Abstract
The mitochondria of different cells are different in their morphological and biochemical properties. These organelles generate free radicals during activity, leading inevitably to mitochondrial DNA damage. It is not clear how this problem is addressed in long-lived cells, such as neurons. We propose the hypothesis that mitochondria within the same cell also differ in lifespan and ability to divide. According to our suggestion, cells have a pool of ‘stem’ mitochondria with low metabolic activity and a pool of ‘differentiated’ mitochondria with significantly shorter lifespans and high metabolic activity. We consider synaptic mitochondria as a possible example of ‘differentiated’ mitochondria. They are significantly smaller than mitochondria from the cell body, and they are different in key enzyme activity levels, proteome, and lipidome. Synaptic mitochondria are more sensitive to different damaging factors. It has been established that neurons have a sorting mechanism that sends mitochondria with high membrane potential to presynaptic endings. This review describes the properties of synaptic mitochondria and their role in the regulation of synaptic transmission.
References
Aitken, P.G. and Braitman, D.J. (1989). The effects of cyanide on neural and synaptic function in hippocampal slices. Neurotoxicology 10, 239–247.Search in Google Scholar
Almeida, A., Almeida, J., Bolanos, J.P., and Moncada, S. (2001). Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically-generated ATP in astrocytes protection. Proc. Natl. Acad. Sci. U.S.A. 98, 15294–15299.10.1073/pnas.261560998Search in Google Scholar
Arora, K.K. and Pedersen, P.L. (1988). Functional significance of mitochondrial bound hexokinase in tumor cell metabolism. Evidence for preferential phosphorylation of glucose by intramitochondrially generated ATP. Am. Soc. Biochem. Mol. Biol. 263, 17422–17428.10.1016/S0021-9258(19)77853-3Search in Google Scholar
Ashrafi, G., Schlehe, J.S., LaVoie, J.L., and Schwarz, T.L. (2014). Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J. Cell Biol. 206, 665–670.10.1083/jcb.201401070Search in Google Scholar PubMed PubMed Central
Attwell, D. and Gibb, A. (2005). Neuroenergetic and the kinetic design of excitatory synapses. Nat. Rev. Neurosci. 6, 841–849.10.1038/nrn1784Search in Google Scholar PubMed
Attwell, D. and Laughlin, S.B. (2001). An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 21, 1133–1145.10.1097/00004647-200110000-00001Search in Google Scholar PubMed
Bao, L., Avshalumov, M.V., and Rice, M.E. (2005). Partial mitochondrial inhibition causes striatal dopamine release suppression and medium spiny neuron depolarization via H2O2 elevation, not ATP depletion. J. Neurochem. 25, 10029–10040.10.1523/JNEUROSCI.2652-05.2005Search in Google Scholar PubMed PubMed Central
Benard, G., Bellance, N., James, D., Parrone, P., Fernandez, H., Letellier, T., and Rossignol, R. (2007). Mitochondrial bioenergetics and structural network organization. J. Cell Sci. 120, 838–848.10.1242/jcs.03381Search in Google Scholar PubMed
Billups, B. and Forsythe, I.D. (2002). Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J. Neurosci. 22, 5840–5847.10.1523/JNEUROSCI.22-14-05840.2002Search in Google Scholar
Bolanos, J.P., Almeida, A., and Moncada, S. (2010). Glycolosis: a bioenergetic or a survival pathway? Trends Biochem. Sci. 35, 145–149.10.1016/j.tibs.2009.10.006Search in Google Scholar PubMed
Brown, M.B., Sullivan, P.G., and Geddes, J.W. (2006). Synaptic mitochondria are more susceptible to Ca2+ overload than nonsynaptic mitochondria. J. Biol. Chem. 281, 11658–11668.10.1074/jbc.M510303200Search in Google Scholar PubMed
Cai, Q. and Tammineni, P. (2016). Alterations in mitochondrial quality control in Alzheimer’s disease. Front. Cell. Neurosci. 10, 24.10.3389/fncel.2016.00024Search in Google Scholar
Cai, Q., Zakaria, H.M., Simone, A., and Sheng, Z.H. (2012). Spatial parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr. Biol. 22, 545–552.10.1016/j.cub.2012.02.005Search in Google Scholar
Cagalinec, M., Safiulina, D., Liiv, M., Liiv, J., Choubey, V., Wareski, P., Veksler, V., and Kaasik, A. (2013). Principles of the mitochondrial fusion and fission cycle in neurons. J. Cell Sci. 126, 2187–2197.10.1242/jcs.118844Search in Google Scholar
Carafoli, E. (2003). Historical review: mitochondria and calcium: ups and downs of an unusual relationship. Trends Biochem. Sci. 28, 175–181.10.1016/S0968-0004(03)00053-7Search in Google Scholar
