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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

General Review Article

Isolated Mitochondrial Preparations and In organello Assays: A Powerful and Relevant Ex vivo Tool for Assessment of Brain (Patho)physiology

Author(s): Faraz Ahmad*, Siva Ramamorthy, Mohammed Y. Areeshi, Ghulam Md. Ashraf and Shafiul Haque*

Volume 21, Issue 6, 2023

Published on: 03 March, 2023

Page: [1433 - 1449] Pages: 17

DOI: 10.2174/1570159X21666230303123555

Price: $65

Abstract

Mitochondria regulate multiple aspects of neuronal development, physiology, plasticity, and pathology through their regulatory roles in bioenergetic, calcium, redox, and cell survival/death signalling. While several reviews have addressed these different aspects, a comprehensive discussion focussing on the relevance of isolated brain mitochondria and their utilities in neuroscience research has been lacking. This is relevant because the employment of isolated mitochondria rather than their in situ functional evaluation, offers definitive evidence of organelle-specificity, negating the interference from extra mitochondrial cellular factors/signals. This mini-review was designed primarily to explore the commonly employed in organello analytical assays for the assessment of mitochondrial physiology and its dysfunction, with a particular focus on neuroscience research. The authors briefly discuss the methodologies for biochemical isolation of mitochondria, their quality assessment, and cryopreservation. Further, the review attempts to accumulate the key biochemical protocols for in organello assessment of a multitude of mitochondrial functions critical for neurophysiology, including assays for bioenergetic activity, calcium and redox homeostasis, and mitochondrial protein translation. The purpose of this review is not to examine each and every method or study related to the functional assessment of isolated brain mitochondria, but rather to assemble the commonly used protocols of in organello mitochondrial research in a single publication. The hope is that this review will provide a suitable platform aiding neuroscientists to choose and apply the required protocols and tools to address their particular mechanistic, diagnostic, or therapeutic question dealing within the confines of the research area of mitochondrial patho-physiology in the neuronal perspective.

Graphical Abstract

[1]
Khacho, M.; Harris, R.; Slack, R.S. Mitochondria as central regulators of neural stem cell fate and cognitive function. Nat. Rev. Neurosci., 2019, 20(1), 34-48.
[http://dx.doi.org/10.1038/s41583-018-0091-3] [PMID: 30464208]
[2]
Belenguer, P.; Duarte, J.M.N.; Schuck, P.F.; Ferreira, G.C. Mitochondria and the brain: bioenergetics and beyond. Neurotox. Res., 2019, 36(2), 219-238.
[http://dx.doi.org/10.1007/s12640-019-00061-7] [PMID: 31152314]
[3]
Kann, O.; Kovács, R. Mitochondria and neuronal activity. Am. J. Physiol. Cell Physiol., 2007, 292(2), C641-C657.
[http://dx.doi.org/10.1152/ajpcell.00222.2006] [PMID: 17092996]
[4]
Völgyi, K.; Gulyássy, P.; Háden, K.; Kis, V.; Badics, K.; Kékesi, K.A.; Simor, A.; Györffy, B.; Tóth, E.A.; Lubec, G.; Juhász, G.; Dobolyi, A. Synaptic mitochondria: A brain mitochondria cluster with a specific proteome. J. Proteomics, 2015, 120, 142-157.
[http://dx.doi.org/10.1016/j.jprot.2015.03.005] [PMID: 25782751]
[5]
Dubinsky, J.M. Heterogeneity of nervous system mitochondria: Location, location, location! Exp. Neurol., 2009, 218(2), 293-307.
[http://dx.doi.org/10.1016/j.expneurol.2009.05.020] [PMID: 19464292]
[6]
Fedorovich, S.V.; Waseem, T.V.; Puchkova, L.V. Biogenetic and morphofunctional heterogeneity of mitochondria: The case of synaptic mitochondria. Rev. Neurosci., 2017, 28(4), 363-373.
[http://dx.doi.org/10.1515/revneuro-2016-0077] [PMID: 28195557]
[7]
Ly, C.V.; Verstreken, P. Mitochondria at the synapse. Neuroscientist, 2006, 12(4), 291-299.
[http://dx.doi.org/10.1177/1073858406287661] [PMID: 16840705]
[8]
Vos, M.; Lauwers, E.; Verstreken, P. Synaptic mitochondria in synaptic transmission and organization of vesicle pools in health and disease. Front. Synaptic Neurosci., 2010, 2, 139.
[http://dx.doi.org/10.3389/fnsyn.2010.00139] [PMID: 21423525]
[9]
Stauch, K.L.; Purnell, P.R.; Fox, H.S. Quantitative proteomics of synaptic and nonsynaptic mitochondria: insights for synaptic mitochondrial vulnerability. J. Proteome Res., 2014, 13(5), 2620-2636.
[http://dx.doi.org/10.1021/pr500295n] [PMID: 24708184]
[10]
Raefsky, S.M.; Mattson, M.P. Adaptive responses of neuronal mitochondria to bioenergetic challenges: Roles in neuroplasticity and disease resistance. Free Radic. Biol. Med., 2017, 102, 203-216.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.11.045] [PMID: 27908782]
[11]
Ahmad, F.; Haque, S.; Ravinayagam, V.; Ahmad, A.; Kamli, M.R.; Barreto, G.E. Developmental lead (Pb)-induced deficits in redox and bioenergetic status of cerebellar synapses are ameliorated by ascorbate supplementation. Toxicology, 2020, 440, 152492.
[http://dx.doi.org/10.1016/j.tox.2020.152492] [PMID: 32407874]
[12]
Ahmad, F.; Salahuddin, M.; Alamoudi, W.; Acharya, S. Dysfunction of cortical synapse-specific mitochondria in developing rats exposed to lead and its amelioration by ascorbate supplementation. Neuropsychiatr. Dis. Treat., 2018, 14, 813-824.
[http://dx.doi.org/10.2147/NDT.S148248] [PMID: 29606875]
[13]
Wang, L.; Guo, L.; Lu, L.; Sun, H.; Shao, M.; Beck, S.J.; Li, L.; Ramachandran, J.; Du, Y.; Du, H. Synaptosomal mitochondrial dysfunction in 5xFAD mouse model of Alzheimer’s disease. PLoS One, 2016, 11(3), e0150441.
[http://dx.doi.org/10.1371/journal.pone.0150441] [PMID: 26942905]
[14]
Du, H.; Guo, L.; Yan, S.; Sosunov, A.A.; McKhann, G.M.; ShiDu Yan, S. Early deficits in synaptic mitochondria in an Alzheimer’s disease mouse model. Proc. Natl. Acad. Sci. USA, 2010, 107(43), 18670-18675.
[http://dx.doi.org/10.1073/pnas.1006586107] [PMID: 20937894]
[15]
Guo, L.; Tian, J.; Du, H. Mitochondrial dysfunction and synaptic transmission failure in Alzheimer’s Disease. J. Alzheimers Dis., 2017, 57(4), 1071-1086.
[http://dx.doi.org/10.3233/JAD-160702] [PMID: 27662318]
[16]
Grimm, A.; Eckert, A. Brain aging and neurodegeneration: From a mitochondrial point of view. J. Neurochem., 2017, 143(4), 418-431.
[http://dx.doi.org/10.1111/jnc.14037] [PMID: 28397282]
[17]
Pei, L.; Wallace, D.C. Mitochondrial etiology of neuropsychiatric disorders. Biol. Psychiatry, 2018, 83(9), 722-730.
[http://dx.doi.org/10.1016/j.biopsych.2017.11.018] [PMID: 29290371]
[18]
Jeanneteau, F.; Arango-Lievano, M. Linking mitochondria to synapses: New insights for stress-related neuropsychiatric disorders. Neural Plast., 2016, 2016, 3985063.
[19]
Cabral-Costa, J.V.; Kowaltowski, A.J. Neurological disorders and mitochondria. Mol. Aspects Med., 2020, 71, 100826.
[http://dx.doi.org/10.1016/j.mam.2019.10.003] [PMID: 31630771]
[20]
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]
[21]
Martin, L.J. Biology of mitochondria in neurodegenerative diseases. Prog. Mol. Biol. Transl. Sci., 2012, 107, 355-415.
[http://dx.doi.org/10.1016/B978-0-12-385883-2.00005-9] [PMID: 22482456]
[22]
Frezza, C.; Cipolat, S.; Scorrano, L. Organelle isolation: Functional mitochondria from mouse liver, muscle and cultured filroblasts. Nat. Protoc., 2007, 2(2), 287-295.
