Mitochondria and synaptic plasticity in the mature and aging nervous system

Current Neuropharmacology

Volumn 15, Issue 1, 2017, Pages 166-173

  Todorova, Vyara ^a   Blokland, Arjan ^b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Aging; ATP; Calcium; Learning and memory; Long term potentiation; Mitochondria; Synaptic plasticity

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYCLOSPORIN A; REACTIVE OXYGEN METABOLITE;

AGING; BRAIN MITOCHONDRION; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; DENDRITIC SPINE; ELECTROSTIMULATION; GENE EXPRESSION; GENE MUTATION; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; MITOCHONDRIAL RESPIRATION; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVOUS SYSTEM; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; RESPIRATORY CHAIN; REVIEW; SYNAPTIC TRANSMISSION; ANIMAL; CYTOLOGY; MITOCHONDRION; PHYSIOLOGY; SYNAPSE;

AGING; ANIMALS; HUMANS; MITOCHONDRIA; NERVOUS SYSTEM; NEURONAL PLASTICITY; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 85011769647     PISSN: 1570159X     EISSN: 18756190     Source Type: Journal    
DOI: 10.2174/1570159X14666160414111821     Document Type: Review

References (87)

1. Malenka, R.C.; Nicoll, R.A. Long-term potentiation--a decade of progress? Science, 1999, 285(5435), 1870-1874 [http://dx.doi.org/10.1126/science.285.5435.1870] [PMID: 10489359]
2. Cheng, A.; Hou, Y.; Mattson, M.P. Mitochondria and neuroplasticity. ASN Neuro, 2010, 2(5), e00045 [http://dx.doi.org/10.1042/AN20100019] [PMID: 20957078]
3. Malenka, R.C.; Bear, M.F. LTP and LTD: an embarrassment of riches. Neuron, 2004, 44(1), 5-21 [http://dx.doi.org/10.1016/j.neuron.2004.09.012] [PMID: 15450156]
4. Shepherd, J.D.; Huganir, R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol., 2007, 23, 613-643 [http://dx.doi.org/10.1146/annurev.cellbio.23.090506.123516] [PMID: 17506699]
5. Bramham, C.R. Local protein synthesis, actin dynamics, and LTP consolidation. Curr. Opin. Neurobiol., 2008, 18(5), 524-531 [http://dx.doi.org/10.1016/j.conb.2008.09.013] [PMID: 18834940]
6. Greer, P.L.; Greenberg, M.E. From synapse to nucleus: calciumdependent gene transcription in the control of synapse development and function. Neuron, 2008, 59(6), 846-860 [http://dx.doi.org/10.1016/j.neuron.2008.09.002] [PMID: 18817726]
7. Shah, M.M.; Hammond, R.S.; Hoffman, D.A. Dendritic ion channel trafficking and plasticity. Trends Neurosci., 2010, 33(7), 307-316 [http://dx.doi.org/10.1016/j.tins.2010.03.002] [PMID: 20363038]
8. Morris, R.G. NMDA receptors and memory encoding. Neuropharmacology, 2013, 74, 32-40 [http://dx.doi.org/10.1016/j.neuropharm.2013.04.014] [PMID: 23628345]
9. Mattson, M.P.; Liu, D. Mitochondrial potassium channels and uncoupling proteins in synaptic plasticity and neuronal cell death. Biochem. Biophys. Res. Commun., 2003, 304(3), 539-549 [http://dx.doi.org/10.1016/S0006-291X(03)00627-2] [PMID: 12729589]
10. Wieraszko, A. Changes in the hippocampal slices energy metabolism following stimulation and long-term potentiation of Schaffer collaterals-pyramidal cell synapses tested with the 2-deoxyglucose technique. Brain Res., 1982, 237(2), 449-457 [http://dx.doi.org/10.1016/0006-8993(82)90456-5] [PMID: 7083005]
11. Stanton, P.K.; Schanne, F.A. Hippocampal long-term potentiation increases mitochondrial calcium pump activity in rat. Brain Res., 1986, 382(1), 185-188 [http://dx.doi.org/10.1016/0006-8993(86)90130-7] [PMID: 2945618]
12. Williams, J.M.; Thompson, V.L.; Mason-Parker, S.E.; Abraham, W.C.; Tate, W.P. Synaptic activity-dependent modulation of mitochondrial gene expression in the rat hippocampus. Brain Res. Mol. Brain Res., 1998, 60(1), 50-56 [http://dx.doi.org/10.1016/S0169-328X(98)00165-X] [PMID: 9748499]
13. Bruce, A.; Johnson, A.; Lewis, J.; Raff, M.; Roberts, K. Peter Walter Energy Conversion: Mitochondria and Chloroplasts. In: Molecular Biology of the Cell; Garland Science, 2007; 1392, pp. 767-831.