Castegna, A., Lauderback, C.M., Mohmmad-Abdul, H., and Butterfield, D.A. (2004). Modulation of phospholipid asymmetry in synaptosomal membranes by the lipid peroxidation products, 4-hydroxynonenal and acrolein: implications for Alzheimer’s disease. Brain Res. 1004, 193–197.10.1016/j.brainres.2004.01.036Search in Google Scholar PubMed
Castro, M.A., Beltran, F.A., Brauchi, S., and Concha, I.I. (2009). A metabolic switch in brain: glucose and lactate metabolism modulation by ascorbic acid. J. Neurochem. 110, 423–440.10.1111/j.1471-4159.2009.06151.xSearch in Google Scholar PubMed
Chung, W.S., Clarke, L.E., Wang, G.X., Stafford, B.K., Sher, A., Chakraborty, C., Joung, J., Foo, L.C., Thompson, A., Chen, C., et al. (2013). Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature 504, 394–400.10.1038/nature12776Search in Google Scholar PubMed PubMed Central
Cobine, P.A., Ojeda, L.D., Rigby, K.M., and Winge, D.R. (2004). Yeast contain a non-proteinaceous pool of copper in the mitochondrial matrix. J. Biol. Chem. 279, 14447–14455.10.1074/jbc.M312693200Search in Google Scholar PubMed
Cobine, P.A., Pierrel, F., Bestwick, M.L., and Winge, D.R. (2006). Mitochondrial matrix copper complex used in metallation of cytochrome oxidase and superoxide dismutase. J. Biol. Chem. 281, 36552–36559.10.1074/jbc.M606839200Search in Google Scholar PubMed
Copeland, W.C. and Longley, M.J. (2014). Mitochondrial genome maintenance in health and disease. DNA Rep. (Amsterdam) 19, 190–198.10.1016/j.dnarep.2014.03.010Search in Google Scholar PubMed PubMed Central
Costa, C., Belcastro, V., Tozzi, A., Di Filippo, M., Siliguini, S., Autuori, A., Picconi, B., Fedele, E., Pittaluga, A., Raiteri, M., et al. (2008). Electrophysiology and pharmacology of striatal neuronal dysfunction induced by mitochondrial complex I inhibition. J. Neurosci. 28, 8040–8052.10.1523/JNEUROSCI.1947-08.2008Search in Google Scholar PubMed PubMed Central
Dagani, F., Gorini, A., Polgatti, M., Villa, R.F., and Benzi, G. (1983). Rat cortex synaptic and nonsynaptic mitochondria: enzymatic characterization and pharmacological effects of naftidrofuryl. J. Neurosci. Res. 10, 135–140.10.1002/jnr.490100203Search in Google Scholar PubMed
Davey, G.P., Canevari, L., and Clark, J.B. (1997). Threshold effects in synaptosomal and nonsynaptic mitochondria from hippocampal CA1 and paramedian neocortex brain regions. J. Neurochem. 69, 2564–2570.10.1046/j.1471-4159.1997.69062564.xSearch in Google Scholar PubMed
Davis, C.H., Kim, K.Y., Bushong, E.A., Milis, E.A., Boassa, D., Shih, T., Kinebuchi, M., Phan, S., Zhou, Y., Bihlmeyer, N.A., et al. (2014). Transcellular degradation of axonal mitochondria. Proc. Natl. Acad. Sci. USA 111, 9633–9638.10.1073/pnas.1404651111Search in Google Scholar PubMed PubMed Central
De Rasmo, D., Signorile, A., Roca, E., and Papa, S. (2009). cAMP response element-binding protein (CREB) is imported into mitochondria and promotes protein synthesis. FEBS J. 276, 4325–4333.10.1111/j.1742-4658.2009.07133.xSearch in Google Scholar PubMed
De Robertis, E.D. and Bennett, H.S. (1955). Some features of the submicroscopic morphology of synapses in frog and earthworm. J. Biophys. Biochem. Cytol. 1, 47–58.10.1083/jcb.1.1.47Search in Google Scholar PubMed PubMed Central
DeKosky, S.T., Scheff, S.W., and Styren, S.D. (1996). Structural correlates of cognition in dementia: quantification and assessment of synaptic charge. Neurodegeneration 5, 417–421.10.1006/neur.1996.0056Search in Google Scholar PubMed
Desmukh, D.R., Owen, O.E., and Patel, M.S. (1980). Effect of aging on the metabolism of pyruvate and 3-hydroxybutyrate in nonsynaptic and synaptic mitochondria from rat brain. J. Neurochem. 34, 1219–1224.10.1111/j.1471-4159.1980.tb09962.xSearch in Google Scholar PubMed
Diaz-Ruiz, R., Averet, N., Araiza, D., Pinson, B., Uribe-Carvajal, S., Devin, A., and Rigoulet, M. (2008). Mitochondrial oxidative phosphorylation is regulated by fructose 1,6-bisphosphate. A possible role in Crabtree effect induction? J. Biol. Chem. 283, 26948–26955.10.1074/jbc.M800408200Search in Google Scholar PubMed
Du, H., Guo, L., Yan, S., Sosunov, A.A., McKhann, G.M., and Yan, S.S.D. (2010). Early deficits in synaptic mitochondria in an Alzheimer’s disease mouse model. Proc. Natl. Acad. Sci. USA 107, 18670–18675.10.1073/pnas.1006586107Search in Google Scholar PubMed PubMed Central
Dubinski, J.M. (2009). Heterogenity of nervous system mitochondria: location, location, location! Exp. Neurol. 218, 293–307.10.1016/j.expneurol.2009.05.020Search in Google Scholar PubMed
Duncan, T., Trewick, S.C., Koivisto, P., Bates, P.A., Lindahl, T., and Sedgwick, B. (2002). Reversal of DNA alkylation damage by two human dioxygenases. Proc. Natl. Acad. Sci. U.S.A. 99, 16660–16665.10.1073/pnas.262589799Search in Google Scholar PubMed PubMed Central