[http://dx.doi.org/10.1038/nprot.2006.478] [PMID: 17406588]
[23]
Sperling, J.A.; Sakamuri, S.S.V.P.; Albuck, A.L.; Sure, V.N.; Evans, W.R.; Peterson, N.R.; Rutkai, I.; Mostany, R.; Satou, R.; Katakam, P.V.G. Measuring respiration in isolated murine brain mitochondria: Implications for mechanistic stroke studies. Neuromolecular Med., 2019, 21(4), 493-504.
[http://dx.doi.org/10.1007/s12017-019-08552-8] [PMID: 31172441]
[24]
Hartwig, S.; Feckler, C.; Lehr, S.; Wallbrecht, K.; Wolgast, H.; Müller-Wieland, D.; Kotzka, J. A critical comparison between two classical and a kit-based method for mitochondria isolation. Proteomics, 2009, 9(11), 3209-3214.
[http://dx.doi.org/10.1002/pmic.200800344] [PMID: 19415664]
[25]
Hogeboom, G.H.; Schneider, W.C.; Pallade, G.E. Cytochemical studies of mammalian tissues; isolation of intact mitochondria from rat liver; some biochemical properties of mitochondria and submicroscopic particulate material. J. Biol. Chem., 1948, 172(2), 619-635.
[http://dx.doi.org/10.1016/S0021-9258(19)52749-1] [PMID: 18901182]
[26]
Lampl, T.; Crum, J.A.; Davis, T.A.; Milligan, C.; Del Gaizo Moore, V. Isolation and functional analysis of mitochondria from cultured cells and mouse tissue. J. Vis. Exp., 2015, (97), 52076.
[http://dx.doi.org/10.3791/52076] [PMID: 25866954]
[27]
Wettmarshausen, J.; Perocchi, F. Isolation of functional mitochondria from cultured cells and mouse tissues. Methods Mol. Biol., 2017, 1567, 15-32.
[http://dx.doi.org/10.1007/978-1-4939-6824-4_2] [PMID: 28276010]
[28]
Kristián, T.; Hopkins, I.B.; McKenna, M.C.; Fiskum, G. Isolation of mitochondria with high respiratory control from primary cultures of neurons and astrocytes using nitrogen cavitation. J. Neurosci. Methods, 2006, 152(1-2), 136-143.
[http://dx.doi.org/10.1016/j.jneumeth.2005.08.018] [PMID: 16253339]
[29]
Graham, J.M. Purification of a crude mitochondrial fraction by density‐gradient centrifugation. Curr. Protoc. Cell Biol., 1999, 4.
[http://dx.doi.org/10.1002/0471143030.cb0304s04]
[30]
Ozawa, K.; Seta, K.; Takeda, H.; Ando, K.; Handa, H.; Araki, C. On the isolation of mitochondria with high respiratory control from rat brain. J. Biochem., 1966, 59(5), 501-510.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a128334] [PMID: 4225395]
[31]
Stahl, W.L.; Smith, J.C.; Napolitano, L.M.; Basford, R.E. Brain mitochondria. I. Isolation of bovine brain mitochondria. J. Cell Biol., 1963, 19(2), 293-307.
[http://dx.doi.org/10.1083/jcb.19.2.293] [PMID: 14090748]
[32]
Clayton, DA; Shadel, GS Purification of mitochondria by sucrose step density gradient centrifugation. Cold Spring Harb Protoc., 2014, 2014(10), pdb.prot080028.
[http://dx.doi.org/10.1101/pdb.prot080028]
[33]
Sauerbeck, A.; Pandya, J.; Singh, I.; Bittman, K.; Readnower, R.; Bing, G.; Sullivan, P. Analysis of regional brain mitochondrial bioenergetics and susceptibility to mitochondrial inhibition utilizing a microplate based system. J. Neurosci. Methods, 2011, 198(1), 36-43.
[http://dx.doi.org/10.1016/j.jneumeth.2011.03.007] [PMID: 21402103]
[34]
Hamberger, A.; Blomstrand, C.; Lehninger, A.L. Comparative studies on mitochondria isolated from neuron-enriched and glia-enriched fractions of rabbit and beef brain. J. Cell Biol., 1970, 45(2), 221-234.
[http://dx.doi.org/10.1083/jcb.45.2.221] [PMID: 5513605]
[35]
Lai, J.C.K.; Walsh, J.M.; Dennis, S.C.; Clark, J.B. Synaptic and non-synaptic mitochondria from rat brain: isolation and characterization. J. Neurochem., 1977, 28(3), 625-631.
[http://dx.doi.org/10.1111/j.1471-4159.1977.tb10434.x] [PMID: 16086]
[36]
Morota, S.; Hansson, M.J.; Ishii, N.; Kudo, Y.; Elmér, E.; Uchino, H. Spinal cord mitochondria display lower calcium retention capacity compared with brain mitochondria without inherent differences in sensitivity to cyclophilin D inhibition. J. Neurochem., 2007, 103(5), 2066-2076.
[http://dx.doi.org/10.1111/j.1471-4159.2007.04912.x] [PMID: 17868326]
[37]
Sims, N.R. Rapid isolation of metabolically active mitochondria from rat brain and subregions using Percoll density gradient centrifugation. J. Neurochem., 1990, 55(2), 698-707.
[http://dx.doi.org/10.1111/j.1471-4159.1990.tb04189.x] [PMID: 2164576]
[38]
Sims, N.R.; Anderson, M.F. Isolation of mitochondria from rat brain using Percoll density gradient centrifugation. Nat. Protoc., 2008, 3(7), 1228-1239.
[http://dx.doi.org/10.1038/nprot.2008.105] [PMID: 18600228]
[39]
Kristian, T. Isolation of mitochondria from the CNS. Curr. Protoc. Neurosci., 2010.
[http://dx.doi.org/10.1002/0471142301.ns0722s52]
[40]
Spinazzi, M.; Casarin, A.; Pertegato, V.; Salviati, L.; Angelini, C. Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nat. Protoc., 2012, 7(6), 1235-1246.
[http://dx.doi.org/10.1038/nprot.2012.058] [PMID: 22653162]
[41]
Valenti, D.; de Bari, L.; De Filippis, B.; Ricceri, L.; Vacca, R.A. Preservation of mitochondrial functional integrity in mitochondria isolated from small cryopreserved mouse brain areas. Anal. Biochem., 2014, 444, 25-31.
[http://dx.doi.org/10.1016/j.ab.2013.08.030] [PMID: 24018341]
[42]
Barksdale, K.A.; Perez-Costas, E.; Gandy, J.C.; Melendez-Ferro, M.; Roberts, R.C.; Bijur, G.N. Mitochondrial viability in mouse and human postmortem brain. FASEB J., 2010, 24(9), 3590-3599.
[http://dx.doi.org/10.1096/fj.09-152108] [PMID: 20466876]
[43]
García-Roche, M.; Casal, A.; Carriquiry, M.; Radi, R.; Quijano, C.; Cassina, A. Respiratory analysis of coupled mitochondria in cryopreserved liver biopsies. Redox Biol., 2018, 17, 207-212.
[http://dx.doi.org/10.1016/j.redox.2018.03.008] [PMID: 29704825]
[44]
Acin-Perez, R.; Benador, I.Y.; Petcherski, A.; Veliova, M.; Benavides, G.A.; Lagarrigue, S.; Caudal, A.; Vergnes, L.; Murphy, A.N.; Karamanlidis, G.; Tian, R.; Reue, K.; Wanagat, J.; Sacks, H.; Amati, F.; Darley-Usmar, V.M.; Liesa, M.; Divakaruni, A.S.; Stiles, L.; Shirihai, O.S. A novel approach to measure mitochondrial respiration in frozen biological samples. EMBO J., 2020, 39(13), e104073.
[http://dx.doi.org/10.15252/embj.2019104073] [PMID: 32432379]
[45]
Clayton, DA; Shadel, GS Isolation of mitochondria from tissue culture cells. Cold Spring Harb Protoc., 2014, 2014(10), pdb.prot080002..
[http://dx.doi.org/10.1101/pdb.prot080002]
[46]
Almeida, A.; Medina, J.M. A rapid method for the isolation of metabolically active mitochondria from rat neurons and astrocytes in primary culture. Brain Res. Brain Res. Protoc., 1998, 2(3), 209-214.