14. Mattson, M.P.; Gleichmann, M.; Cheng, A. Mitochondria in neuroplasticity and neurological disorders. Neuron, 2008, 60(5), 748-766 [http://dx.doi.org/10.1016/j.neuron.2008.10.010] [PMID: 19081372]
15. Simpson, P.B. The local control of cytosolic Ca2+ as a propagator of CNS communication--integration of mitochondrial transport mechanisms and cellular responses. J. Bioenerg. Biomembr., 2000, 32(1), 5-13 [http://dx.doi.org/10.1023/A:1005552126516] [PMID: 11768762]
16. Mattson, M.P. Mitochondrial regulation of neuronal plasticity. Neurochem. Res., 2007, 32(4-3), 707-715 [http://dx.doi.org/10. 1007/s11064-006-9170-3] [PMID: 17024568]
17. Su, B.; Ji, Y.S.; Sun, X.L.; Liu, X.H.; Chen, Z.Y. Brain-derived neurotrophic factor (BDNF)-induced mitochondrial motility arrest and presynaptic docking contribute to BDNF-enhanced synaptic transmission. J. Biol. Chem., 2014, 289(3), 1213-1226 [http://dx.doi.org/10.1074/jbc.M113.526129] [PMID: 24302729]
18. Brot, S.; Auger, C.; Bentata, R.; Rogemond, V.; Ménigoz, S.; Chounlamountri, N.; Girard-Egrot, A.; Honnorat, J.; Moradi-Améli, M. Collapsin response mediator protein 5 (CRMP5) induces mitophagy, thereby regulating mitochondrion numbers in dendrites. J. Biol. Chem., 2014, 289(4), 2261-2276 [http://dx.doi.org/10.1074/jbc.M113.490862] [PMID: 24324268]
19. Manczak, M.; Sheiko, T.; Craigen, W.J.; Reddy, P.H. Reduced VDAC1 protects against Alzheimer’s disease, mitochondria, and synaptic deficiencies. J. Alzheimers Dis., 2013, 37(4), 679-690 [PMID: 23948905]
20. Ivannikov, M.V.; Sugimori, M.; Llinás, R.R. Synaptic vesicle exocytosis in hippocampal synaptosomes correlates directly with total mitochondrial volume. J. Mol. Neurosci., 2013, 49(1), 223-230 [http://dx.doi.org/10.1007/s12031-012-9848-8] [PMID: 22772899]
21. Amaral, M.D.; Pozzo-Miller, L. Intracellular Ca2+ stores and Ca2+ influx are both required for BDNF to rapidly increase quantal vesicular transmitter release. Neural. Plast., 2012, 2012, 203536.
