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Abstract

Mitochondria are essential for eukaryotic life. These double-membrane organelles often form highly dynamic tubular networks interacting with many cellular structures. Their highly convoluted contiguous inner membrane compartmentalizes the organelle, which is crucial for mitochondrial function. Since the diameter of the mitochondrial tubules is generally close to the diffraction limit of light microscopy, it is often challenging, if not impossible, to visualize submitochondrial structures or protein distributions using conventional light microscopy. This renders super-resolution microscopy particularly valuable, and attractive, for studying mitochondria. Super-resolution microscopy encompasses a diverse set of approaches that extend resolution, as well as nanoscopy techniques that can even overcome the diffraction limit. In this review, we provide an overview of recent studies using super-resolution microscopy to investigate mitochondria, discuss the strengths and opportunities of the various methods in addressing specific questions in mitochondrial biology, and highlight potential future developments.

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2020-05-06
2024-04-26
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Literature Cited

  1. 1. 
    Abbe E. 1873. Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung. Arch. Mikrosk. Anat. 9413–68
  2. 2. 
    Ader NR, Hoffmann PC, Ganeva I, Borgeaud AC, Wang C et al. 2019. Molecular and topological reorganizations in mitochondrial architecture interplay during Bax-mediated steps of apoptosis. eLife 8e40712
  3. 3. 
    Appelhans T, Richter CP, Wilkens V, Hess ST, Piehler J, Busch KB 2012. Nanoscale organization of mitochondrial microcompartments revealed by combining tracking and localization microscopy. Nano Lett 12610–16
  4. 4. 
    Bachmann M, Fiederling F, Bastmeyer M 2016. Practical limitations of superresolution imaging due to conventional sample preparation revealed by a direct comparison of CLSM, SIM and dSTORM. J. Microsc. 262306–15
  5. 5. 
    Balzarotti F, Eilers Y, Gwosch KC, Gynnå AH, Westphal V et al. 2017. Nanometer resolution imaging and tracking of fluorescent molecules with minimal photon fluxes. Science 355606–12
  6. 6. 
    Baumgart F, Arnold AM, Rossboth BK, Brameshuber M, Schütz GJ 2018. What we talk about when we talk about nanoclusters. Methods Appl. Fluoresc. 7013001
  7. 7. 
    Bereiter-Hahn J, Vöth M. 1994. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27198–219
  8. 8. 
    Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S et al. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 3131642–45
  9. 9. 
    Born M, Wolf E. 1999. Principles of Optics Cambridge, UK: Cambridge Univ. Press 7th ed.
  10. 10. 
    Bottanelli F, Kromann EB, Allgeyer ES, Erdmann RS, Wood Baguley S et al. 2016. Two-colour live-cell nanoscale imaging of intracellular targets. Nat. Commun. 710778
  11. 11. 
    Brakemann T, Stiel AC, Weber G, Andresen M, Testa I et al. 2011. A reversibly photoswitchable GFP-like protein with fluorescence excitation decoupled from switching. Nat. Biotechnol. 29942–47
  12. 12. 
    Brown TA, Tkachuk AN, Shtengel G, Kopek BG, Bogenhagen DF et al. 2011. Superresolution fluorescence imaging of mitochondrial nucleoids reveals their spatial range, limits, and membrane interaction. Mol. Cell Biol. 314994–5010
  13. 13. 
    Chan CY, Pedley AM, Kim D, Xia C, Zhuang X, Benkovic SJ 2018. Microtubule-directed transport of purine metabolons drives their cytosolic transit to mitochondria. PNAS 11513009–14
  14. 14. 
    Chatre L, Ricchetti M. 2013. Large heterogeneity of mitochondrial DNA transcription and initiation of replication exposed by single-cell imaging. J. Cell Sci. 126914–26
  15. 15. 
    Chen BC, Legant WR, Wang K, Shao L, Milkie DE et al. 2014. Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science 3461257998
  16. 16. 
    Chen F, Tillberg PW, Boyden ES 2015. Optical imaging: expansion microscopy. Science 347543–48
  17. 17. 
    Chen Y, Liu W, Zhang Z, Zheng C, Huang Y et al. 2018. Multi-color live-cell super-resolution volume imaging with multi-angle interference microscopy. Nat. Commun. 94818
  18. 18. 
    Demmerle J, Innocent C, North AJ, Ball G, Müller M et al. 2017. Strategic and practical guidelines for successful structured illumination microscopy. Nat. Protoc. 12988–1010
  19. 19. 
    Dertinger T, Colyer R, Iyer G, Weiss S, Enderlein J 2009. Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI). PNAS 10622287–92
  20. 20. 
