1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Analytical Chemistry
  4. Volume 15, 2022
  5. Article

Annual Review of Analytical Chemistry

Volume 15, 2022

Analysis of Mitochondria by Single-Organelle Resolution

Abstract

Cellular organelles are highly specialized compartments with distinct functions. With the increasing resolution of detection methods, it is becoming clearer that same organelles may have different functions or properties not only within different cell populations of a tissue but also within the same cell. Dysfunction or altered function affects the organelle itself and may also lead to malignancies or undesirable cell death. To understand cellular function or dysfunction, it is therefore necessary to analyze cellular components at the single-organelle level. Here, we review the recent advances in analyzing cellular function at single-organelle resolution using high-parameter flow cytometry or multicolor confocal microscopy. We focus on the analysis of mitochondria, as they are organelles at the crossroads of various cellular signaling pathways and functions. However, most of the applied methods/technologies are transferable to any other organelle, such as the endoplasmic reticulum, lysosomes, or peroxisomes.

Keyword(s): flow cytometry, microscopy, mitochondria, organelles, single-organelle analysis
Loading

Article metrics loading...

/content/journals/10.1146/annurev-anchem-061020-111722
2022-06-13
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/anchem/15/1/annurev-anchem-061020-111722.html?itemId=/content/journals/10.1146/annurev-anchem-061020-111722&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Lang BF, Gray MW, Burger G. 1999. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33:351–97
     [Google Scholar]
  2. 2.
    West AP, Shadel GS, Ghosh S. 2011. Mitochondria in innate immune responses. Nat. Rev. Immunol. 11:389–402
     [Google Scholar]
  3. 3.
    Wanderoy S, Hees JT, Klesse R, Edlich F, Harbauer AB. 2020. Kill one or kill the many: interplay between mitophagy and apoptosis. Biol. Chem. 402:73–88
     [Google Scholar]
  4. 4.
    Attwell D, Laughlin SB. 2001. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 21:1133–45
     [Google Scholar]
  5. 5.
    Belanger M, Allaman I, Magistretti PJ. 2011. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14:724–38
     [Google Scholar]
  6. 6.
    Overly CC, Rieff HI, Hollenbeck PJ. 1996. Organelle motility and metabolism in axons versus dendrites of cultured hippocampal neurons. J. Cell Sci. 109:Part 5971–80
     [Google Scholar]
  7. 7.
    Stauch KL, Purnell PR, Fox HS. 2014. Quantitative proteomics of synaptic and nonsynaptic mitochondria: insights for synaptic mitochondrial vulnerability. J. Proteome Res. 13:2620–36
     [Google Scholar]
  8. 8.
    Lewis TL Jr., Kwon SK, Lee A, Shaw R, Polleux F. 2018. MFF-dependent mitochondrial fission regulates presynaptic release and axon branching by limiting axonal mitochondria size. Nat. Commun. 9:5008
     [Google Scholar]
  9. 9.
    Divakaruni SS, Van Dyke AM, Chandra R, LeGates TA, Contreras M et al. 2018. Long-term potentiation requires a rapid burst of dendritic mitochondrial fission during induction. Neuron 100:860–75.e7
     [Google Scholar]
  10. 10.
    Wiesner RJ, Ruegg JC, Morano I. 1992. Counting target molecules by exponential polymerase chain reaction: copy number of mitochondrial DNA in rat tissues. Biochem. Biophys. Res. Commun. 183:553–59
     [Google Scholar]
  11. 11.
    Mansouri A, Gattolliat CH, Asselah T. 2018. Mitochondrial dysfunction and signaling in chronic liver diseases. Gastroenterology 155:629–47
     [Google Scholar]
  12. 12.
    Jost PJ, Grabow S, Gray D, McKenzie MD, Nachbur U et al. 2009. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 460:1035–39
     [Google Scholar]
  13. 13.
    Ernster L, Schatz G. 1981. Mitochondria: a historical review. J. Cell Biol. 91:227s–55s
     [Google Scholar]
  14. 14.