22. Nguyen, P.V.; Atwood, H.L. Altered impulse activity modifies synaptic physiology and mitochondria in crayfish phasic motor neurons. J. Neurophysiol., 1994, 72(6), 2944-2955 [PMID: 7897501]
23. Alnaes, E.; Rahamimoff, R. On the role of mitochondria in transmitter release from motor nerve terminals. J. Physiol., 1975, 248(2), 285-306 [http://dx.doi.org/10.1113/jphysiol.1975.sp010974] [PMID: 50439]
24. Tang, Y.; Zucker, R.S. Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron, 1997, 18(3), 483-491 [http://dx.doi.org/10.1016/S0896-6273(00)81248-9] [PMID: 9115741]
25. Billups, B.; Forsythe, I.D. Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J. Neurosci., 2002, 22(14), 5840-5847 [PMID: 12122046]
26. Medler, K.; Gleason, E.L. Mitochondrial Ca(2+) buffering regulates synaptic transmission between retinal amacrine cells. J. Neurophysiol., 2002, 87(3), 1426-1439 [PMID: 11877517]
27. Li, Z.; Okamoto, K.; Hayashi, Y.; Sheng, M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell, 2004, 119(6), 873-887 [http://dx.doi.org/10.1016/j.cell.2004.11.003] [PMID: 15607982]
28. Wong, R.O.; Ghosh, A. Activity-dependent regulation of dendritic growth and patterning. Nat. Rev. Neurosci., 2002, 3(10), 803-812 [http://dx.doi.org/10.1038/nrn941] [PMID: 12360324]
29. Yuste, R.; Bonhoeffer, T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci., 2001, 24, 1071-1089 [http://dx.doi.org/10.1146/annurev.neuro.24.1.1071] [PMID: 11520928]
30. Carlisle, H.J.; Kennedy, M.B. Spine architecture and synaptic plasticity. Trends Neurosci., 2005, 28(4), 182-187 [http://dx.doi.org/10.1016/j.tins.2005.01.008] [PMID: 15808352]
31. Cameron, H.A.; Kaliszewski, C.K.; Greer, C.A. Organization of mitochondria in olfactory bulb granule cell dendritic spines. Synapse, 1991, 8(2), 107-118 [http://dx.doi.org/10.1002/syn.890080205] [PMID: 1715612]
32. Popov, V.; Medvedev, N.I.; Davies, H.A.; Stewart, M.G. Mitochondria form a filamentous reticular network in hippocampal dendrites but are present as discrete bodies in axons: a threedimensional ultrastructural study. J. Comp. Neurol., 2005, 492(1), 50-65 [http://dx.doi.org/10.1002/cne.20682] [PMID: 16175555]
33. Valenti, D.; de Bari, L.; De Filippis, B.; Henrion-Caude, A.; Vacca, R.A. Mitochondrial dysfunction as a central actor in intellectual disability-related diseases: an overview of Down syndrome, autism, Fragile X and Rett syndrome. Neurosci. Biobehav. Rev., 2014, 46(Pt 2), 202-217 [http://dx.doi.org/10.1016/j.neubiorev.2014.01.012] [PMID: 24548784]
34. Cherra, S.J., III; Steer, E.; Gusdon, A.M.; Kiselyov, K.; Chu, C.T. Mutant LRRK2 elicits calcium imbalance and depletion of dendritic mitochondria in neurons. Am. J. Pathol., 2013, 182(2), 474-484 [http://dx.doi.org/10.1016/j.ajpath.2012.10.027] [PMID: 23231918]
35. Morris, R.L.; Hollenbeck, P.J. The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J. Cell Sci., 1993, 104(Pt 3), 917-927 [PMID: 8314882]
36. Attwell, D.; Laughlin, S.B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab., 2001, 21(10), 1133-1145 [http://dx.doi.org/10.1097/00004647-200110000-00001] [PMID: 11598490]