Dunkley, P.R., Jarvie, P.E., and Robinson, P.J. (2008). A rapid percoll gradient procedure for preparation of synaptosomes. Nat. Protocols 3, 1718–1728.10.1038/nprot.2008.171Search in Google Scholar PubMed
Ericson, N.G., Kulawiec, M., Vermulst, M., Sheahan, K., O’Sullivan, J., Salk, J.J., and Bielas, J.H. (2012). Decreased mitochondrial DNA mutagenesis in human colorectal cancer. PLoS Genet. 8, e1002689.10.1371/journal.pgen.1002689Search in Google Scholar PubMed PubMed Central
Fedorovich, S.V., Aksentsev, S.L., and Konev, S.V. (1996). Acidosis inhibits calcium accumulation in intrasynaptosomal mitochondria. Acta Neurobiol. Exp. 56, 703.10.55782/ane-1996-1175Search in Google Scholar
Finkel, T., Menazza, S., Holmstrom, K.M., Parks, R.J., Liu, J., Sun, J., Liu, J., Pan, X., and Murphy, E. (2015). The ins and outs of mitochondrial calcium. Circ. Res. 116, 1810–1819.10.1161/CIRCRESAHA.116.305484Search in Google Scholar PubMed PubMed Central
Fogg, V.C., Lanning, N.J., and Mackeigan, J.P. (2011). Mitochondria in cancer: at the crossroads of life and death. Chin. J. Cancer. 30, 526–539.10.5732/cjc.011.10018Search in Google Scholar PubMed PubMed Central
Fujiwara, T. and Harigae, H. (2015). Biology of heme in mammalian erythroid cells and related disorders. Biomed. Res. Int. 2015:278536.10.1155/2015/278536Search in Google Scholar PubMed PubMed Central
Gazit, N., Vertkin, I., Shapira, I., Helm, M., Slomowitz, E., Sheiba, M., Mor, Y., Rizzoli, S., and Slutsky, I. (2016). IGF-1 receptor differentially regulates spontaneous and evoked transmission via mitochondria at hippocampal synapses. Neuron 89, 583–597.10.1016/j.neuron.2015.12.034Search in Google Scholar PubMed PubMed Central
Giminez-Cassina, A., Martinez-Francois, J.R., Fisher, J.K., Szlyk, B., Polak, K., Wiwczar, J., Tanner, G.R., Lutas, A., Yellen, G., and Danial, N.N. (2012). BAD-dependent regulation of fuel metabolism and KATP channel activity confers resistance to epileptic seizures. Neuron 74, 719–730.10.1016/j.neuron.2012.03.032Search in Google Scholar PubMed PubMed Central
Gray, E.G. and Whittaker, V.P. (1962). The isolation of nerve endings from brain: an electron-microscopic study of cell fragments derived by homogenization and centrifugation. J. Anat. 96, 79–88.Search in Google Scholar
Guzun, R., Kaambre, T., Bagur, R., Grichine, A., Usson, Y., Varikmaa, M., Anmann, T., Tepp, K., Timohhina, N., Shevchuk, I., et al. (2015). Modular organization of cardiac energy metabolism: energy conversion, transfer and feedback regulation. Acta Physiol. (Oxford) 213, 84–106.10.1111/apha.12287Search in Google Scholar PubMed PubMed Central
Haag, S., Sloan, K.E., Ranjan, N., Warda, A.S., Kretschmer, J., Blessing, C., Hubner, B., Seikowski, J., Dennerlein, S., Rehling, P., et al. (2016). NSUN3 and ABH1 modify the wobble position of mt-tRNAMet to expand codon recognition in mitochondrial translation. EMBO J. 35, 2104–2119.10.15252/embj.201694885Search in Google Scholar
Hagen, T.M., Yowe, D.L., Bartholomew, J.C., Wehr, C.M., Do, K.L., Park, J.Y., and Ames, B.N. (1997). Mitochondrial decay in hepatocytes from old rats: membrane potential declines, heterogeneity and oxidants increase. Proc. Natl. Acad. Sci. U.S.A. 94, 3064–3069.10.1073/pnas.94.7.3064Search in Google Scholar
Hajos, F. (1975). An improved method for the preparation of synaptosomal fractions in high purity. Brain Res. 93, 485–489.10.1016/0006-8993(75)90186-9Search in Google Scholar
Hara, Y., Yuk, F., Puri, R., Janssen, W.G.M., Rapp, P.R., and Morrison, J.H. (2014). Presynaptic mitochondrial morphology in monkey prefrontal cortex correlates with working memory and is improved with estrogen treatment. Proc. Natl. Acad. Sci. U.S.A. 111, 486–491.10.1073/pnas.1311310110Search in Google Scholar PubMed PubMed Central
Harris, J.J., Jolivet, R., and Attwell, D. (2012). Synaptic energy use and supply. Neuron 75, 762–777.10.1016/j.neuron.2012.08.019Search in Google Scholar PubMed
Herrero-Mendez, A., Almeida, A., Fernandez, E., Maestre, C., Moncada, S., and Bolanos, J.P. (2009). The bioenergetic and antioxidants status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat. Cell Biol. 11, 747–752.10.1038/ncb1881Search in Google Scholar PubMed
Hong, S., Dissing-Oleson, L., and Stevens, B. (2016). New insights on the role of microglia in synaptic pruning in health and disease. Curr. Opin. Neurobiol. 36, 128–134.10.1016/j.conb.2015.12.004Search in Google Scholar PubMed PubMed Central