    Faitg J, Davey T, Turnbull DM, White K, Vincent AE. 2020. Mitochondrial morphology and function: two for the price of one!. J. Microsc. 278:89–106
     [Google Scholar]
  15. 15.
    Quintana A, Schwindling C, Wenning AS, Becherer U, Rettig J et al. 2007. T cell activation requires mitochondrial translocation to the immunological synapse. PNAS 104:14418–23
     [Google Scholar]
  16. 16.
    Cieri D, Vicario M, Giacomello M, Vallese F, Filadi R et al. 2018. SPLICS: a split green fluorescent protein-based contact site sensor for narrow and wide heterotypic organelle juxtaposition. Cell Death Differ. 25:1131–45
     [Google Scholar]
  17. 17.
    Cottet-Rousselle C, Ronot X, Leverve X, Mayol JF. 2011. Cytometric assessment of mitochondria using fluorescent probes. Cytometry A 79:405–25
     [Google Scholar]
  18. 18.
    Zhang S, Zhu S, Yang L, Zheng Y, Gao M et al. 2012. High-throughput multiparameter analysis of individual mitochondria. Anal. Chem. 84:6421–28
     [Google Scholar]
  19. 19.
    Schneider A, Kurz S, Manske K, Janas M, Heikenwalder M et al. 2019. Single organelle analysis to characterize mitochondrial function and crosstalk during viral infection. Sci. Rep. 9:8492
     [Google Scholar]
  20. 20.
    Ma L, Zhu S, Tian Y, Zhang W, Wang S et al. 2016. Label-free analysis of single viruses with a resolution comparable to that of electron microscopy and the throughput of flow cytometry. Angew. Chem. Int. Ed. 55:10239–43
     [Google Scholar]
  21. 21.
    Rajotte D, Stearns CD, Kabcenell AK. 2003. Isolation of mast cell secretory lysosomes using flow cytometry. Cytometry A 55:94–101
     [Google Scholar]
  22. 22.
    Degtyarev M, Reichelt M, Lin K. 2014. Novel quantitative autophagy analysis by organelle flow cytometry after cell sonication. PLOS ONE 9:e87707
     [Google Scholar]
  23. 23.
    Fialka I, Steinlein P, Ahorn H, Bock G, Burbelo PD et al. 1999. Identification of syntenin as a protein of the apical early endocytic compartment in Madin-Darby canine kidney cells. J. Biol. Chem. 274:26233–39
     [Google Scholar]
  24. 24.
    MacDonald JA, Bothun AM, Annis SN, Sheehan H, Ray S et al. 2019. A nanoscale, multi-parametric flow cytometry-based platform to study mitochondrial heterogeneity and mitochondrial DNA dynamics. Commun. Biol. 2:258
     [Google Scholar]
  25. 25.
    Fecher C, Trovò L, Müller SA, Snaidero N, Wettmarshausen J et al. 2019. Cell-type-specific profiling of brain mitochondria reveals functional and molecular diversity. Nat. Neurosci. 22:1731–42
     [Google Scholar]
  26. 26.
    Wyant GA, Abu-Remaileh M, Frenkel EM, Laqtom NN, Dharamdasani V et al. 2018. NUFIP1 is a ribosome receptor for starvation-induced ribophagy. Science 360:751–58
     [Google Scholar]
  27. 27.
    Chen WW, Freinkman E, Wang T, Birsoy K, Sabatini DM. 2016. Absolute quantification of matrix metabolites reveals the dynamics of mitochondrial metabolism. Cell 166:1324–37.e11
     [Google Scholar]
  28. 28.
    Abu-Remaileh M, Wyant GA, Kim C, Laqtom NN, Abbasi M et al. 2017. Lysosomal metabolomics reveals V-ATPase- and mTOR-dependent regulation of amino acid efflux from lysosomes. Science 358:807–13
     [Google Scholar]
  29. 29.
    Pflugradt R, Schmidt U, Landenberger B, Sanger T, Lutz-Bonengel S. 2011. A novel and effective separation method for single mitochondria analysis. Mitochondrion 11:308–14
     [Google Scholar]
  30. 30.