37. Verstreken, P.; Ly, C.V.; Venken, K.J.; Koh, T.W.; Zhou, Y.; Bellen, H.J. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron, 2005, 47(3), 365-378 [http://dx.doi.org/10.1016/j.neuron.2005.06.018] [PMID: 16055061]
38. Stefani, G.; Onofri, F.; Valtorta, F.; Vaccaro, P.; Greengard, P.; Benfenati, F. Kinetic analysis of the phosphorylation-dependent interactions of synapsin I with rat brain synaptic vesicles. J. Physiol., 1997, 504(Pt 3), 501-515 [http://dx.doi.org/10.1111/j.1469-7793.1997.501bd.x] [PMID: 9401959]
39. Cunha, R.A.; Vizi, E.S.; Ribeiro, J.A.; Sebastião, A.M. Preferential release of ATP and its extracellular catabolism as a source of adenosine upon high-but not low-frequency stimulation of rat hippocampal slices. J. Neurochem., 1996, 67(5), 2180-2187 [http://dx.doi.org/10.1046/j.1471-4159.1996.67052180.x] [PMID: 8863529]
40. Trenkner, E.; el Idrissi, A.; Harris, C. Balanced interaction of growth factors and taurine regulate energy metabolism, neuronal survival, and function of cultured mouse cerebellar cells under depolarizing conditions. Adv. Exp. Med. Biol., 1996, 403, 507-517 [http://dx.doi.org/10.1007/978-1-4899-0182-8_55] [PMID: 8915389]
41. Mattson, M.P.; Lovell, M.A.; Furukawa, K.; Markesbery, W.R. Neurotrophic factors attenuate glutamate-induced accumulation of peroxides, elevation of intracellular Ca2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J. Neurochem., 1995, 65(4), 1740-1751 [http://dx.doi.org/10.1046/j.1471-4159.1995.65041740.x] [PMID: 7561872]
42. Roberson, E.D.; English, J.D.; Adams, J.P.; Selcher, J.C.; Kondratick, C.; Sweatt, J.D. The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J. Neurosci., 1999, 19(11), 4337-4348 [PMID: 10341237]
43. Schuchmann, S.; Buchheim, K.; Heinemann, U.; Hosten, N.; Buttgereit, F. Oxygen consumption and mitochondrial membrane potential indicate developmental adaptation in energy metabolism of rat cortical neurons. Eur. J. Neurosci., 2005, 21(10), 2721-2732 [http://dx.doi.org/10.1111/j.1460-9568.2005.04109.x] [PMID: 15926920]
44. Lu, B.; Wang, K.H.; Nose, A. Molecular mechanisms underlying neural circuit formation. Curr. Opin. Neurobiol., 2009, 19(2), 162-167 [http://dx.doi.org/10.1016/j.conb.2009.04.004] [PMID: 19457653]
45. Burkhalter, J.; Fiumelli, H.; Allaman, I.; Chatton, J.Y.; Martin, J.L. Brain-derived neurotrophic factor stimulates energy metabolism in developing cortical neurons. J. Neurosci., 2003, 23(23), 8212-8220 [PMID: 12967982]
46. Markham, A.; Cameron, I.; Franklin, P.; Spedding, M. BDNF increases rat brain mitochondrial respiratory coupling at complex I, but not complex II. Eur. J. Neurosci., 2004, 20(5), 1189-1196 [http://dx.doi.org/10.1111/j.1460-9568.2004.03578.x] [PMID: 15341590]
47. Markham, A.; Cameron, I.; Bains, R.; Franklin, P.; Kiss, J.P.; Schwendimann, L.; Gressens, P.; Spedding, M. Brain-derived neurotrophic factor-mediated effects on mitochondrial respiratory coupling and neuroprotection share the same molecular signalling pathways. Eur. J. Neurosci., 2012, 35(3), 366-374 [http://dx.doi.org/10.1111/j.1460-9568.2011.07965.x] [PMID: 22288477]