Hrynevich, S.V., Waseem, T.V., Hebert, A., Pellerin, L., Fedorovich, S.V. (2016). β-hydroxybutyrate supports synaptic vesicle cycling but reduces endocytosis and exocytosis in rat brain synaptosomes. Neurochem. Int. 93, 73–81.10.1016/j.neuint.2015.12.014Search in Google Scholar PubMed
Huster, D., Finegold, M.J., Morgan, C.T., Burkhead, J.L., Nixon, R., Vanderwerf, S.M., Gilliam, C.T., and Lutsenko, S. (2006). Consequences of copper accumulation in the livers of the Atp7b-/- (Wilson disease gene) knockout mice. Am. J. Pathol. 168, 423–434.10.2353/ajpath.2006.050312Search in Google Scholar PubMed PubMed Central
Ikemoto, A., Bole, D.G., and Ueda, T. (2003). Glycolysis and glutamate accumulation into synaptic vesicles. Role of glyceraldehyde phosphate dehydrogenase and 3-phosphoglycerate kinase. J. Biol. Chem. 278, 5929–5940.10.1074/jbc.M211617200Search in Google Scholar PubMed
Ivannikov, M.V., Sugimori, M., and Llinas, R.R. (2013). Synaptic vesicle exocytosis in hippocampal synaptosomes correlates directly with total mitochondrial volume. J. Mol. Neurosci. 49, 223–230.10.1007/s12031-012-9848-8Search in Google Scholar PubMed PubMed Central
Johnson, D.T., Harris, R.A¯, Blair, P.V., and Balaban, R.S. (2007a). Functional consequences of mitochondrial proteome heterogeneity. Am. J. Physiol. Cell. Physiol. 292, C698–C707.10.1152/ajpcell.00109.2006Search in Google Scholar PubMed
Johnson, D.T., Johnson, D.T., Harris, R.A., French, S., Blair, P.V., You, J., Bemis, K.G., Wang, M., and Balaban, R.S. (2007b). Tissue heterogeneity of the mammalian mitochondrial proteome. Am. J. Physiol. Cell. Physiol. 292, C689–C697.10.1152/ajpcell.00108.2006Search in Google Scholar PubMed
Kaasik, A., Saifiulina, D., Choubey, V., Kuum, V., Zharkovsky, A., and Veksler, V. (2007). Mitochondrial swelling impairs the transport of organelles in cerebellar granule neurons. J. Biol. Chem. 282, 32821–32826.10.1074/jbc.M702295200Search in Google Scholar PubMed
Kamer, K.J. and Mootha, V.K. (2015). The molecular era of the mitochondrial calcium uniporter. Nature Rev. Mol. Cell. Biol. 16, 545–553.10.1038/nrm4039Search in Google Scholar PubMed
Kanabus, M., Heales, S.J., and Rahman, S. (2014). Development of pharmacological strategies for mitochondrial disorders. Br. J. Pharmacol. 171, 1798–1817.10.1111/bph.12456Search in Google Scholar PubMed PubMed Central
Kennedy, S.R., Salk, J.J., Schmitt, M.W., and Loeb, L.A. (2013). Ultra-sensitive sequencing reveals an age-related increase in somatic mitochondrial mutations that are inconsistent with oxidative damage. PLoS Genet. 9, e1003794.10.1371/journal.pgen.1003794Search in Google Scholar PubMed PubMed Central
Kenney, G.E. and Rosenzweig, A.C. (2012). Chemistry and biology of the copper chelator methanobactin. ACS Chem. Biol. 7, 260–268.10.1021/cb2003913Search in Google Scholar PubMed PubMed Central
Kiebish, M.A., Han, X., Cheng, H., Lunceford, A., Clarke, C.F., Moon, H., Chuang, J.H., and Seyfried, T.N. (2008). Lipidomic analysis and electron transport chain activities in C57BL/6J mouse brain mitochondria. J. Neurochem. 106, 299–312.10.1111/j.1471-4159.2008.05383.xSearch in Google Scholar PubMed PubMed Central
Knott, A.B., Perkins, G., Schwarzenbacher, R., and Bossy-Wetzel, E. (2008). Mitochondrial fragmentation in neurodegeneration. Nat. Rev. Neurosci. 9, 505–518.10.1038/nrn2417Search in Google Scholar PubMed PubMed Central
Kroemer, G., Galuzzi, L., and Brenner, C. (2007). Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87, 99–163.10.1152/physrev.00013.2006Search in Google Scholar PubMed
Lai, J.C.K. and Clark, J.B. (1976). Preparation and properties of mitochondria derived from synaptosomes. Biochem. J. 154, 423–432.10.1042/bj1540423Search in Google Scholar PubMed PubMed Central
Lai, J.C.K., Walsh, J.M., Dennis, S.C., and Clark, J.B. (1977). Synaptic and non-synaptic mitochondria from rat brain: isolation and characterization. J. Neurochem. 28, 625–631.10.1111/j.1471-4159.1977.tb10434.xSearch in Google Scholar PubMed
Lang, F., Lang, K.S., Lang, P.A., Huber, S.M., and Wieder, T. (2006). Mechanism and significance of eryptosis. Antioxid. Redox Signal. 8, 1183–1192.10.1089/ars.2006.8.1183Search in Google Scholar PubMed
Lang, F., Gulbins, E., Lerche, H., Huber, S.M., Kempe, D.S., and Foller, M. (2008). Eryptosis, a window to systemic disease. Cell Physiol. Biochem. 22, 373–380.10.1159/000185448Search in Google Scholar PubMed
Leary, S.C., Winge, D.R., and Cobine, P.A. (2009). “Pulling the plug” on cellular copper: the role of mitochondria in copper export. Biochim. Biophys. Acta 1793, 146–153.10.1016/j.bbamcr.2008.05.002Search in Google Scholar PubMed PubMed Central