    Dlaskova A, Spacek T, Santorova J, Plecita-Hlavata L, Berkova Z et al. 2010. 4Pi microscopy reveals an impaired three-dimensional mitochondrial network of pancreatic islet beta-cells, an experimental model of type-2 diabetes. Biochim. Biophys. Acta 17971327–41
  21. 21. 
    Donnert G, Keller J, Wurm CA, Rizzoli SO, Westphal V et al. 2007. Two-color far-field fluorescence nanoscopy. Biophys. J. 92L67–69
  22. 22. 
    Egner A, Jakobs S, Hell SW 2002. Fast 100-nm resolution three-dimensional microscope reveals structural plasticity of mitochondria in live yeast. PNAS 993370–75
  23. 23. 
    Fallaize D, Chin LS, Li L 2015. Differential submitochondrial localization of PINK1 as a molecular switch for mediating distinct mitochondrial signaling pathways. Cell Signal 272543–54
  24. 24. 
    Fiolka R, Shao L, Rego EH, Davidson MW, Gustafsson MG 2012. Time-lapse two-color 3D imaging of live cells with doubled resolution using structured illumination. PNAS 1095311–15
  25. 25. 
    Fonseca TB, Sánchez-Guerrero A, Milosevic I, Raimundo N 2019. Mitochondrial fission requires DRP1 but not dynamins. Nature 570E34–42
  26. 26. 
    Frei MS, Hoess P, Lampe M, Nijmeijer B, Kueblbeck M et al. 2019. Photoactivation of silicon rhodamines via a light-induced protonation. Nat. Commun. 104580
  27. 27. 
    French JB, Jones SA, Deng H, Pedley AM, Kim D et al. 2016. Spatial colocalization and functional link of purinosomes with mitochondria. Science 351733–37
  28. 28. 
    Frey TG, Mannella CA. 2000. The internal structure of mitochondria. Trends Biochem. Sci. 25319–24
  29. 29. 
    Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK 2011. ER tubules mark sites of mitochondrial division. Science 334358–62
  30. 30. 
    Gambarotto D, Zwettler FU, Le Guennec M, Schmidt-Cernohorska M, Fortun D et al. 2019. Imaging cellular ultrastructures using expansion microscopy (U-ExM). Nat. Methods 1671–74
  31. 31. 
    Gibson TJ, Seiler M, Veitia RA 2013. The transience of transient overexpression. Nat. Methods 10715–21
  32. 32. 
    Gilkerson RW, Selker JML, Capaldi RA 2003. The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett 546355–58
  33. 33. 
    Gregor I, Enderlein J. 2019. Image scanning microscopy. Curr. Opin. Chem. Biol. 5174–83
  34. 34. 
    Grosse L, Wurm CA, Brüser C, Neumann D, Jans DC, Jakobs S 2016. Bax assembles into large ring-like structures remodeling the mitochondrial outer membrane in apoptosis. EMBO J 35402–13
  35. 35. 
    Grotjohann T, Testa I, Leutenegger M, Bock H, Urban NT et al. 2011. Diffraction-unlimited all-optical imaging and writing with a photochromic GFP. Nature 478204–8
  36. 36. 
    Gugel H, Bewersdorf J, Jakobs S, Engelhardt J, Storz R, Hell SW 2004. Cooperative 4Pi excitation and detection yields sevenfold sharper optical sections in live-cell microscopy. Biophys. J. 874146–52
  37. 37. 
    Guo Y, Li D, Zhang S, Yang Y, Liu JJ et al. 2018. Visualizing intracellular organelle and cytoskeletal interactions at nanoscale resolution on millisecond timescales. Cell 1751430–42.e17
  38. 38. 
    Gustafsson CM, Falkenberg M, Larsson NG 2016. Maintenance and expression of mammalian mitochondrial DNA. Annu. Rev. Biochem. 85133–60
  39. 39. 
    Gustafsson MG. 2000. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 19882–87
  40. 40. 
    Gustafsson MG. 2005. Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. PNAS 10213081–86
  41. 41. 
    Gustafsson MG, Shao L, Carlton PM, Wang CJ, Golubovskaya IN et al. 2008. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 944957–70
  42. 42. 
    Gustafsson MGL. 1999. Extended resolution fluorescence microscopy. Curr. Opin. Struct. Biol. 9627–34
  43. 43. 
    Hackenbrock CR. 1968. Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states. PNAS 61598–605
  44. 44. 
    Han Y, Li M, Qiu F, Zhang M, Zhang YH 2017. Cell-permeable organic fluorescent probes for live-cell long-term super-resolution imaging reveal lysosome-mitochondrion interactions. Nat. Commun. 81307
  45. 45. 