    Morris J, Na YJ, Zhu H, Lee JH, Giang H et al. 2017. Pervasive within-mitochondrion single-nucleotide variant heteroplasmy as revealed by single-mitochondrion sequencing. Cell Rep. 21:2706–13
     [Google Scholar]
  31. 31.
    Presley AD, Fuller KM, Arriaga EA. 2003. MitoTracker Green labeling of mitochondrial proteins and their subsequent analysis by capillary electrophoresis with laser-induced fluorescence detection. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 793:141–50
     [Google Scholar]
  32. 32.
    Friedman JR, Nunnari J. 2014. Mitochondrial form and function. Nature 505:335–43
     [Google Scholar]
  33. 33.
    Liesa M, Shirihai OS. 2013. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 17:491–506
     [Google Scholar]
  34. 34.
    Szabadkai G, Simoni AM, Chami M, Wieckowski MR, Youle RJ, Rizzuto R. 2004. Drp-1-dependent division of the mitochondrial network blocks intraorganellar Ca2+ waves and protects against Ca2+-mediated apoptosis. Mol. Cell 16:59–68
     [Google Scholar]
  35. 35.
    Suzuki R, Hotta K, Oka K. 2018. Transitional correlation between inner-membrane potential and ATP levels of neuronal mitochondria. Sci. Rep. 8:2993
     [Google Scholar]
  36. 36.
    Wolf DM, Segawa M, Kondadi AK, Anand R, Bailey ST et al. 2019. Individual cristae within the same mitochondrion display different membrane potentials and are functionally independent. EMBO J. 38:e101056
     [Google Scholar]
  37. 37.
    Sivandzade F, Bhalerao A, Cucullo L. 2019. Analysis of the mitochondrial membrane potential using the cationic JC-1 dye as a sensitive fluorescent probe. Bio Protoc. 9:e3128
     [Google Scholar]
  38. 38.
    Perry SW, Norman JP, Barbieri J, Brown EB, Gelbard HA. 2011. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. BioTechniques 50:98–115
     [Google Scholar]
  39. 39.
    Jung DW, Davis MH, Brierley GP. 1989. Estimation of matrix pH in isolated heart mitochondria using a fluorescent probe. Anal. Biochem. 178:348–54
     [Google Scholar]
  40. 40.
    Bencina M. 2013. Illumination of the spatial order of intracellular pH by genetically encoded pH-sensitive sensors. Sensors 13:16736–58
     [Google Scholar]
  41. 41.
    Miesenbock G, De Angelis DA, Rothman JE 1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192–95
     [Google Scholar]
  42. 42.
    Orij R, Postmus J, Ter Beek A, Brul S, Smits GJ 2009. In vivo measurement of cytosolic and mitochondrial pH using a pH-sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiology 155:268–78
     [Google Scholar]
  43. 43.
    Jankowski A, Kim JH, Collins RF, Daneman R, Walton P, Grinstein S 2001. In situ measurements of the pH of mammalian peroxisomes using the fluorescent protein pHluorin. J. Biol. Chem. 276:48748–53
     [Google Scholar]
  44. 44.
    Reifenrath M, Boles E. 2018. A superfolder variant of pH-sensitive pHluorin for in vivo pH measurements in the endoplasmic reticulum. Sci. Rep. 8:11985
     [Google Scholar]
  45. 45.
    Santo-Domingo J, Giacomello M, Poburko D, Scorrano L, Demaurex N. 2013. OPA1 promotes pH flashes that spread between contiguous mitochondria without matrix protein exchange. EMBO J. 32:1927–40
     [Google Scholar]
  46. 46.
    Picard M, Sandi C. 2021. The social nature of mitochondria: implications for human health. Neurosci. Biobehav. Rev. 120:595–610
     [Google Scholar]
  47. 47.
    Katayama H, Kogure T, Mizushima N, Yoshimori T, Miyawaki A. 2011. A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem. Biol. 18:1042–52
     [Google Scholar]
  48. 48.
    Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA et al. 2007. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282:24131–45
     [Google Scholar]
  49. 49.