Lemasters, J.J. (2014). Variants of mitochondrial autophagy: types 1 and 2 mitophagy and micromitophagy (type 3). Redox Biol. 2:749–754.10.1016/j.redox.2014.06.004Search in Google Scholar PubMed PubMed Central
Leong, S.F., Lai, J.C.K., Lim, L., and Clark, J.B. (1984). The activities of some energy-metabolizing enzymes in nonsynaptic (free) and synaptic mitochondria derived from selected brain regions. J. Neurochem. 42, 1306–1312.10.1111/j.1471-4159.1984.tb02788.xSearch in Google Scholar PubMed
Li, Z., Okamoto, K.-I., Hayashi, Y., and Sheng, M. (2004). The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119, 873–887.10.1016/j.cell.2004.11.003Search in Google Scholar PubMed
Li, H., Alavin, K.N., Lazrove, E., Mehta, N., Jones, A., Zhang, P., Licznerski, P., Graham, M., Uo, T., Guo, J., et al. (2013). A BCL-Xl-Drp1 complex regulates synaptic vesicle membrane dynamics during endocytosis. Nat. Cell Biol. 15, 773–785.10.1038/ncb2791Search in Google Scholar PubMed PubMed Central
Li, C., Zhang, G., Zhao, L., Ma, Z., and Chen, H. (2016). Metabolic reprogramming in cancer cells: glycolysis, glutaminolysis, and Bcl-2 proteins as novel therapeutic targets for cancer. World J. Surg. Oncol. 14, 15.10.1186/s12957-016-0769-9Search in Google Scholar
Lill, R., Srinivasan, V., and Muhlenhoff, U. (2014). The role of mitochondria in cytosolic-nuclear iron–sulfur protein biogenesis and in cellular iron regulation. Curr. Opin. Microbiol. 22, 111–119.10.1016/j.mib.2014.09.015Search in Google Scholar
Lin, M.T. and Beal, M.F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787–795.10.1038/nature05292Search in Google Scholar
Lores-Arnaiz, S. and Bustamante, J. (2011). Age-related alterations in mitochondrial physiological parameters and nitric oxide production in synaptic and non-synaptic brain cortex mitochondria. Neuroscience 188, 117–124.10.1016/j.neuroscience.2011.04.060Search in Google Scholar
MacAskill, A.F., Atkin, T.A., and Kittler, J.T. (2010). Mitochondrial trafficking and the provision of energy and calcium buffering at excitatory synapses. Eur. J. Neurosci. 32, 231–240.10.1111/j.1460-9568.2010.07345.xSearch in Google Scholar
Maftah, A., Ratinaud, M.H., Dumas, M., Bont, F., Meybeck, A., and Julien, R. (1994). Human epidermal cells progressively lose their cardiolipins during ageing without change in mitochondrial transmembrane potential. Mech. Ageing Dev. 77, 83–96.10.1016/0047-6374(94)90017-5Search in Google Scholar
Marland, J.R., Hasel, P., Bonnycastle, K., and Cousin, M.A. (2016). Mitochondrial calcium uptake modulates synaptic vesicle endocytosis in central nerve terminals. J. Biol. Chem. 291, 2080–2086.10.1074/jbc.M115.686956Search in Google Scholar
Martinez, A.O., Over, D., Armstrong, L.S., Manzano, L., Taylor, R., and Chambers, J. (1991). Separation of two subpopulations of old human fibroblasts by mitochondria (rhodamine 123) fluorescence. Growth Dev. Aging 55, 185–191.Search in Google Scholar
Mattson, M.P. (2015). Late-onset dementia: a mosaic of prototypical pathologies modifiable by diet and lifestyle. Aging Mech. Dis. 1, 15003.10.1038/npjamd.2015.3Search in Google Scholar
Mattson, M.P., Gleichman, M., and Cheung, A. (2008). Mitochondria in neuroplasticity and neurological disorders. Neuron 60, 748–766.10.1016/j.neuron.2008.10.010Search in Google Scholar
McFarland, R., Taylor, R.W., and Turnbull, D.M. (2007). Mitochondrial disease – its impact, etiology and pathology. Curr. Top. Dev. Biol. 77, 113–155.10.1016/S0070-2153(06)77005-3Search in Google Scholar
McKenna, M.C., Hopkins, I.B., Lindauer, S.L., and Bamford, P. (2006). Aspartate aminotransferase in synaptic and nonsynaptic mitochondria: differential effect of compounds that influences transient hetero-enzyme complex (metabolon) formation. Neurochem. Int. 48, 629–636.10.1016/j.neuint.2005.11.018Search in Google Scholar PubMed
Mettert, E.L. and Kiley, P.J. (2015). Fe-S proteins that regulate gene expression. Biochim. Biophys. Acta. 1853, 1284–1293.10.1016/j.bbamcr.2014.11.018Search in Google Scholar PubMed PubMed Central
Miller, K.E. and Sheetz, M.P. (2004). Axonal mitochondrial transport and potential are correlated. J. Cell Sci. 117, 2791–2804.10.1242/jcs.01130Search in Google Scholar PubMed
Miyamoto, A., Wake, H., Moorhouse, A.J., and Nabekura, J. (2013). Microglia and synapse interactions: fine tuning neural circuits and candidate molecules. Front. Cell. Neurosci. 7, 70.10.3389/fncel.2013.00070Search in Google Scholar PubMed PubMed Central