48. Dunwiddie, T.; Madison, D.; Lynch, G. Synaptic transmission is required for initiation of long-term potentiation. Brain Res., 1978, 150(2), 413-417 [http://dx.doi.org/10.1016/0006-8993(78)90293-7] [PMID: 209851]
49. Lynch, G.; Larson, J.; Kelso, S.; Barrionuevo, G.; Schottler, F. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature, 1983, 305(5936), 719-721 [http://dx.doi.org/10.1038/305719a0] [PMID: 6415483]
50. Baimbridge, K.G.; Miller, J.J. Calcium uptake and retention during long-term potentiation of neuronal activity in the rat hippocampal slice preparation. Brain Res., 1981, 221(2), 299-305 [http://dx.doi.org/10.1016/0006-8993(81)90779-4] [PMID: 7284771]
51. Thayer, S.A.; Miller, R.J. Regulation of the intracellular free calcium concentration in single rat dorsal root ganglion neurones in vitro. J. Physiol., 1990, 425, 85-115 [http://dx.doi.org/10.1113/jphysiol.1990.sp018094] [PMID: 2213592]
52. Delaney, K.R.; Tank, D.W. A quantitative measurement of the dependence of short-term synaptic enhancement on presynaptic residual calcium. J. Neurosci., 1994, 14(10), 5885-5902 [PMID: 7931551]
53. Yang, F.; He, X.P.; Russell, J.; Lu, B. Ca2+ influx-independent synaptic potentiation mediated by mitochondrial Na(+)-Ca2+ exchanger and protein kinase C. J. Cell Biol., 2003, 163(3), 511-523 [http://dx.doi.org/10.1083/jcb.200307027] [PMID: 14610054]
54. Weeber, E.J.; Levy, M.; Sampson, M.J.; Anflous, K.; Armstrong, D.L.; Brown, S.E.; Sweatt, J.D.; Craigen, W.J. The role of mitochondrial porins and the permeability transition pore in learning and synaptic plasticity. J. Biol. Chem., 2002, 277(21), 18891-18897 [http://dx.doi.org/10.1074/jbc.M201649200] [PMID: 11907043]
55. Levy, M.; Faas, G.C.; Saggau, P.; Craigen, W.J.; Sweatt, J.D. Mitochondrial regulation of synaptic plasticity in the hippocampus. J. Biol. Chem., 2003, 278(20), 17727-17734 [http://dx.doi.org/10.1074/jbc.M212878200] [PMID: 12604600]
56. Bindokas, V.P.; Lee, C.C.; Colmers, W.F.; Miller, R.J. Changes in mitochondrial function resulting from synaptic activity in the rat hippocampal slice. J. Neurosci., 1998, 18(12), 4570-4587 [PMID: 9614233]
57. Foy, M.R.; Baudry, M.; Diaz Brinton, R.; Thompson, R.F. Estrogen and hippocampal plasticity in rodent models. J. Alzheimers Dis., 2008, 15(4), 589-603 [PMID: 19096158]
58. Harooni, H.E.; Naghdi, N.; Sepehri, H.; Rohani, A.H. The role of hippocampal nitric oxide (NO) on learning and immediate, shortand long-term memory retrieval in inhibitory avoidance task in male adult rats. Behav. Brain Res., 2009, 201(1), 166-172 [http://dx.doi.org/10.1016/j.bbr.2009.02.011] [PMID: 19428630]
59. Minichiello, L. TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci., 2009, 10(12), 850-860 [http://dx.doi.org/10.1038/nrn2738] [PMID: 19927149]
60. Brinton, R.D. Estrogen-induced plasticity from cells to circuits: predictions for cognitive function. Trends Pharmacol. Sci., 2009, 30(4), 212-222 [http://dx.doi.org/10.1016/j.tips.2008.12.006] [PMID: 19299024]
61. Gutsaeva, D.R.; Carraway, M.S.; Suliman, H.B.; Demchenko, I.T.; Shitara, H.; Yonekawa, H.; Piantadosi, C.A. Transient hypoxia stimulates mitochondrial biogenesis in brain subcortex by a neuronal nitric oxide synthase-dependent mechanism. J. Neurosci., 2008, 28(9), 2015-2024 [http://dx.doi.org/10.1523/JNEUROSCI. 5654-07.2008] [PMID: 18305236]