    Castillo K, Valenzuela V, Matus S, Nassif M, Onate M et al. 2013. Measurement of autophagy flux in the nervous system in vivo. Cell Death. Dis. 4:e917
     [Google Scholar]
  50. 50.
    An H, Ordureau A, Korner M, Paulo JA, Harper JW. 2020. Systematic quantitative analysis of ribosome inventory during nutrient stress. Nature 583:303–9
     [Google Scholar]
  51. 51.
    Yoshii SR, Mizushima N. 2017. Monitoring and measuring autophagy. Int. J. Mol. Sci. 18:1865
     [Google Scholar]
  52. 52.
    Sun N, Yun J, Liu J, Malide D, Liu C et al. 2015. Measuring in vivo mitophagy. Mol. Cell 60:685–96
     [Google Scholar]
  53. 53.
    McWilliams TG, Prescott AR, Allen GF, Tamjar J, Munson MJ et al. 2016. mito-QC illuminates mitophagy and mitochondrial architecture in vivo. J. Cell Biol. 214:333–45
     [Google Scholar]
  54. 54.
    McWilliams TG, Prescott AR, Montava-Garriga L, Ball G, Singh F et al. 2018. Basal mitophagy occurs independently of PINK1 in mouse tissues of high metabolic demand. Cell Metab. 27:439–49.e5
     [Google Scholar]
  55. 55.
    Pickrell AM, Youle RJ. 2015. The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson's disease. Neuron 85:257–73
     [Google Scholar]
  56. 56.
    Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K et al. 2004. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304:1158–60
     [Google Scholar]
  57. 57.
    Paul S, Pickrell AM. 2021. Hidden phenotypes of PINK1/Parkin knockout mice. Biochim. Biophys. Acta Gen. Subj. 1865:129871
     [Google Scholar]
  58. 58.
    Cornelissen T, Vilain S, Vints K, Gounko N, Verstreken P, Vandenberghe W. 2018. Deficiency of parkin and PINK1 impairs age-dependent mitophagy in Drosophila. eLife 7:e35878
     [Google Scholar]
  59. 59.
    Deshwal S, Fiedler KU, Langer T. 2020. Mitochondrial proteases: multifaceted regulators of mitochondrial plasticity. Annu. Rev. Biochem. 89:501–28
     [Google Scholar]
  60. 60.
    Sugiura A, McLelland GL, Fon EA, McBride HM. 2014. A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J. 33:2142–56
     [Google Scholar]
  61. 61.
    Ferree AW, Trudeau K, Zik E, Benador IY, Twig G et al. 2013. MitoTimer probe reveals the impact of autophagy, fusion, and motility on subcellular distribution of young and old mitochondrial protein and on relative mitochondrial protein age. Autophagy 9:1887–96
     [Google Scholar]
  62. 62.
    Li H, Doric Z, Berthet A, Jorgens DM, Nguyen MK et al. 2021. Longitudinal tracking of neuronal mitochondria delineates PINK1/Parkin-dependent mechanisms of mitochondrial recycling and degradation. Sci. Adv. 7:eabf6580
     [Google Scholar]
  63. 63.
    Bomba-Warczak E, Edassery SL, Hark TJ, Savas JN. 2021. Long-lived mitochondrial cristae proteins in mouse heart and brain. J. Cell Biol. 220:e202005193
     [Google Scholar]
  64. 64.
    Berridge MJ, Lipp P, Bootman MD. 2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1:11–21
     [Google Scholar]
  65. 65.
    McCormack JG, Halestrap AP, Denton RM. 1990. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol. Rev. 70:391–425
     [Google Scholar]
  66. 66.
    Schild L, Keilhoff G, Augustin W, Reiser G, Striggow F 2001. Distinct Ca2+ thresholds determine cytochrome c release or permeability transition pore opening in brain mitochondria. FASEB J. 15:565–67
     [Google Scholar]
  67. 67.
