlante A, Bobba A, Calissano P, Passarella S and Marra E (2003) The apoptosis/necrosis transition in cerebellar granule cells depends on the mutual relationship of the antioxidant and the proteolytic systems which regulate ROS production and cytochrome c release en route to death. J. Neurochem. 84: 960-971
34. Tabuchi A, Funaji K, Nakatsubo J, Fukuchi M, Tsuchiya T and Tsuda M (2003) Inactivation of aconitase during the apoptosis of mouse cerebellar granule neurons induced by a deprivation of membrane depolarization. J. Neurosci. Res. 71: 504-515
35. 2 production by membrane potential and NAD(P)H redox state. J. Neurochem. 86: 1101-1107
36. Kirkland RA, Windelbom JA, Kasprzak JM and Franklin JL (2002) A Bax-induced pro-oxidant state is critical for cytochrome c release during programmed neuronal death. J. Neurosci. 22: 6480-6490
37. Kirkland RA and Franklin JL (2003) Bax, reactive oxygen, and cytochrome c release in neuronal apoptosis. Antioxid. Redox. Signal. 5: 589-596
38. Liu YB, Fiskum G and Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80: 780-787
39. Nicholls DG (1977) The effective proton conductances of the inner membrane of mitochondria from brown adipose tissue: Dependency on proton electrochemical gradient. Eur. J. Biochem. 77: 349-356
40. 2+ of rat cerebellar granule cells in explant culture. J. Neurosci. 7: 1384-1400
41. Pocock JM, Cousin MA and Nicholls DG (1993) The calcium channel coupled to glutamate exocytosis from cerebellar granule cells is inhibited by the spider toxin Aga-GI. Neuropharmacology 32: 1185-1194
42. Galli C, Meucci O, Scorziello A, Werge TM, Calissano P and Schettini G (1995) Apoptosis in cerebellar granule cells is blocked by high KCl, forskolin, and IGF-1 through distinct mechanisms of action: The involvement of intracellular calcium and RNA synthesis. J. Neurosci. 15: 1172-1179
43. Nicholls DG and Scott ID (1980) The regulation of brain mitochondrial calcium-ion transport: The role of ATP in the discrimination between kinetic and membrane-potential-dependent Ca efflux mechanisms. Biochem. J. 186: 833-839
44. Bobba A, Canu N, Atlante A, Petragallo V, Calissano P and Marra E (2002) Proteasome inhibitors prevent cytochrome c release during apoptosis but not in excitotoxic death of cerebellar granule neurons. FEBS Lett. 515: 8-12
45. Precht TA, Phelps RA, Linseman DA, Butts BD, Le SS, Laessig TA, Bouchard RJ and Heidenreich KA (2005) The permeability transition pore triggers Bax translocation to mitochondria during neuronal apoptosis. Cell Death. Differ. 12: 255-265
46. Madesh M and Hajnoczky G (2001) VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J. Cell Biol. 155: 1003-1015
47. 2+-induced reactive oxygen species production promotes cytochrome c release from rat liver mitochondria via mitochondrial permeability transition (MPT)-dependent and MPT-independent mechanisms: Role of cardiolipin. J. Biol. Chem. 279: 53103-53108
48. Petrosillo G, Ruggiero FM and Paradies G (2003) Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria. FASEB J. 17: 2202-2208
49. Ward MW, Rego AC, Frenguelli BG and Nicholls DG (2000) Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurosci. 20: 7208-7219