62. Klinge, C.M. Estrogenic control of mitochondrial function and biogenesis. J. Cell. Biochem., 2008, 105(6), 1342-1351 [http://dx.doi.org/10.1002/jcb.21936] [PMID: 18846505]
63. Renton, J.P.; Xu, N.; Clark, J.J.; Hansen, M.R. Interaction of neurotrophin signaling with Bcl-2 localized to the mitochondria and endoplasmic reticulum on spiral ganglion neuron survival and neurite growth. J. Neurosci. Res., 2010, 88(10), 2239-2251 [http://dx.doi.org/10.1002/jnr.22381] [PMID: 20209634]
64. Burke, S.N.; Barnes, C.A. Senescent synapses and hippocampal circuit dynamics. Trends Neurosci., 2010, 33(3), 153-161 [http://dx.doi.org/10.1016/j.tins.2009.12.003] [PMID: 20071039]
65. Foster, T.C. Challenges and opportunities in characterizing cognitive aging across species. Front. Aging Neurosci., 2012, 4, 33 [http://dx.doi.org/10.3389/fnagi.2012.00033] [PMID: 23189053]
66. Barnes, C.A. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol., 1979, 93(1), 74-104 [http://dx.doi.org/10.1037/h0077579] [PMID: 221551]
67. Landfield, P.W.; Lynch, G. Impaired monosynaptic potentiation in in vitro hippocampal slices from aged, memory-deficient rats. J. Gerontol., 1977, 32(5), 523-533 [http://dx.doi.org/10.1093/geronj/32.5.523] [PMID: 196001]
68. Burgdorf, J.; Zhang, X.L.; Weiss, C.; Matthews, E.; Disterhoft, J.F.; Stanton, P.K.; Moskal, J.R. The N-methyl-D-aspartate receptor modulator GLYX-13 enhances learning and memory, in young adult and learning impaired aging rats. Neurobiol. Aging, 2011, 32(4), 698-706 [http://dx.doi.org/10.1016/j.neurobiolaging. 2009.04.012] [PMID: 19446371]
69. Lister, J.P.; Barnes, C.A. Neurobiological changes in the hippocampus during normative aging. Arch. Neurol., 2009, 66(7), 829-833 [http://dx.doi.org/10.1001/archneurol.2009.125] [PMID: 19597084]
70. Dorszewska, J. Cell biology of normal brain aging: synaptic plasticity-cell death. Aging Clin. Exp. Res., 2013, 25(1), 25-34 [http://dx.doi.org/10.1007/s40520-013-0004-2] [PMID: 23740630]
71. Toescu, E.C.; Verkhratsky, A. Ca2+ and mitochondria as substrates for deficits in synaptic plasticity in normal brain ageing. J. Cell. Mol. Med., 2004, 8(2), 181-190 [http://dx.doi.org/10.1111/j.1582-4934.2004.tb00273.x] [PMID: 15256066]
72. Barnes, C.A.; McNaughton, B.L. An age comparison of the rates of acquisition and forgetting of spatial information in relation to longterm enhancement of hippocampal synapses. Behav. Neurosci., 1985, 99(6), 1040-1048 [http://dx.doi.org/10.1037/0735-7044.99.6. 1040] [PMID: 3843538]
73. Troulinaki, K.; Bano, D. Mitochondrial deficiency: a double-edged sword for aging and neurodegeneration. Front. Genet., 2012, 3, 244 [http://dx.doi.org/10.3389/fgene.2012.00244] [PMID: 23248639]
74. Schon, E.A.; Przedborski, S. Mitochondria: the next (neurode) generation. Neuron, 2011, 70(6), 1033-1053 [http://dx.doi.org/10.1016/j.neuron.2011.06.003] [PMID: 21689593]
75. Toescu, E.C.; Myronova, N.; Verkhratsky, A. Age-related structural and functional changes of brain mitochondria. Cell Calcium, 2000, 28(5-6), 329-338 [http://dx.doi.org/10.1054/ceca.2000.0167] [PMID: 11115372]