    Lampl S, Janas MK, Donakonda S, Brugger M, Lohr K et al. 2020. Reduced mitochondrial resilience enables non-canonical induction of apoptosis after TNF receptor signaling in virus-infected hepatocytes. J. Hepatol. 73:1347–59
     [Google Scholar]
  68. 68.
    Davidson SM, Duchen MR. 2018. Imaging mitochondrial calcium fluxes with fluorescent probes and single- or two-photon confocal microscopy. Methods Mol. Biol. 1782:171–86
     [Google Scholar]
  69. 69.
    Grienberger C, Konnerth A. 2012. Imaging calcium in neurons. Neuron 73:862–85
     [Google Scholar]
  70. 70.
    Suzuki J, Kanemaru K, Iino M. 2016. Genetically encoded fluorescent indicators for organellar calcium imaging. Biophys. J. 111:1119–31
     [Google Scholar]
  71. 71.
    Kwon SK, Sando R 3rd, Lewis TL, Hirabayashi Y, Maximov A, Polleux F. 2016. LKB1 regulates mitochondria-dependent presynaptic calcium clearance and neurotransmitter release properties at excitatory synapses along cortical axons. PLOS Biol. 14:e1002516
     [Google Scholar]
  72. 72.
    Vaccaro V, Devine MJ, Higgs NF, Kittler JT. 2017. Miro1-dependent mitochondrial positioning drives the rescaling of presynaptic Ca2+ signals during homeostatic plasticity. EMBO Rep. 18:231–40
     [Google Scholar]
  73. 73.
    De Vos KJ, Morotz GM, Stoica R, Tudor EL, Lau KF et al. 2012. VAPB interacts with the mitochondrial protein PTPIP51 to regulate calcium homeostasis. Hum. Mol. Genet. 21:1299–311
     [Google Scholar]
  74. 74.
    Suzuki J, Kanemaru K, Ishii K, Ohkura M, Okubo Y, Iino M. 2014. Imaging intraorganellar Ca2+ at subcellular resolution using CEPIA. Nat. Commun. 5:4153
     [Google Scholar]
  75. 75.
    Suzanne M, Steller H. 2013. Shaping organisms with apoptosis. Cell Death Differ. 20:669–75
     [Google Scholar]
  76. 76.
    Nguyen TTM, Gillet G, Popgeorgiev N. 2021. Caspases in the developing central nervous system: apoptosis and beyond. Front. Cell Dev. Biol. 9:702404
     [Google Scholar]
  77. 77.
    Labi V, Erlacher M. 2015. How cell death shapes cancer. Cell Death. Dis. 6:e1675
     [Google Scholar]
  78. 78.
    Barber GN. 2001. Host defense, viruses and apoptosis. Cell Death Differ. 8:113–26
     [Google Scholar]
  79. 79.
    Strasser A, Harris AW, Huang DC, Krammer PH, Cory S 1995. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J. 14:6136–47
     [Google Scholar]
  80. 80.
    Pihan P, Carreras-Sureda A, Hetz C. 2017. BCL-2 family: integrating stress responses at the ER to control cell demise. Cell Death Differ. 24:1478–87
     [Google Scholar]
  81. 81.
    Susnow N, Zeng L, Margineantu D, Hockenbery DM. 2009. Bcl-2 family proteins as regulators of oxidative stress. Semin. Cancer Biol. 19:42–49
     [Google Scholar]
  82. 82.
    Tait SW, Green DR. 2010. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11:621–32
     [Google Scholar]
  83. 83.
    Hao Z, Mak TW. 2010. Type I and type II pathways of Fas-mediated apoptosis are differentially controlled by XIAP. J. Mol. Cell Biol. 2:63–64
     [Google Scholar]
  84. 84.
    Lartigue L, Kushnareva Y, Seong Y, Lin H, Faustin B, Newmeyer DD. 2009. Caspase-independent mitochondrial cell death results from loss of respiration, not cytotoxic protein release. Mol. Biol. Cell 20:4871–84
     [Google Scholar]
  85. 85.
    Tait SW, Ichim G, Green DR. 2014. Die another way—non-apoptotic mechanisms of cell death. J. Cell Sci. 127:2135–44
     [Google Scholar]
  86. 86.