    Harner M, Korner C, Walther D, Mokranjac D, Kaesmacher J et al. 2011. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 304356–70
  46. 46. 
    Heintzmann R, Huser T. 2017. Super-resolution structured illumination microscopy. Chem. Rev. 11713890–908
  47. 47. 
    Hell SW, Dyba M, Jakobs S 2004. Concepts for nanoscale resolution in fluorescence microscopy. Curr. Opin. Neurobiol. 14599–609
  48. 48. 
    Hell SW, Wichmann J. 1994. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19780–82
  49. 49. 
    Hess ST, Girirajan TP, Mason MD 2006. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 914258–72
  50. 50. 
    Hirvonen LM, Wicker K, Mandula O, Heintzmann R 2009. Structured illumination microscopy of a living cell. Eur. Biophys. J. 38807–12
  51. 51. 
    Hofmann M, Eggeling C, Jakobs S, Hell SW 2005. Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. PNAS 10217565–69
  52. 52. 
    Holt IJ, He J, Mao CC, Boyd-Kirkup JD, Martinsson P et al. 2007. Mammalian mitochondrial nucleoids: organizing an independently minded genome. Mitochondrion 7311–21
  53. 53. 
    Hoppins S, Collins SR, Cassidy-Stone A, Hummel E, Devay RM et al. 2011. A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J. Cell Biol. 195323–40
  54. 54. 
    Huang B, Jones SA, Brandenburg B, Zhuang X 2008. Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution. Nat. Methods 51047–52
  55. 55. 
    Huang F, Sirinakis G, Allgeyer ES, Schroeder LK, Duim WC et al. 2016. Ultra-high resolution 3D imaging of whole cells. Cell 1661028–40
  56. 56. 
    Huang X, Fan J, Li L, Liu H, Wu R et al. 2018. Fast, long-term, super-resolution imaging with Hessian structured illumination microscopy. Nat. Biotechnol. 36451–59
  57. 57. 
    Iborra FJ, Kimura H, Cook PR 2004. The functional organization of mitochondrial genomes in human cells. BMC Biol 29
  58. 58. 
    Ilgen P, Stoldt S, Conradi LC, Wurm CA, Ruschoff J et al. 2014. STED super-resolution microscopy of clinical paraffin-embedded human rectal cancer tissue. PLOS ONE 9e101563
  59. 59. 
    Jans DC, Wurm CA, Riedel D, Wenzel D, Stagge F et al. 2013. STED super-resolution microscopy reveals an array of MINOS clusters along human mitochondria. PNAS 1108936–41
  60. 60. 
    Ji N, Shroff H, Zhong H, Betzig E 2008. Advances in the speed and resolution of light microscopy. Curr. Opin. Neurobiol. 18605–16
  61. 61. 
    Ji WK, Hatch AL, Merrill RA, Strack S, Higgs HN 2015. Actin filaments target the oligomeric maturation of the dynamin GTPase Drp1 to mitochondrial fission sites. eLife 4e11553
  62. 62. 
    Jiang YF, Lin SS, Chen JM, Tsai HZ, Hsieh TS, Fu CY 2017. Directing the self-assembly of tumour spheroids by bioprinting cellular heterogeneous models with alginate/gelatin hydrogels. Sci. Rep. 745474
  63. 63. 
    Kalkavan H, Green DR. 2018. MOMP, cell suicide as a BCL-2 family business. Cell Death Differ 2546–55
  64. 64. 
    Kehrein K, Schilling R, Möller-Hergt BV, Wurm CA, Jakobs S et al. 2015. Organization of mitochondrial gene expression in two distinct ribosome-containing assemblies. Cell Rep 10843–53
  65. 65. 
    Kilian N, Goryaynov A, Lessard MD, Hooker G, Toomre D et al. 2018. Assessing photodamage in live-cell STED microscopy. Nat. Methods 15755–56
  66. 66. 
    Klar TA, Jakobs S, Dyba M, Egner A, Hell SW 2000. Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. PNAS 978206–10
  67. 67. 
    Klotzsch E, Smorodchenko A, Löfler L, Moldzio R, Parkinson E et al. 2015. Superresolution microscopy reveals spatial separation of UCP4 and F0F1-ATP synthase in neuronal mitochondria. PNAS 112130–35
  68. 68. 
    Kopek BG, Shtengel G, Xu CS, Clayton DA, Hess HF 2012. Correlative 3D superresolution fluorescence and electron microscopy reveal the relationship of mitochondrial nucleoids to membranes. PNAS 1096136–41
  69. 69. 
    Korobova F, Gauvin TJ, Higgs HN 2014. A role for myosin II in mammalian mitochondrial fission. Curr. Biol. 24409–14
  70. 70. 