76. Gilmer, L.K.; Ansari, M.A.; Roberts, K.N.; Scheff, S.W. Agerelated changes in mitochondrial respiration and oxidative damage in the cerebral cortex of the Fischer 344 rat. Mech. Ageing Dev., 2010, 131(2), 133-143 [http://dx.doi.org/10.1016/j.mad.2009.12.011] [PMID: 20080122]
77. Yin, F.; Jiang, T.; Cadenas, E. Metabolic triad in brain aging: mitochondria, insulin/IGF-1 signalling and JNK signalling. Biochem. Soc. Trans., 2013, 41(1), 101-105 [http://dx.doi.org/10.1042/BST20120260] [PMID: 23356266]
78. Sedelnikova, O.A.; Horikawa, I.; Zimonjic, D.B.; Popescu, N.C.; Bonner, W.M.; Barrett, J.C. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat. Cell Biol., 2004, 6(2), 168-170 [http://dx.doi.org/10.1038/ncb1095] [PMID: 14755273]
79. Brawek, B.; Löffler, M.; Wagner, K.; Huppertz, H.J.; Wendling, A.S.; Weyerbrock, A.; Jackisch, R.; Feuerstein, T.J. Reactive oxygen species (ROS) in the human neocortex: role of aging and cognition. Brain Res. Bull., 2010, 81(4-5), 484-490 [http://dx.doi.org/10.1016/j.brainresbull.2009.10.011] [PMID: 19854245]
80. Sastre, J.; Pallardó, F.V.; Viña, J. Mitochondrial oxidative stress plays a key role in aging and apoptosis. IUBMB Life, 2000, 49(5), 427-435 [http://dx.doi.org/10.1080/152165400410281] [PMID: 10902575]
81. Indo, H.P.; Davidson, M.; Yen, H.C.; Suenaga, S.; Tomita, K.; Nishii, T.; Higuchi, M.; Koga, Y.; Ozawa, T.; Majima, H.J. Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion, 2007, 7(1-2), 106-118 [http://dx.doi.org/10.1016/j.mito.2006.11.026] [PMID: 17307400]
82. Nicholls, D.G.; Vesce, S.; Kirk, L.; Chalmers, S. Interactions between mitochondrial bioenergetics and cytoplasmic calcium in cultured cerebellar granule cells. Cell Calcium, 2003, 34(4-5), 407-424 [http://dx.doi.org/10.1016/S0143-4160(03)00144-1] [PMID: 12909085]
83. Toescu, E.C.; Verkhratsky, A. Neuronal ageing from an intraneuronal perspective: roles of endoplasmic reticulum and mitochondria. Cell Calcium, 2003, 34(4-5), 311-323 [http://dx.doi.org/10.1016/S0143-4160(03)00142-8] [PMID: 12909078]
84. Gunter, T.E.; Buntinas, L.; Sparagna, G.; Eliseev, R.; Gunter, K. Mitochondrial calcium transport: mechanisms and functions. Cell Calcium, 2000, 28(5-6), 285-296 [http://dx.doi.org/10.1054/ceca.2000.0168] [PMID: 11115368]
85. Toescu, E.C.; Verkhratsky, A. Assessment of mitochondrial polarization status in living cells based on analysis of the spatial heterogeneity of rhodamine 123 fluorescence staining. Pflugers Arch., 2000, 440(6), 941-947 [http://dx.doi.org/10.1007/s004240000390] [PMID: 11041562]
86. Xiong, J.; Verkhratsky, A.; Toescu, E.C. Changes in mitochondrial status associated with altered Ca2+ homeostasis in aged cerebellar granule neurons in brain slices. J. Neurosci., 2002, 22(24), 10761-10771 [PMID: 12486169]
87. Li, Y.C.; Zhai, X.Y.; Ohsato, K.; Futamata, H.; Shimada, O.; Atsumi, S. Mitochondrial accumulation in the distal part of the initial segment of chicken spinal motoneurons. Brain Res., 2004, 1026(2), 235-243 [http://dx.doi.org/10.1016/j.brainres.2004. 08.016] [PMID: 15488485]