[http://dx.doi.org/10.1016/S1385-299X(97)00044-5] [PMID: 9507134]
[47]
Devi, L.; Prabhu, B.M.; Galati, D.F.; Avadhani, N.G.; Anandatheerthavarada, H.K. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer’s disease brain is associated with mitochondrial dysfunction. J. Neurosci., 2006, 26(35), 9057-9068.
[http://dx.doi.org/10.1523/JNEUROSCI.1469-06.2006] [PMID: 16943564]
[48]
Prajapati, P.; Wang, W.X.; Nelson, P.T.; Springer, J.E. Methodology for subcellular fractionation and MicroRNA examination of mitochondria, mitochondria associated ER membrane (MAM), ER, and cytosol from human brain. Methods Mol. Biol., 2020, 2063, 139-154.
[http://dx.doi.org/10.1007/978-1-0716-0138-9_11] [PMID: 31667768]
[49]
Hansson, M.J.; Morota, S.; Chen, L.; Matsuyama, N.; Suzuki, Y.; Nakajima, S.; Tanoue, T.; Omi, A.; Shibasaki, F.; Shimazu, M.; Ikeda, Y.; Uchino, H.; Elmér, E. Cyclophilin D-sensitive mitochondrial permeability transition in adult human brain and liver mitochondria. J. Neurotrauma, 2011, 28(1), 143-153.
[http://dx.doi.org/10.1089/neu.2010.1613] [PMID: 21121808]
[50]
Khattar, N.K.; Yablonska, S.; Baranov, S.V.; Baranova, O.V.; Kretz, E.S.; Larkin, T.M.; Carlisle, D.L.; Richardson, R.M.; Friedlander, R.M. Isolation of functionally active and highly purified neuronal mitochondria from human cortex. J. Neurosci. Methods, 2016, 263, 1-6.
[http://dx.doi.org/10.1016/j.jneumeth.2016.01.017] [PMID: 26808294]
[51]
Wang, X.; Leverin, A.L.; Han, W.; Zhu, C.; Johansson, B.R.; Jacotot, E.; Ten, V.S.; Sims, N.R.; Hagberg, H. Isolation of brain mitochondria from neonatal mice. J. Neurochem., 2011, 119(6), 1253-1261.
[http://dx.doi.org/10.1111/j.1471-4159.2011.07525.x] [PMID: 21985402]
[52]
Pallotti, F.; Lenaz, G. Isolation and subfractionation of mitochondria from animal cells and tissue culture lines. Methods Cell Biol., 2007, 80, 3-44.
[http://dx.doi.org/10.1016/S0091-679X(06)80001-4] [PMID: 17445687]
[53]
Hill, R.L.; Kulbe, J.R.; Singh, I.N.; Wang, J.A.; Hall, E.D. Synaptic mitochondria are more susceptible to traumatic brain injury-induced oxidative damage and respiratory dysfunction than non-synaptic mitochondria. Neuroscience, 2018, 386, 265-283.
[http://dx.doi.org/10.1016/j.neuroscience.2018.06.028] [PMID: 29960045]
[54]
Brown, M.R.; Sullivan, P.G.; Geddes, J.W. Synaptic mitochondria are more susceptible to Ca2+overload than nonsynaptic mitochondria. J. Biol. Chem., 2006, 281(17), 11658-11668.
[http://dx.doi.org/10.1074/jbc.M510303200] [PMID: 16517608]
[55]
Annunziata, I.; Weesner, J.A.; d’Azzo, A. Isolation of mitochondria-associated ER membranes (MAMs), synaptic MAMs, and glycosphingolipid enriched microdomains (GEMs) from brain tissues and neuronal cells. Methods Mol. Biol., 2021, 2277, 357-370.
[http://dx.doi.org/10.1007/978-1-0716-1270-5_22] [PMID: 34080162]
[56]
Wieckowski, M.R.; Giorgi, C.; Lebiedzinska, M.; Duszynski, J.; Pinton, P. Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat. Protoc., 2009, 4(11), 1582-1590.
[http://dx.doi.org/10.1038/nprot.2009.151] [PMID: 19816421]
[57]
Schreiner, B.; Ankarcrona, M. Isolation of mitochondria-associated membranes (MAM) from mouse brain tissue. Methods Mol. Biol., 2017, 1567, 53-68.
[http://dx.doi.org/10.1007/978-1-4939-6824-4_5] [PMID: 28276013]
[58]
Islinger, M.; Wildgruber, R.; Völkl, A. Preparative free-flow electrophoresis, a versatile technology complementing gradient centrifugation in the isolation of highly purified cell organelles. Electrophoresis, 2018, 39(18), 2288-2299.
[http://dx.doi.org/10.1002/elps.201800187] [PMID: 29761848]
[59]
Hackenbrock, C.R. Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states. Proc. Natl. Acad. Sci. USA, 1968, 61(2), 598-605.
[http://dx.doi.org/10.1073/pnas.61.2.598] [PMID: 4176482]
[60]
Frey, T.G.; Mannella, C.A. The internal structure of mitochondria. Trends Biochem. Sci., 2000, 25(7), 319-324.
[http://dx.doi.org/10.1016/S0968-0004(00)01609-1] [PMID: 10871882]
[61]
Ahmad, F.; Alamoudi, W.; Haque, S.; Salahuddin, M.; Alsamman, K. Simple, reliable, and time-efficient colorimetric method for the assessment of mitochondrial function and toxicity. Bosn. J. Basic Med. Sci., 2018, 18(4), 367-374.
[http://dx.doi.org/10.17305/bjbms.2018.3323] [PMID: 29984676]
[62]
Ghazi-Khansari, M.; Mohammadi-Bardbori, A.; Hosseini, M-J. Using Janus green B to study paraquat toxicity in rat liver mitochondria: role of ACE inhibitors (thiol and nonthiol ACEi). Ann. N. Y. Acad. Sci., 2006, 1090(1), 98-107.
[http://dx.doi.org/10.1196/annals.1378.010] [PMID: 17384251]
[63]
Kundu, T.; Bhattacharjee, B.; Hazra, S.; Ghosh, A.K.; Bandyopadhyay, D.; Pramanik, A. Synthesis and biological assessment of pyrrolobenzoxazine scaffold as a potent antioxidant. J. Med. Chem., 2019, 62(13), 6315-6329.
[http://dx.doi.org/10.1021/acs.jmedchem.9b00717] [PMID: 31246452]
[64]
Wang, X.; Yan, X.; Yang, Y.; Yang, W.; Zhang, Y.; Wang, J.; Ye, D.; Wu, Y.; Ma, P.; Yan, B. Dibutyl phthalate-mediated oxidative stress induces splenic injury in mice and the attenuating effects of vitamin E and curcumin. Food Chem. Toxicol., 2020, 136, 110955.
[http://dx.doi.org/10.1016/j.fct.2019.110955] [PMID: 31712109]
[65]
Lemasters, J.J.; Ramshesh, V.K. Imaging of mitochondrial polarization and depolarization with cationic fluorophores. Methods Cell Biol., 2007, 80, 283-295.
[http://dx.doi.org/10.1016/S0091-679X(06)80014-2] [PMID: 17445700]
[66]
Chazotte, B. Labeling mitochondria with MitoTracker dyes. Cold Spring Harb. Protoc., 2011, 2011(8), 990-2.
[http://dx.doi.org/10.1101/pdb.prot5648] [PMID: 21807856]
[67]
Lecoeur, H.; Langonné, A.; Baux, L.; Rebouillat, D.; Rustin, P.; Prévost, M.C.; Brenner, C.; Edelman, L.; Jacotot, E. Real-time flow cytometry analysis of permeability transition in isolated mitochondria. Exp. Cell Res., 2004, 294(1), 106-117.
[http://dx.doi.org/10.1016/j.yexcr.2003.10.030] [PMID: 14980506]
[68]
Tanji, K.; Bonilla, E. Optical imaging techniques (histochemical, immunohistochemical, and in situ hybridization staining methods) to visualize mitochondria. Methods Cell Biol., 2007, 80, 135-154.
[http://dx.doi.org/10.1016/S0091-679X(06)80006-3] [PMID: 17445692]
[69]
Westensee, I.N.; Brodszkij, E.; Qian, X.; Marcelino, T.F.; Lefkimmiatis, K.; Städler, B. Mitochondria encapsulation in hydrogel‐based artificial cells as ATP producing subunits. Small, 2021, 17(24), 2007959.