    Tait SW, Green DR. 2008. Caspase-independent cell death: leaving the set without the final cut. Oncogene 27:6452–61
     [Google Scholar]
  87. 87.
    Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR. 2000. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat. Cell Biol. 2:156–62
     [Google Scholar]
  88. 88.
    Deshmukh M, Kuida K, Johnson EM Jr. 2000. Caspase inhibition extends the commitment to neuronal death beyond cytochrome c release to the point of mitochondrial depolarization. J. Cell Biol. 150:131–43
     [Google Scholar]
  89. 89.
    Martinou I, Desagher S, Eskes R, Antonsson B, Andre E et al. 1999. The release of cytochrome c from mitochondria during apoptosis of NGF-deprived sympathetic neurons is a reversible event. J. Cell Biol. 144:883–89
     [Google Scholar]
  90. 90.
    Colell A, Ricci JE, Tait S, Milasta S, Maurer U et al. 2007. GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell 129:983–97
     [Google Scholar]
  91. 91.
    Tait SW, Parsons MJ, Llambi F, Bouchier-Hayes L, Connell S et al. 2010. Resistance to caspase-independent cell death requires persistence of intact mitochondria. Dev. Cell 18:802–13
     [Google Scholar]
  92. 92.
    Ichim G, Lopez J, Ahmed SU, Muthalagu N, Giampazolias E et al. 2015. Limited mitochondrial permeabilization causes DNA damage and genomic instability in the absence of cell death. Mol. Cell 57:860–72
     [Google Scholar]
  93. 93.
    Mai N, Chrzanowska-Lightowlers ZM, Lightowlers RN. 2017. The process of mammalian mitochondrial protein synthesis. Cell Tissue Res. 367:5–20
     [Google Scholar]
  94. 94.
    Chomyn A. 1996. In vivo labeling and analysis of human mitochondrial translation products. Methods Enzymol. 264:197–211
     [Google Scholar]
  95. 95.
    Dieterich DC, Hodas JJ, Gouzer G, Shadrin IY, Ngo JT et al. 2010. In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat. Neurosci. 13:897–905
     [Google Scholar]
  96. 96.
    Yousefi R, Fornasiero EF, Cyganek L, Montoya J, Jakobs S et al. 2021. Monitoring mitochondrial translation in living cells. EMBO Rep. 22:e51635
     [Google Scholar]
  97. 97.
    Zorkau M, Albus CA, Berlinguer-Palmini R, Chrzanowska-Lightowlers ZMA, Lightowlers RN. 2021. High-resolution imaging reveals compartmentalization of mitochondrial protein synthesis in cultured human cells. PNAS 118:e2008778118
     [Google Scholar]
  98. 98.
    Richter-Dennerlein R, Oeljeklaus S, Lorenzi I, Ronsor C, Bareth B et al. 2016. Mitochondrial protein synthesis adapts to influx of nuclear-encoded protein. Cell 167:471–83.e10
     [Google Scholar]
  99. 99.
    Harbauer AB. 2017. Mitochondrial health maintenance in axons. Biochem. Soc. Trans. 45:1045–52
     [Google Scholar]
  100. 100.
    Cioni JM, Lin JQ, Holtermann AV, Koppers M, Jakobs MAH et al. 2019. Late endosomes act as mRNA translation platforms and sustain mitochondria in axons. Cell 176:56–72.e15
     [Google Scholar]
  101. 101.
    Kuzniewska B, Cysewski D, Wasilewski M, Sakowska P, Milek J et al. 2020. Mitochondrial protein biogenesis in the synapse is supported by local translation. EMBO Rep. 21:e48882
     [Google Scholar]
/content/journals/10.1146/annurev-anchem-061020-111722
Loading
Analysis of Mitochondria by Single-Organelle Resolution
Annual Review of Analytical Chemistry 15, 1 (2022); https://doi.org/10.1146/annurev-anchem-061020-111722
/content/journals/10.1146/annurev-anchem-061020-111722
/content/journals/10.1146/annurev-anchem-061020-111722
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error