Naga, K.K., Sullivan, P.G., and Geddes, J.W. (2007). High cyclophilin D content of synaptic mitochondria results in increased vulnerability to permeability transition. J. Neurosci. 27, 7469–7475.10.1523/JNEUROSCI.0646-07.2007Search in Google Scholar PubMed PubMed Central
Neifakh, S.A. and Puchkova, L.V. (1974). Letter: On the repression of mitochondrial DNA transcription by fructose 1,6-diphosphate and its derepression by cyclic adenosine 3′,5′-monophosphate. Mol. Cell. Biochem. 3, 165–168.10.1007/BF01659188Search in Google Scholar PubMed
Nicholls, D.G. (1993). The glutamatergic nerve terminals. Eur. J. Biochem. 212, 613–631.10.1007/978-3-642-78757-7_6Search in Google Scholar
Opazo, K.M., Greenough, M.A., and Bush, A.I. (2014). Copper: from neurotransmission to neuroproteostasis. Front. Aging Neurosci. 6, 143.10.3389/fnagi.2014.00143Search in Google Scholar PubMed PubMed Central
Orrenius, S., Gogvadze, V., and Zhivotovsky, B. (2015). Calcium and mitochondria in the regulation of cell death. Biochem. Biophys. Res. Commun. 460, 72–81.10.1016/j.bbrc.2015.01.137Search in Google Scholar PubMed
Pan, Z., Sikandar, S., Witherspoon, M., Dizon, D., Nguyen, T., Benirschke, K., Wiley, C., Vrana, P., and Lipkin, S.M. (2008). Impaired placental trophoblast lineage differentiation in Alkbh1-/- mice. Dev. Dyn. 237, 316–327.10.1002/dvdy.21418Search in Google Scholar PubMed
Panieri, E., Gogvadze, V., Norberg, E., Venkatesh, R., Orrenius, S., and Zhivotovsky, B. (2013). Reactive oxygen species generated in different compartments induce cell death, survival, or senescence. Free Radic. Biol. Med. 57, 176–187.10.1016/j.freeradbiomed.2012.12.024Search in Google Scholar PubMed
Parton, R.G., Simons, K., and Dotti, C.G. (1992). Axonal and dendritic endocytic pathway in cultured neurons. J. Cell. Biol. 119, 123–137.10.1083/jcb.119.1.123Search in Google Scholar PubMed PubMed Central
Patergnani, S., Missiroli, S., Marchi, S., and Giorgi, C. (2015). Mitochondria-associated endoplasmic reticulum membranes microenvironment: targeting autophagic and apoptotic pathways in cancer therapy. Front. Oncol. 5, 173.10.3389/fonc.2015.00173Search in Google Scholar PubMed PubMed Central
Pathak, D., Shields, L., Mendelsohn, B.A., Haddad, D., Lin, W., Gerencser, A.A., Kim, H., Brand, M.D., Edwards, R.H., and Nakamura, K. (2015). The role of mitochondrially derived ATP in synaptic vesicle recycling. J. Biol. Chem. 290, 22325–22336.10.1074/jbc.M115.656405Search in Google Scholar PubMed PubMed Central
Pellerin, L. and Magistretti, P. (2012). Sweet sixteen for ANLS. J. Cereb. Blood Flow Metab. 32, 1152–1166.10.1038/jcbfm.2011.149Search in Google Scholar PubMed PubMed Central
Peng, F., Lutsenko, S., Sun, X., and Muzik, O. (2012). Imaging copper metabolism imbalance in Atp7b-/- knockout mouse model of Wilson’s disease with PET-CT and orally administered 64CuCl2. Mol. Imaging Biol. 14, 600–607.10.1007/s11307-011-0532-0Search in Google Scholar PubMed
Pivovarova, N.B. and Andrews, S.B. (2010). Calcium-dependent mitochondrial function and dysfunction in neurons. FEBS J. 277, 3622–3636.10.1111/j.1742-4658.2010.07754.xSearch in Google Scholar PubMed PubMed Central
Raiteri, L. and Raiteri, M. (2000). Synaptosomes still viable after 25 years of superfusion. Neurochem. Res. 25, 1265–1274.10.1023/A:1007648229795Search in Google Scholar
Raiteri, L., Stigliani, S., Zedda, L., Raiteri, M., and Bonanno, G. (2002). Multiple mechanism of transmitter release evoked by ‘pathologically’ elevated extracellular [K+]: involvement transporter reversal and mitochondrial calcium. J. Neurochem. 80, 706–714.10.1046/j.0022-3042.2001.00750.xSearch in Google Scholar PubMed
Raiteri, L., Zapettini, S., Milanese, M., Fedele, M., Raiteri, M., and Bonanno, G. (2007). Mechanisms of glutamate release elicited in rat cerebrocortical nerve endings by ‘pathologically’ elevated extraterminal K+ concentration. J. Neurochem. 103, 952–961.10.1111/j.1471-4159.2007.04784.xSearch in Google Scholar PubMed
Rangaraju, V., Calloway, N., and Ryan, T.A. (2014). Activity-driven local ATP synthesis is required for synaptic function. Cell 156, 825–835.10.1016/j.cell.2013.12.042Search in Google Scholar PubMed PubMed Central
Rasgado-Flores, H. and Blaustein, M.P. (1987). ATP-dependent regulation of cytoplasmic free calcium in nerve terminals. Am. J. Physiol. 252, C588–C594.10.1152/ajpcell.1987.252.6.C588Search in Google Scholar PubMed
Rintoul, G.L., Filiano, A.J., Brocard, J.B., Kress, G.J., and Reynolds, I.J. (2003). Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J. Neurosci. 23, 7881–7888.10.1523/JNEUROSCI.23-21-07881.2003Search in Google Scholar