[http://dx.doi.org/10.1002/smll.202007959] [PMID: 33969618]
[70]
Bhosale, G.; Duchen, M.R. Investigating the mitochondrial permeability transition pore in disease phenotypes and drug screening. Curr. Protocols Pharmacol., 2019, 85(1), e59.
[http://dx.doi.org/10.1002/cpph.59] [PMID: 31081999]
[71]
Koh, J.Y.; Choi, D.W. Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J. Neurosci. Methods, 1987, 20(1), 83-90.
[http://dx.doi.org/10.1016/0165-0270(87)90041-0] [PMID: 2884353]
[72]
Xu, J.; Chen, Q.; Zen, K.; Zhang, C.; Zhang, Q. Synaptosomes secrete and uptake functionally active microRNAs via exocytosis and endocytosis pathways. J. Neurochem., 2013, 124(1), 15-25.
[http://dx.doi.org/10.1111/jnc.12057] [PMID: 23083096]
[73]
Vassault, A. L-Lactate dehydrogenase. UV method with pyruvate and NADH. Methods Enzym Anal, 1983, 3, 118-126.
[74]
Nuñez-Figueredo, Y.; Pardo-Andreu, G.L.; Ramírez-Sánchez, J.; Delgado-Hernández, R.; Ochoa-Rodríguez, E.; Verdecia-Reyes, Y.; Naal, Z.; Muller, A.P.; Portela, L.V.; Souza, D.O. Antioxidant effects of JM-20 on rat brain mitochondria and synaptosomes: Mitoprotection against Ca2+-induced mitochondrial impairment. Brain Res. Bull., 2014, 109, 68-76.
[http://dx.doi.org/10.1016/j.brainresbull.2014.10.001] [PMID: 25305343]
[75]
Colombini, M. Measurement of VDAC permeability in intact mitochondria and in reconstituted systems. Methods Cell Biol., 2007, 80, 241-260.
[http://dx.doi.org/10.1016/S0091-679X(06)80012-9] [PMID: 17445698]
[76]
Douce, R.; Bourguignon, J.; Brouquisse, R.; Neuburger, M. Isolation of plant mitochondria: General principles and criteria of integrity. Methods Enzymol., 1987, 148, 403-415.
[http://dx.doi.org/10.1016/0076-6879(87)48039-7]
[77]
Vacca, R.A.; Valenti, D.; Bobba, A.; Merafina, R.S.; Passarella, S.; Marra, E. Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco Bright-Yellow 2 cells en route to heat shock-induced cell death. Plant Physiol., 2006, 141(1), 208-219.
[http://dx.doi.org/10.1104/pp.106.078683] [PMID: 16531480]
[78]
Dietrich, P.; Alli, S.; Mulligan, M.K.; Cox, R.; Ashbrook, D.G.; Williams, R.W.; Dragatsis, I. Identification of cyclin D1 as a major modulator of 3-nitropropionic acid-induced striatal neurodegeneration. Neurobiol. Dis., 2022, 162, 105581.
[http://dx.doi.org/10.1016/j.nbd.2021.105581] [PMID: 34871739]
[79]
Lanza, I.R.; Nair, K.S. Functional assessment of isolated mitochondria in vitro. Methods Enzymol., 2009, 457, 349-372.
[http://dx.doi.org/10.1016/S0076-6879(09)05020-4] [PMID: 19426878]
[80]
Rasmussen, H.N.; Andersen, A.J.; Rasmussen, U.F. Optimization of preparation of mitochondria from 25-100 mg skeletal muscle. Anal. Biochem., 1997, 252(1), 153-159.
[http://dx.doi.org/10.1006/abio.1997.2304] [PMID: 9324953]
[81]
Rasmussen, H.N.; Rasmussen, U.F. Small scale preparation of skeletal muscle mitochondria, criteria of integrity, and assays with reference to tissue function. Mol. Cell. Biochem., 1997, 174(1/2), 55-60.
[http://dx.doi.org/10.1023/A:1006851705996] [PMID: 9309665]
[82]
Srere, P.A. Citrate synthase. Methods Enzymol., 1969, 13, 3-11.
[http://dx.doi.org/10.1016/0076-6879(69)13005-0] [PMID: 11265473]
[83]
Valenti, D.; Vacca, R.A.; de Pinto, M.C.; De Gara, L.; Marra, E.; Passarella, S. In the early phase of programmed cell death in Tobacco Bright Yellow 2 cells the mitochondrial adenine nucleotide translocator, adenylate kinase and nucleoside diphosphate kinase are impaired in a reactive oxygen species-dependent manner. Biochim. Biophys. Acta Bioenerg., 2007, 1767(1), 66-78.
[http://dx.doi.org/10.1016/j.bbabio.2006.11.004] [PMID: 17184729]
[84]
Bergmeyer, H.U.; Gawehn, K.; Grassl, M. Enzymatic assay of fumarase. Methods Enzym Anal., 1974, 1, 543-545.
[85]
Atlante, A.; Calissano, P.; Bobba, A.; Azzariti, A.; Marra, E.; Passarella, S. Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ROS scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death. J. Biol. Chem., 2000, 275(47), 37159-37166.
[http://dx.doi.org/10.1074/jbc.M002361200] [PMID: 10980192]
[86]
De Loecker, P.; Fuller, B.J.; De Loecker, W. The effects of cryopreservation on protein synthesis and membrane transport in isolated rat liver mitochondria. Cryobiology, 1991, 28(5), 445-453.
[http://dx.doi.org/10.1016/0011-2240(91)90053-Q] [PMID: 1752132]
[87]
Yamaguchi, R.; Andreyev, A.; Murphy, A.N.; Perkins, G.A.; Ellisman, M.H.; Newmeyer, D.D. Mitochondria frozen with trehalose retain a number of biological functions and preserve outer membrane integrity. Cell Death Differ., 2007, 14(3), 616-624.
[http://dx.doi.org/10.1038/sj.cdd.4402035] [PMID: 16977331]
[88]
Nukala, V.N.; Singh, I.N.; Davis, L.M.; Sullivan, P.G. Cryopreservation of brain mitochondria: A novel methodology for functional studies. J. Neurosci. Methods, 2006, 152(1-2), 48-54.
[http://dx.doi.org/10.1016/j.jneumeth.2005.08.017] [PMID: 16246427]
[89]
Kuznetsov, A.V.; Kunz, W.S.; Saks, V.; Usson, Y.; Mazat, J.P.; Letellier, T.; Gellerich, F.N.; Margreiter, R. Cryopreservation of mitochondria and mitochondrial function in cardiac and skeletal muscle fibers. Anal. Biochem., 2003, 319(2), 296-303.
[http://dx.doi.org/10.1016/S0003-2697(03)00326-9] [PMID: 12871725]
[90]
Schieber, O.; Dietrich, A.; Maréchal-Drouard, L. Cryopreservation of plant mitochondria as a tool for protein import or in organello protein synthesis studies. Plant Physiol., 1994, 106(1), 159-164.
[http://dx.doi.org/10.1104/pp.106.1.159] [PMID: 12232314]
[91]
Zorova, L.D.; Popkov, V.A.; Plotnikov, E.Y.; Silachev, D.N.; Pevzner, I.B.; Jankauskas, S.S.; Babenko, V.A.; Zorov, S.D.; Balakireva, A.V.; Juhaszova, M.; Sollott, S.J.; Zorov, D.B.; Zorov, S.D.; Balakireva, A.V.; Juhaszova, M.; Sollott, S.J.; Zorov, D.B. Mitochondrial membrane potential. Anal. Biochem., 2018, 552, 50-59.
[http://dx.doi.org/10.1016/j.ab.2017.07.009] [PMID: 28711444]
[92]
Perry, S.W.; Norman, J.P.; Barbieri, J.; Brown, E.B.; Gelbard, H.A. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotechniques, 2011, 50(2), 98-115.
[http://dx.doi.org/10.2144/000113610] [PMID: 21486251]
[93]
Scaduto, R.C., Jr; Grotyohann, L.W. Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys. J., 1999, 76(1), 469-477.
[http://dx.doi.org/10.1016/S0006-3495(99)77214-0] [PMID: 9876159]
[94]
Bunting, J.R.; Phan, T.V.; Kamali, E.; Dowben, R.M. Fluorescent cationic probes of mitochondria. Metrics and mechanism of interaction. Biophys. J., 1989, 56(5), 979-993.
[http://dx.doi.org/10.1016/S0006-3495(89)82743-2] [PMID: 2605307]
[95]
Tahara, E.B.; Navarete, F.D.T.; Kowaltowski, A.J. Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radic. Biol. Med., 2009, 46(9), 1283-1297.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.02.008] [PMID: 19245829]
[96]
Åkerman, K.E.O.; Wikström, M.K.F. Safranine as a probe of the mitochondrial membrane potential. FEBS Lett., 1976, 68(2), 191-197.
[http://dx.doi.org/10.1016/0014-5793(76)80434-6] [PMID: 976474]
[97]
Sivandzade, F.; Bhalerao, A.; Cucullo, L. Analysis of the mitochondrial membrane potential using the cationic JC-1 dye as a sensitive fluorescent probe. Bio Protoc., 2019, 9(1), e3128.
[http://dx.doi.org/10.21769/BioProtoc.3128] [PMID: 30687773]
[98]
Lugli, E.; Troiano, L.; Cossarizza, A. Polychromatic analysis of mitochondrial membrane potential using JC-1. Curr. Protoc. Cytom., 2007, Chapter 7: Unit7.32.
[99]
Cossarizza, A.; Salvioli, S. Flow cytometric analysis of mitochondrial membrane potential using JC‐1. Curr. Protoc. Cytom., 2000, Chapter 9:Unit 9.14.
[100]
Reers, M.; Smiley, S.T.; Mottola-Hartshorn, C.; Chen, A.; Lin, M.; Chen, L.B. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol., 1995, 260, 406-417.
[http://dx.doi.org/10.1016/0076-6879(95)60154-6] [PMID: 8592463]
[101]
Noterman, M.F.; Chaubey, K.; Lin-Rahardja, K.; Rajadhyaksha, A.M.; Pieper, A.A.; Taylor, E.B. Dual-process brain mitochondria isolation preserves function and clarifies protein composition. Proc. Natl. Acad. Sci. USA, 2021, 118(11), e2019046118.
[http://dx.doi.org/10.1073/pnas.2019046118] [PMID: 33836587]
[102]
Lores-Arnaiz, S.; Lombardi, P.; Karadayian, A.G.; Orgambide, F.; Cicerchia, D.; Bustamante, J. Brain cortex mitochondrial bioenergetics in synaptosomes and non-synaptic mitochondria during aging. Neurochem. Res., 2016, 41(1-2), 353-363.
[http://dx.doi.org/10.1007/s11064-015-1817-5] [PMID: 26818758]
[103]
Hurst, S.; Hoek, J.; Sheu, S.S. Mitochondrial Ca2+ and regulation of the permeability transition pore. J. Bioenerg. Biomembr., 2017, 49(1), 27-47.
[http://dx.doi.org/10.1007/s10863-016-9672-x] [PMID: 27497945]
[104]
Chinopoulos, C. Mitochondrial permeability transition pore: Back to the drawing board. Neurochem. Int., 2018, 117, 49-54.
[http://dx.doi.org/10.1016/j.neuint.2017.06.010] [PMID: 28647376]
[105]
Halestrap, A.P. What is the mitochondrial permeability transition pore? J. Mol. Cell. Cardiol., 2009, 46(6), 821-831.
[http://dx.doi.org/10.1016/j.yjmcc.2009.02.021] [PMID: 19265700]
[106]
Mnatsakanyan, N.; Beutner, G.; Porter, G.A.; Alavian, K.N.; Jonas, E.A. Physiological roles of the mitochondrial permeability transition pore. J. Bioenerg. Biomembr., 2017, 49(1), 13-25.
[http://dx.doi.org/10.1007/s10863-016-9652-1] [PMID: 26868013]
[107]
Choo, Y.S.; Johnson, G.V.W.; MacDonald, M.; Detloff, P.J.; Lesort, M. Mutant huntingtin directly increases susceptibility of mitochondria to the calcium-induced permeability transition and cytochrome c release. Hum. Mol. Genet., 2004, 13(14), 1407-1420.
[http://dx.doi.org/10.1093/hmg/ddh162] [PMID: 15163634]
[108]
Mirandola, S.R.; Melo, D.R.; Saito, A.; Castilho, R.F. 3-nitropropionic acid-induced mitochondrial permeability transition: Comparative study of mitochondria from different tissues and brain regions. J. Neurosci. Res., 2010, 88(3), 630-639.
[PMID: 19795369]
[109]
Brustovetsky, N.; Brustovetsky, T.; Purl, K.J.; Capano, M.; Crompton, M.; Dubinsky, J.M. Increased susceptibility of striatal mitochondria to calcium-induced permeability transition. J. Neurosci., 2003, 23(12), 4858-4867.
[http://dx.doi.org/10.1523/JNEUROSCI.23-12-04858.2003] [PMID: 12832508]
[110]
Pérez, M.J.; Quintanilla, R.A. Development or disease: Duality of the mitochondrial permeability transition pore. Dev. Biol., 2017, 426(1), 1-7.
[http://dx.doi.org/10.1016/j.ydbio.2017.04.018] [PMID: 28457864]
[111]
Li, V.; Brustovetsky, T.; Brustovetsky, N. Role of cyclophilin D-dependent mitochondrial permeability transition in glutamate-induced calcium deregulation and excitotoxic neuronal death. Exp. Neurol., 2009, 218(2), 171-182.
[http://dx.doi.org/10.1016/j.expneurol.2009.02.007] [PMID: 19236863]
[112]
Amigo, I.; Menezes-Filho, S.L.; Luévano-Martínez, L.A.; Chausse, B.; Kowaltowski, A.J. Caloric restriction increases brain mitochondrial calcium retention capacity and protects against excitotoxicity. Aging Cell, 2017, 16(1), 73-81.
[http://dx.doi.org/10.1111/acel.12527] [PMID: 27619151]
[113]
Chalmers, S.; Nicholls, D.G. The relationship between free and total calcium concentrations in the matrix of liver and brain mitochondria. J. Biol. Chem., 2003, 278(21), 19062-19070.
[http://dx.doi.org/10.1074/jbc.M212661200] [PMID: 12660243]
[114]
Hyder, F.; Rothman, D.L.; Bennett, M.R. Cortical energy demands of signaling and nonsignaling components in brain are conserved across mammalian species and activity levels. Proc. Natl. Acad. Sci. USA, 2013, 110(9), 3549-3554.
[http://dx.doi.org/10.1073/pnas.1214912110] [PMID: 23319606]
[115]
Barrientos, A.; Fontanesi, F.; Díaz, F. Evaluation of the mitochondrial respiratory chain and oxidative phosphorylation system using polarography and spectrophotometric enzyme assays. Curr. Protoc. Hum. Genet, 2009. Available from: https://onlinelibrary.wiley.com/doi/10.1002/0471142905.hg1903s63
[http://dx.doi.org/10.1002/0471142905.hg1903s63]
[116]
Agbas, A.; Krishnamurthy, P.; Michaelis, M.L.; Michaelis, E.K. Mitochondrial electron transfer cascade enzyme activity assessment in cultured neurons and select brain regions. Curr. Protoc. Toxicol., 2019, 80(1), e73.
[http://dx.doi.org/10.1002/cptx.73] [PMID: 30951613]
[117]
Kirby, D.M.; Thorburn, D.R.; Turnbull, D.M.; Taylor, R.W. Biochemical assays of respiratory chain complex activity. Methods Cell Biol., 2007, 80, 93-119.
[http://dx.doi.org/10.1016/S0091-679X(06)80004-X] [PMID: 17445690]
[118]
Doerrier, C.; Garcia-Souza, L.F.; Krumschnabel, G.; Wohlfarter, Y.; Mészáros, A.T.; Gnaiger, E. High-resolution fluorespirometry and OXPHOS protocols for human cells, permeabilized fibers from small biopsies of muscle, and isolated mitochondria. Methods Mol. Biol., 2018, 1782, 31-70.
[http://dx.doi.org/10.1007/978-1-4939-7831-1_3] [PMID: 29850993]
[119]
Villani, G.; Attardi, G. Polarographic assays of respiratory chain complex activity. Methods Cell Biol., 2007, 80, 121-133.