Rizzuto, R. and Pozzan, T. (2006). Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol. Rev. 86, 369–408.10.1152/physrev.00004.2005Search in Google Scholar PubMed
Rizzuto, R., De Stefani, D., Raffaello, A., and Mammucari, C. (2012). Mitochondria as sensors and regulators of calcium signaling. Nat. Rev. Mol. Cell. Biol. 13, 566–578.10.1038/nrm3412Search in Google Scholar PubMed
Scarpulla, R.C. (2012). Nucleus-encoded regulators of mitochondrial function: integration of respiratory chain expression, nutrient sensing and metabolic stress. Biochim. Biophys. Acta 1819, 1088–1097.10.1016/j.bbagrm.2011.10.011Search in Google Scholar PubMed PubMed Central
Schafer, D.P. and Stevens, B. (2013). Phagocytic glial cells: sculpting synaptic circuits in the developing nervous system. Curr. Opin. Neurobiol. 23, 1034–1040.10.1016/j.conb.2013.09.012Search in Google Scholar PubMed PubMed Central
Scheffler, I.E. (1999). Mitochondria (New York, USA: J. Willy and Sons, Inc.).10.1002/0471223891Search in Google Scholar
Shokolenko, I.N., Wilson, G.L., and Alexeyev, M.F. (2014). Aging: a mitochondrial DNA perspective, critical analysis and an update. World J. Exp. Med. 4, 46–57.10.5493/wjem.v4.i4.46Search in Google Scholar PubMed PubMed Central
Stauch, K.L., Purnell, P.R., and Fox, H.S. (2014). Quantitative proteomics of synaptic and nonsynaptic mitochondria: insights for synaptic mitochondrial vulnerability. J. Proteome Res. 13, 2620–2636.10.1021/pr500295nSearch in Google Scholar PubMed PubMed Central
Stehling, O. and Lill, R. (2013). The role of mitochondria in cellular iron-sulfur protein biogenesis: mechanisms, connected processes, and diseases. Cold Spring Harb. Perspect. Biol. 5, a011312.10.1101/cshperspect.a011312Search in Google Scholar PubMed PubMed Central
Stotland, A. and Gottlieb, R.A. (2015). Mitochondrial quality control: easy come, easy go. Biochim. Biophys. Acta 1853, 2802–2811.10.1016/j.bbamcr.2014.12.041Search in Google Scholar PubMed PubMed Central
Stotland, A. and Gottlieb, R.A. (2016). a-MHC MitoTimer mouse: in vivo mitochondrial turnover model reveals remarkable mitochondrial heterogeneity in the heart. J. Mol. Cell. Cardiol. 90, 53–58.10.1016/j.yjmcc.2015.11.032Search in Google Scholar PubMed PubMed Central
Sudhof, T.C. (2004). The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509–547.10.1146/annurev.neuro.26.041002.131412Search in Google Scholar PubMed
Sudhof, T.C. (2013). Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80, 675–690.10.1016/j.neuron.2013.10.022Search in Google Scholar PubMed PubMed Central
Szczepanowska, K. and Trifunovic, A. (2015). Different faces of mitochondrial DNA mutators. Biochim. Biophys. Acta 1847, 1362–1372.10.1016/j.bbabio.2015.05.016Search in Google Scholar PubMed
Thomas, R.L. and Gustafsson, A.B. (2013). MCL1 is critical for mitochondrial function and autophagy in the heart. Autophagy 9, 1902–1903.10.4161/auto.26168Search in Google Scholar PubMed PubMed Central
Terry, R.D., Masliah, E., Salmon, D.P., Butters, N., DeTeresa, R., Hill, R., Hansen, L.A., and Katzman, R. (1991). Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572–580.10.1002/ana.410300410Search in Google Scholar PubMed
Tuppen, H.A., Blakely, E.L., Turnbull, D.M., and Taylor, R.W. (2010). Mitochondrial DNA mutations and human disease. Biochim. Biophys. Acta 1797, 113–128.10.1016/j.bbabio.2009.09.005Search in Google Scholar PubMed
Vandresen-Filho, S., Martins, W.C., Bertoldo, D.B., Mancini, G., De Bem, A.F., and Tasca, C.I. (2015). Cerebral cortex, hippocampus, striatum and cerebellum show differential susceptibility to quinolinic acid-induced oxidative stress. Neurol. Sci. 36, 1449–1456.10.1007/s10072-015-2180-7Search in Google Scholar PubMed
Venditti, P., Di Stefano, L., and Di Meo, S. (2013). Mitochondrial metabolism of reactive oxygen species. Mitochondrion 13, 71–82.10.1016/j.mito.2013.01.008Search in Google Scholar PubMed
Verstreken, P., Ly, C.V., Venken, K.J.T., Koh, T.-W., Zhou, Y., and Bellen, H.J. (2005). Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47, 365–378.10.1016/j.neuron.2005.06.018Search in Google Scholar PubMed
Vest, K.E., Wang, J., Gammon, M.G., Maynard, M.K., White, O.L., Cobine, J.A., Mahone, W.K., and Cobine, P.A. (2016). Overlap of copper and iron uptake systems in mitochondria in Saccharomyces cerevisiae. Open Biol. 6, 150223.10.1098/rsob.150223Search in Google Scholar PubMed PubMed Central
Villa, R.F., Gorini, A., and Hoyer, S. (2006). Differentiated effect of ageing on the enzymes of Kreb’s cycle, electron transfer complexes and glutamate metabolism of non-synaptic and intra-synaptic mitochondria from cerebral cortex. J. Neural Transm. 113, 1659–1670.10.1007/s00702-006-0569-4Search in Google Scholar PubMed