[http://dx.doi.org/10.1016/S0091-679X(06)80005-1] [PMID: 17445691]
[120]
Connolly, N.M.C.; Theurey, P.; Adam-Vizi, V.; Bazan, N.G.; Bernardi, P.; Bolaños, J.P.; Culmsee, C.; Dawson, V.L.; Deshmukh, M.; Duchen, M.R.; Düssmann, H.; Fiskum, G.; Galindo, M.F.; Hardingham, G.E.; Hardwick, J.M.; Jekabsons, M.B.; Jonas, E.A.; Jordán, J.; Lipton, S.A.; Manfredi, G.; Mattson, M.P.; McLaughlin, B.; Methner, A.; Murphy, A.N.; Murphy, M.P.; Nicholls, D.G.; Polster, B.M.; Pozzan, T.; Rizzuto, R.; Satrústegui, J.; Slack, R.S.; Swanson, R.A.; Swerdlow, R.H.; Will, Y.; Ying, Z.; Joselin, A.; Gioran, A.; Moreira Pinho, C.; Watters, O.; Salvucci, M.; Llorente-Folch, I.; Park, D.S.; Bano, D.; Ankarcrona, M.; Pizzo, P.; Prehn, J.H.M. Guidelines on experimental methods to assess mitochondrial dysfunction in cellular models of neurodegenerative diseases. Cell Death Differ., 2018, 25(3), 542-572.
[http://dx.doi.org/10.1038/s41418-017-0020-4] [PMID: 29229998]
[121]
Morava, E; Rodenburg, RJ; Hol, F; De Vries, M; Janssen, A; Van Den Heuvel, L Clinical and biochemical characteristics in patients with a high mutant load of the mitochondrial T8993G/C mutations. Am J Med Genet., 2006, 140 A, 863-8.
[122]
Haraux, F.; Lombès, A. Kinetic analysis of ATP hydrolysis by complex V in four murine tissues: Towards an assay suitable for clinical diagnosis. PLoS One, 2019, 14(8), e0221886.
[http://dx.doi.org/10.1371/journal.pone.0221886] [PMID: 31461494]
[123]
Bosetti, F.; Brizzi, F.; Barogi, S.; Mancuso, M.; Siciliano, G.; Tendi, E.A.; Murri, L.; Rapoport, S.I.; Solaini, G. Cytochrome c oxidase and mitochondrial F1F0-ATPase (ATP synthase) activities in platelets and brain from patients with Alzheimer’s disease. Neurobiol. Aging, 2002, 23(3), 371-376.
[http://dx.doi.org/10.1016/S0197-4580(01)00314-1] [PMID: 11959398]
[124]
Katewa, S.D.; Katyare, S.S. A simplified method for inorganic phosphate determination and its application for phosphate analysis in enzyme assays. Anal. Biochem., 2003, 323(2), 180-187.
[http://dx.doi.org/10.1016/j.ab.2003.08.024] [PMID: 14656523]
[125]
Valenti, D.; Tullo, A.; Caratozzolo, M.F.; Merafina, R.S.; Scartezzini, P.; Marra, E.; Vacca, R.A. Impairment of F1F0-ATPase, adenine nucleotide translocator and adenylate kinase causes mitochondrial energy deficit in human skin fibroblasts with chromosome 21 trisomy. Biochem. J., 2010, 431(2), 299-310.
[http://dx.doi.org/10.1042/BJ20100581] [PMID: 20698827]
[126]
Vives-Bauza, C.; Yang, L.; Manfredi, G. Assay of mitochondrial ATP synthesis in animal cells and tissues. Methods Cell Biol., 2007, 80, 155-171.
[http://dx.doi.org/10.1016/S0091-679X(06)80007-5] [PMID: 17445693]
[127]
Chance, B.; Williams, G.R. Respiratory enzymes in oxidative phosphorylation. VI. The effects of adenosine diphosphate on azide-treated mitochondria. J. Biol. Chem., 1956, 221(1), 477-489.
[http://dx.doi.org/10.1016/S0021-9258(18)65266-4] [PMID: 13345836]
[128]
Gnaiger, E. Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir. Physiol., 2001, 128(3), 277-297.
[http://dx.doi.org/10.1016/S0034-5687(01)00307-3] [PMID: 11718759]
[129]
Brand, M.D.; Nicholls, D.G. Assessing mitochondrial dysfunction in cells. Biochem. J., 2011, 435(2), 297-312.
[http://dx.doi.org/10.1042/BJ20110162] [PMID: 21726199]
[130]
Silva, A.M.; Oliveira, P.J. Evaluation of respiration with clark type electrode in Isolated mitochondria and permeabilized animal cells. Methods Mol. Biol., 2018, 1782, 7-29.
[http://dx.doi.org/10.1007/978-1-4939-7831-1_2] [PMID: 29850992]
[131]
Diepart, C.; Verrax, J.; Calderon, P.B.; Feron, O.; Jordan, B.F.; Gallez, B. Comparison of methods for measuring oxygen consumption in tumor cells in vitro. Anal. Biochem., 2010, 396(2), 250-256.
[http://dx.doi.org/10.1016/j.ab.2009.09.029] [PMID: 19766582]
[132]
Hynes, J.; Hill, R.; Papkovsky, D.B. The use of a fluorescence-based oxygen uptake assay in the analysis of cytotoxicity. Toxicol. In Vitro, 2006, 20(5), 785-792.
[http://dx.doi.org/10.1016/j.tiv.2005.11.002] [PMID: 16386874]
[133]
Hynes, J.; Marroquin, L.D.; Ogurtsov, V.I.; Christiansen, K.N.; Stevens, G.J.; Papkovsky, D.B.; Will, Y. Investigation of drug-induced mitochondrial toxicity using fluorescence-based oxygen-sensitive probes. Toxicol. Sci., 2006, 92(1), 186-200.
[http://dx.doi.org/10.1093/toxsci/kfj208] [PMID: 16638925]
[134]
Hynes, J.; Natoli, E.; Will, Y. Fluorescent pH and oxygen probes of the assessment of mitochondrial toxicity in isolated mitochondria and whole cells, 2009, Chapter 2: Unit 2.16.
[http://dx.doi.org/10.1002/0471140856.tx0216s40]
[135]
Iuso, A.; Repp, B.; Biagosch, C.; Terrile, C.; Prokisch, H. Assessing mitochondrial bioenergetics in isolated mitochondria from various mouse tissues using Seahorse XF96 analyzer. Methods Mol. Biol., 2017, 1567, 217-230.
[http://dx.doi.org/10.1007/978-1-4939-6824-4_13] [PMID: 28276021]
[136]
Sriram, G.; Martinez, J.A.; McCabe, E.R.B.; Liao, J.C.; Dipple, K.M. Single-gene disorders: What role could moonlighting enzymes play? Am. J. Hum. Genet., 2005, 76(6), 911-924.
[http://dx.doi.org/10.1086/430799] [PMID: 15877277]
[137]
Acin-Perez, R.; Benincá, C.; Shabane, B.; Shirihai, O.S.; Stiles, L. Utilization of human samples for assessment of mitochondrial bioenergetics: Gold standards, limitations, and future perspectives. Life (Basel), 2021, 11(9), 949.
[http://dx.doi.org/10.3390/life11090949] [PMID: 34575097]
[138]
Reisch, A.S.; Elpeleg, O. Biochemical assays for mitochondrial activity: Assays of TCA cycle enzymes and PDHc. Methods Cell Biol., 2007, 80, 199-222.
[http://dx.doi.org/10.1016/S0091-679X(06)80010-5] [PMID: 17445696]
[139]
Andreyev, A.Y.; Kushnareva, Y.E.; Starkov, A.A. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc.), 2005, 70(2), 200-214.
[http://dx.doi.org/10.1007/s10541-005-0102-7] [PMID: 15807660]
[140]
Angelova, P.R.; Abramov, A.Y. Role of mitochondrial ROS in the brain: From physiology to neurodegeneration. FEBS Lett., 2018, 592(5), 692-702.
[http://dx.doi.org/10.1002/1873-3468.12964] [PMID: 29292494]
[141]
Cenini, G.; Lloret, A.; Cascella, R. Oxidative stress in neurodegenerative diseases: From a mitochondrial point of view. Oxid. Med. Cell. Longev., 2019, 2019, 1-18.
[http://dx.doi.org/10.1155/2019/2105607] [PMID: 31210837]
[142]
Armstrong, J.S.; Whiteman, M. Measurement of reactive oxygen species in cells and mitochondria. Methods Cell Biol., 2007, 80, 355-377.
[http://dx.doi.org/10.1016/S0091-679X(06)80018-X] [PMID: 17445704]
[143]
Zhao, R.Z.; Jiang, S.; Zhang, L.; Yu, Z.B. Mitochondrial electron transport chain, ROS generation and uncoupling (Review). Int. J. Mol. Med., 2019, 44(1), 3-15.
[http://dx.doi.org/10.3892/ijmm.2019.4188] [PMID: 31115493]
[144]
Starkov, A.A. Measurement of mitochondrial ROS production. Methods Mol. Biol., 2010, 648, 245-255.
[http://dx.doi.org/10.1007/978-1-60761-756-3_16] [PMID: 20700717]
[145]
Zhou, M.; Diwu, Z.; Panchuk-Voloshina, N.; Haugland, R.P. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal. Biochem., 1997, 253(2), 162-168.
[http://dx.doi.org/10.1006/abio.1997.2391] [PMID: 9367498]
[146]
Forman, H.J.; Fridovich, I. Superoxide dismutase: A comparison of rate constants. Arch. Biochem. Biophys., 1973, 158(1), 396-400.
[http://dx.doi.org/10.1016/0003-9861(73)90636-X] [PMID: 4354035]
[147]
Misra, H.P.; Fridovich, I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem., 1972, 247(10), 3170-3175.
[http://dx.doi.org/10.1016/S0021-9258(19)45228-9] [PMID: 4623845]
[148]
Brown, G.C. Nitric oxide as a competitive inhibitor of oxygen consumption in the mitochondrial respiratory chain. Acta Physiol. Scand., 2000, 168(4), 667-674.
[http://dx.doi.org/10.1046/j.1365-201x.2000.00718.x] [PMID: 10759603]
[149]
Navarro, A.; Boveris, A.; Bández, M.J.; Sánchez-Pino, M.J.; Gómez, C.; Muntané, G.; Ferrer, I. Human brain cortex: Mitochondrial oxidative damage and adaptive response in Parkinson disease and in dementia with Lewy bodies. Free Radic. Biol. Med., 2009, 46(12), 1574-1580.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.03.007] [PMID: 19298851]
[150]
Boveris, A.; Arnaiz, S.L.; Bustamante, J.; Alvarez, S.; Valdez, L.; Boveris, A.D.; Navarro, A. Pharmacological regulation of mitochondrial nitric oxide synthase. Methods Enzymol., 2002, 359, 328-339.
[http://dx.doi.org/10.1016/S0076-6879(02)59196-5] [PMID: 12481584]
[151]
Katalinic, V.; Modun, D.; Music, I.; Boban, M. Gender differences in antioxidant capacity of rat tissues determined by 2, 2′-azinobis (3-ethylbenzothiazoline 6-sulfonate; ABTS) and ferric reducing antioxidant power (FRAP) assays. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2005, 140(1), 47-52.
[http://dx.doi.org/10.1016/j.cca.2005.01.005] [PMID: 15792622]
[152]
Shea, T.B.; Rogers, E.; Ashline, D.; Ortiz, D.; Sheu, M.S. Quantification of antioxidant activity in brain tissue homogenates using the ‘total equivalent antioxidant capacity’. J. Neurosci. Methods, 2003, 125(1-2), 55-58.
[http://dx.doi.org/10.1016/S0165-0270(03)00028-1] [PMID: 12763230]
[153]
Siqueira, I.R.; Fochesatto, C.; Andrade, A.; Santos, M.; Hagen, M.; Bello-Klein, A.; Netto, C.A. Total antioxidant capacity is impaired in different structures from aged rat brain. Int. J. Dev. Neurosci., 2005, 23(8), 663-671.
[http://dx.doi.org/10.1016/j.ijdevneu.2005.03.001] [PMID: 16298100]
[154]
Sofic, E.; Sapcanin, A.; Tahirovic, I.; Gavrankapetanovic, I.; Jellinger, K.; Reynolds, G.P.; Tatschner, T.; Riederer, P. Antioxidant capacity in postmortem brain tissues of Parkinson’s and Alzheimer’s diseases. J. Neural Transm. Suppl., 2006, (71), 39-43.
[http://dx.doi.org/10.1007/978-3-211-33328-0_5] [PMID: 17447414]
[155]
Raukas, M.; Rebane, R.; Mahlapuu, R.; Jefremov, V.; Zilmer, K.; Karelson, E.; Bogdanovic, N.; Zilmer, M. Mitochondrial oxidative stress index, activity of redox-sensitive aconitase and effects of endogenous anti- and pro-oxidants on its activity in control, Alzheimer’s disease and Swedish Familial Alzheimer’s disease brain. Free Radic. Res., 2012, 46(12), 1490-1495.
[http://dx.doi.org/10.3109/10715762.2012.728286] [PMID: 22962855]
[156]
Cooper, A.J.L.; Kristal, B.S. Multiple roles of glutathione in the central nervous system. Biol. Chem., 1997, 378(8), 793-802.
[PMID: 9377474]
[157]
Dringen, R.; Hirrlinger, J. Glutathione pathways in the brain. Biol. Chem., 2003, 384(4), 505-516.
[http://dx.doi.org/10.1515/BC.2003.059] [PMID: 12751781]
[158]
Nolfi-Donegan, D.; Braganza, A.; Shiva, S. Mitochondrial electron transport chain: Oxidative phosphorylation, oxidant production, and methods of measurement. Redox Biol., 2020, 37, 101674.
[http://dx.doi.org/10.1016/j.redox.2020.101674] [PMID: 32811789]
[159]
Iskusnykh, I.Y.; Zakharova, A.A.; Pathak, D. Glutathione in brain disorders and aging. Molecules, 2022, 27(1), 324.
[http://dx.doi.org/10.3390/molecules27010324] [PMID: 35011559]
[160]
Sun, Y.; Oberley, L.W.; Li, Y. A simple method for clinical assay of superoxide dismutase. Clin. Chem., 1988, 34(3), 497-500.
[http://dx.doi.org/10.1093/clinchem/34.3.497] [PMID: 3349599]
[161]
Bannister, J.V.; Calabrese, L. Assays for superoxide dismutase. Methods Biochem. Anal., 1987, 32, pp. 279-312. Available from: https://onlinelibrary.wiley.com/doi/10.1002/9780470110539.ch5
[PMID: 3033431]
[162]
Elstner, E.F.; Heupel, A. Inhibition of nitrite formation from hydroxylammoniumchloride: A simple assay for superoxide dismutase. Anal. Biochem., 1976, 70(2), 616-620.
[http://dx.doi.org/10.1016/0003-2697(76)90488-7] [PMID: 817618]
[163]
Vives-Bauza, C.; Starkov, A.; Garcia-Arumi, E. Measurements of the antioxidant enzyme activities of superoxide dismutase, catalase, and glutathione peroxidase. Methods Cell Biol., 2007, 80, 379-393.
[http://dx.doi.org/10.1016/S0091-679X(06)80019-1] [PMID: 17445705]
[164]
Harbauer, A.B. Mitochondrial health maintenance in axons. Biochem. Soc. Trans., 2017, 45(5), 1045-1052.
[http://dx.doi.org/10.1042/BST20170023] [PMID: 28778985]
[165]
Liang, Y. Mitochondrial support and local translation of mitochondrial proteins in synaptic plasticity and function. Histol. Histopathol., 2021, 36(10), 1007-1019.
[PMID: 34032272]
[166]
Fernández-Silva, P.; Acín-Pérez, R.; Fernández-Vizarra, E.; Pérez-Martos, A.; Enriquez, J.A. In vivo and in organello analyses of mitochondrial translation. Methods Cell Biol., 2007, 80, 571-588.
[http://dx.doi.org/10.1016/S0091-679X(06)80028-2] [PMID: 17445714]
[167]
Ahmad, F.; Salahuddin, M.; Alsamman, K.; Herzallah, H.K.; Al-Otaibi, S.T. Neonatal maternal deprivation impairs localized de novo activity-induced protein translation at the synapse in the rat hippocampus. Biosci. Rep., 2018, 38(3), BSR20180118.
[http://dx.doi.org/10.1042/BSR20180118] [PMID: 29700212]
[168]
Ahmad, F.; Singh, K.; Das, D.; Gowaikar, R.; Shaw, E.; Ramachandran, A.; Rupanagudi, K.V.; Kommaddi, R.P.; Bennett, D.A.; Ravindranath, V. Reactive oxygen species-mediated loss of synaptic Akt1 signaling leads to deficient activity-dependent protein translation early in Alzheimer’s disease. Antioxid. Redox Signal., 2017, 27(16), 1269-1280.