Volgyi, K., Gulyassy, P., Haden, K., Kis, V., Badics, K., Kekest, K.A., Simor, A., Gyorffy, B., Toth, E.A., Lubec, G., et al. (2015). Synaptic mitochondria: a brain mitochondria cluster with a specific proteome. J. Proteom. 120, 142–157.10.1016/j.jprot.2015.03.005Search in Google Scholar PubMed
Wallace, D.C. (2011). Bioenergetic origins of complexity and disease. Cold Spring Harb. Symp. Quant. Biol. 76, 1–16.10.1101/sqb.2011.76.010462Search in Google Scholar PubMed PubMed Central
Wang, L.Y. and Augustine, G.J. (2015). Presynaptic nanodomains: a tale of two synapses. Front. Cell. Neurosci. 8, 455.10.3389/fncel.2014.00455Search in Google Scholar PubMed PubMed Central
Wang, X., Winter, D., Ashrafi, G., Schlehe, J., Wong, Y.L., Selkoe, D., Rice, S., Steen, J., LaVoie, M.J., and Schwartz, T.L. (2011). PINK1 and Parkin target Miro for phosphorylation and degradation to arrest motility. Cell 147, 893–906.10.1016/j.cell.2011.10.018Search in Google Scholar PubMed PubMed Central
Westbye, M.P., Feyzi, E., Aas, P.A., Vågbø, C.B., Talstad, V.A., Kavli, B., Hagen, L., Sundheim, O., Akbari, M., Liabakk, N.B., et al. (2008). Human AlkB homolog 1 is a mitochondrial protein that demethylates 3-methylcytosine in DNA and RNA. J. Biol. Chem. 283, 25046–25056.10.1074/jbc.M803776200Search in Google Scholar PubMed PubMed Central
Wilhelm, B.G., Mandad, S., Truckenbrodt, S., Krцhnert, K, Schдfer, C., Rammner, B., Koo, S.J., Claβen, G.A., Krauss, M., Haucke, V., et al. (2014). Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins. Science 344, 1023–1028.10.1126/science.1252884Search in Google Scholar PubMed
Yarana, C., Sanit, J., Chattipakorn, N., and Chattipakorn, S. (2012). Synaptic and nonsynaptic mitochondria demonstrate a different degree of calcium-induced mitochondrial dysfunction. Life Sci. 90, 808–814.10.1016/j.lfs.2012.04.004Search in Google Scholar PubMed
Zatulovskaia, Y.A., Ilyechova, E.Y., and Puchkova, L.V. (2015). The features of copper metabolism in the rat liver during development. PLoS One 10, e0140797.10.1371/journal.pone.0140797Search in Google Scholar PubMed PubMed Central
Zheng, W., Khrapko, K., Coller, H.A., Thilly, W.G., and Copeland, W.C. (2006). Origins of human mitochondrial point mutations as DNA polymerase γ-mediated errors. Mutat. Res. 599, 11–20.10.1016/j.mrfmmm.2005.12.012Search in Google Scholar PubMed
Zhu, P.J. and Krnjevic, K. (1997). Adenosine release mediates cyanide-induced suppression of CA1 neuronal activity. J. Neurosci. 17, 2355–2364.10.1523/JNEUROSCI.17-07-02355.1997Search in Google Scholar
Zischka, H. and Lichtmannegger, J. (2014). Pathological mitochondrial copper overload in livers of Wilson’s disease patients and related animal models. Ann. N. Y. Acad. Sci. 1315, 6–15.10.1111/nyas.12347Search in Google Scholar PubMed
©2017 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Deciphering the modulatory role of oxytocin in human altruism
- How neuroscience can inform the study of individual differences in cognitive abilities
- Biogenetic and morphofunctional heterogeneity of mitochondria: the case of synaptic mitochondria
- Long non-coding RNAs: potential molecular biomarkers for gliomas diagnosis and prognosis
- Defensive reflexes in people with pain – a biomarker of the need to protect? A meta-analytical systematic review
- Blood-brain barrier-supported neurogenesis in healthy and diseased brain
- Mathematics, anxiety, and the brain
- Integrating neurobiology of emotion regulation and trauma therapy: reflections on EMDR therapy
- The potential of transcranial photobiomodulation therapy for treatment of major depressive disorder
Articles in the same Issue
- Frontmatter
- Deciphering the modulatory role of oxytocin in human altruism
- How neuroscience can inform the study of individual differences in cognitive abilities
- Biogenetic and morphofunctional heterogeneity of mitochondria: the case of synaptic mitochondria
- Long non-coding RNAs: potential molecular biomarkers for gliomas diagnosis and prognosis
- Defensive reflexes in people with pain – a biomarker of the need to protect? A meta-analytical systematic review
- Blood-brain barrier-supported neurogenesis in healthy and diseased brain
- Mathematics, anxiety, and the brain
- Integrating neurobiology of emotion regulation and trauma therapy: reflections on EMDR therapy
- The potential of transcranial photobiomodulation therapy for treatment of major depressive disorder