[http://dx.doi.org/10.1089/ars.2016.6860] [PMID: 28264587]
[169]
Ahmad, F.; Salahuddin, M.; Alsamman, K.; AlMulla, A.A.; Salama, K.F. Developmental lead (Pb)-induced deficits in hippocampal protein translation at the synapses are ameliorated by ascorbate supplementation. Neuropsychiatr. Dis. Treat., 2018, 14, 3289-3298.
[http://dx.doi.org/10.2147/NDT.S174083] [PMID: 30568451]
[170]
Côté, C.; Poirier, J.; Boulet, D. Expression of the mammalian mitochondrial genome. Stability of mitochondrial translation products as a function of membrane potential. J. Biol. Chem., 1989, 264(15), 8487-8490.
[PMID: 2722783]
[171]
Almajan, E.R.; Richter, R.; Paeger, L.; Martinelli, P.; Barth, E.; Decker, T.; Larsson, N.G.; Kloppenburg, P.; Langer, T.; Rugarli, E.I. AFG3L2 supports mitochondrial protein synthesis and Purkinje cell survival. J. Clin. Invest., 2012, 122(11), 4048-4058.
[http://dx.doi.org/10.1172/JCI64604] [PMID: 23041622]
[172]
Formosa, L.E.; Hofer, A.; Tischner, C.; Wenz, T.; Ryan, M.T. Translation and assembly of radiolabeled mitochondrial DNA-encoded protein subunits from cultured cells and isolated mitochondria. Methods Mol. Biol., 2016, 1351, 115-129.
[http://dx.doi.org/10.1007/978-1-4939-3040-1_9] [PMID: 26530678]
[173]
Prem, P.N.; Kurian, G.A. High-fat diet increased oxidative stress and mitochondrial dysfunction induced by renal ischemia-reperfusion injury in rat. Front. Physiol., 2021, 12, 715693.
[http://dx.doi.org/10.3389/fphys.2021.715693] [PMID: 34539439]
[174]
Estell, C.; Stamatidou, E.; El-Messeiry, S.; Hamilton, A. In situ imaging of mitochondrial translation shows weak correlation with nucleoid DNA intensity and no suppression during mitosis. J. Cell Sci., 2017, 130(24), jcs.206714.
[http://dx.doi.org/10.1242/jcs.206714] [PMID: 29122981]
[175]
Konovalova, S.; Hilander, T.; Loayza-Puch, F.; Rooijers, K.; Agami, R.; Tyynismaa, H. Exposure to arginine analog canavanine induces aberrant mitochondrial translation products, mitoribosome stalling, and instability of the mitochondrial proteome. Int. J. Biochem. Cell Biol., 2015, 65, 268-74.
[http://dx.doi.org/10.1016/j.biocel.2015.06.018]
[176]
Villeneuve, L.M.; Stauch, K.L.; Fox, H.S. Proteomic analysis of the mitochondria from embryonic and postnatal rat brains reveals response to developmental changes in energy demands. J. Proteomics, 2014, 109, 228-239.
[http://dx.doi.org/10.1016/j.jprot.2014.07.011] [PMID: 25046836]
[177]
Abyadeh, M.; Gupta, V.; Chitranshi, N.; Gupta, V.; Wu, Y.; Saks, D.; Wander Wall, R.; Fitzhenry, M.J.; Basavarajappa, D.; You, Y.; Salekdeh, G.H.; Haynes, P.; Graham, S.L.; Mirzaei, M. Mitochondrial dysfunction in Alzheimer’s disease-a proteomics perspective. Expert Rev. Proteomics, 2021, 18(4), 295-304.
[http://dx.doi.org/10.1080/14789450.2021.1918550] [PMID: 33874826]
[178]
Broadwater, L.; Pandit, A.; Clements, R.; Azzam, S.; Vadnal, J.; Sulak, M.; Yong, V.W.; Freeman, E.J.; Gregory, R.B.; McDonough, J. Analysis of the mitochondrial proteome in multiple sclerosis cortex. Biochim. Biophys. Acta Mol. Basis Dis., 2011, 1812(5), 630-641.
[http://dx.doi.org/10.1016/j.bbadis.2011.01.012] [PMID: 21295140]
[179]
Fu, H.; Li, W.; Liu, Y.; Lao, Y.; Liu, W.; Chen, C.; Yu, H.; Lee, N.T.K.; Chang, D.C.; Li, P.; Pang, Y.; Tsim, K.W.K.; Li, M.; Han, Y. Mitochondrial proteomic analysis and characterization of the intracellular mechanisms of bis(7)-tacrine in protecting against glutamate-induced excitotoxicity in primary cultured neurons. J. Proteome Res., 2007, 6(7), 2435-2446.
[http://dx.doi.org/10.1021/pr060615g] [PMID: 17530875]
[180]
Pienaar, I.S.; Schallert, T.; Hattingh, S.; Daniels, W.M.U. Behavioral and quantitative mitochondrial proteome analyses of the effects of simvastatin: implications for models of neural degeneration. J. Neural Transm. (Vienna), 2009, 116(7), 791-806.
[http://dx.doi.org/10.1007/s00702-009-0247-4] [PMID: 19504041]
[181]
Kabiri, Y.; von Toerne, C.; Fontes, A.; Knolle, P.A.; Zischka, H. Isolation and purification of mitochondria from cell culture for proteomic analyses. Methods Mol. Biol., 2021, 2261, 411-419.
[http://dx.doi.org/10.1007/978-1-0716-1186-9_25] [PMID: 33421004]
[182]
Pienaar, I.S.; Dexter, D.T.; Burkhard, P.R. Mitochondrial proteomics as a selective tool for unraveling Parkinson’s disease pathogenesis. Expert Rev. Proteomics, 2010, 7(2), 205-226.
[http://dx.doi.org/10.1586/epr.10.8] [PMID: 20377388]
[183]
Ahmad, F.; Haque, S.; Chavda, V.; Ashraf, G.M. Recent advances in synaptosomal proteomics in Alzheimer’s Disease. Curr. Protein Pept. Sci., 2021, 22(6), 479-492.
[http://dx.doi.org/10.2174/1389203722666210618110233] [PMID: 34148536]
[184]
Butterfield, D.A.; Palmieri, E.M.; Castegna, A. Clinical implications from proteomic studies in neurodegenerative diseases: Lessons from mitochondrial proteins. Expert Rev. Proteomics, 2016, 13(3), 259-274.
[http://dx.doi.org/10.1586/14789450.2016.1149470] [PMID: 26837425]
[185]
Chen, X.; Li, J.; Hou, J.; Xie, Z.; Yang, F. Mammalian mitochondrial proteomics: Insights into mitochondrial functions and mitochondria-related diseases. Expert Rev. Proteomics, 2010, 7(3), 333-345.
[http://dx.doi.org/10.1586/epr.10.22] [PMID: 20536306]
[186]
Butterfield, D.A.; Boyd-Kimball, D. Mitochondrial oxidative and nitrosative stress and Alzheimer disease. Antioxidants, 2020, 9(9), 818.
[http://dx.doi.org/10.3390/antiox9090818] [PMID: 32887505]
[187]
Jiang, Y.; Wang, X. Comparative mitochondrial proteomics: Perspective in human diseases. J. Hematol. Oncol., 2012, 5(1), 11.
[http://dx.doi.org/10.1186/1756-8722-5-11] [PMID: 22424240]
[188]
Ingram, T.; Chakrabarti, L. Proteomic profiling of mitochondria: What does it tell us about the ageing brain? Aging (Albany NY), 2016, 8(12), 3161-3179.
[http://dx.doi.org/10.18632/aging.101131] [PMID: 27992860]
[189]
Zanfardino, P.; Doccini, S.; Santorelli, F.M.; Petruzzella, V. Tackling dysfunction of mitochondrial bioenergetics in the brain. Int. J. Mol. Sci., 2021, 22(15), 8325.
[http://dx.doi.org/10.3390/ijms22158325] [PMID: 34361091]
[190]
Fountoulakis, M. Application of proteomics technologies in the investigation of the brain. Mass Spectrom. Rev., 2004, 23(4), 231-258.
[http://dx.doi.org/10.1002/mas.10075] [PMID: 15133836]
[191]
Gu, F.; Chauhan, V.; Kaur, K.; Brown, W.T.; LaFauci, G.; Wegiel, J.; Chauhan, A. Alterations in mitochondrial DNA copy number and the activities of electron transport chain complexes and pyruvate dehydrogenase in the frontal cortex from subjects with autism. Transl. Psychiatry, 2013, 3(9), e299.
[http://dx.doi.org/10.1038/tp.2013.68] [PMID: 24002085]

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