    Korobova F, Ramabhadran V, Higgs HN 2013. An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INf2. Science 339464–67
  71. 71. 
    Kraus F, Miron E, Demmerle J, Chitiashvili T, Budco A et al. 2017. Quantitative 3D structured illumination microscopy of nuclear structures. Nat. Protoc. 121011–28
  72. 72. 
    Kukat C, Davies KM, Wurm CA, Spåhr H, Bonekamp NA et al. 2015. Cross-strand binding of TFAM to a single mtDNA molecule forms the mitochondrial nucleoid. PNAS 11211288–93
  73. 73. 
    Kukat C, Wurm CA, Spåhr H, Falkenberg M, Larsson NG, Jakobs S 2011. Super-resolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA. PNAS 10813534–39
  74. 74. 
    Lackner LL. 2019. The expanding and unexpected functions of mitochondria contact sites. Trends Cell Biol 29580–90
  75. 75. 
    Laissue PP, Alghamdi RA, Tomancak P, Reynaud EG, Shroff H 2017. Assessing phototoxicity in live fluorescence imaging. Nat. Methods 14657–61
  76. 76. 
    Lau L, Lee YL, Sahl SJ, Stearns T, Moerner WE 2012. STED microscopy with optimized labeling density reveals 9-fold arrangement of a centriole protein. Biophys. J. 1022926–35
  77. 77. 
    Lawrence EJ, Boucher E, Mandato CA 2016. Mitochondria-cytoskeleton associations in mammalian cytokinesis. Cell Div 113
  78. 78. 
    Legros F, Malka F, Frachon P, Lombès A, Rojo M 2004. Organization and dynamics of human mitochondrial DNA. J. Cell Sci. 1172653–62
  79. 79. 
    Li D, Shao L, Chen BC, Zhang X, Zhang M et al. 2015. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics. Science 349aab3500
  80. 80. 
    Li Y, Almassalha LM, Chandler JE, Zhou X, Stypula-Cyrus YE et al. 2017. The effects of chemical fixation on the cellular nanostructure. Exp. Cell Res. 358253–59
  81. 81. 
    Liu W, Liu Q, Zhang Z, Han Y, Kuang C et al. 2019. Three-dimensional super-resolution imaging of live whole cells using galvanometer-based structured illumination microscopy. Opt. Express 277237–48
  82. 82. 
    Lukinavicius G, Umezawa K, Olivier N, Honigmann A, Yang G et al. 2013. A near-infrared fluorophore for live-cell super-resolution microscopy of cellular proteins. Nat. Chem. 5132–39
  83. 83. 
    Mannella CA, Marko M, Penczek P, Barnard D, Frank J 1994. The internal compartmentation of rat-liver mitochondria: tomographic study using the high-voltage transmission electron microscope. Microsc. Res. Tech. 27278–83
  84. 84. 
    Mannella CA, Pfeiffer DR, Bradshaw PC, Moraru II, Slepchenko B et al. 2001. Topology of the mitochondrial inner membrane: dynamics and bioenergetics implications. IUBMB Life 5293–100
  85. 85. 
    Manor U, Bartholomew S, Golani G, Christenson E, Kozlov M et al. 2015. A mitochondria-anchored isoform of the actin-nucleating spire protein regulates mitochondrial division. eLife 4e08828
  86. 86. 
    McArthur K, Whitehead LW, Heddleston JM, Li L, Padman BS et al. 2018. BAK/BAX macropores facilitate mitochondrial herniation and mtDNA efflux during apoptosis. Science 359eaao6047
  87. 87. 
    Messina A, Reina S, Guarino F, De Pinto V 2012. VDAC isoforms in mammals. Biochim. Biophys. Acta 18181466–76
  88. 88. 
    Model K, Meisinger C, Kühlbrandt W 2008. Cryo-electron microscopy structure of a yeast mitochondrial preprotein translocase. J. Mol. Biol. 3831049–57
  89. 89. 
    Müller CB, Enderlein J. 2010. Image scanning microscopy. Phys. Rev. Lett. 104198101
  90. 90. 
    Murley A, Lackner LL, Osman C, West M, Voeltz GK et al. 2013. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. eLife 2e00422
  91. 91. 
    Murley A, Nunnari J. 2016. The emerging network of mitochondria-organelle contacts. Mol. Cell 61648–53
  92. 92. 
    Nass MM. 1969. Mitochondrial DNA. I. Intramitochondrial distribution and structural relations of single- and double-length circular DNA. J. Mol. Biol. 42521–28
  93. 93. 
    Nass MM, Nass S. 1963. Intramitochondrial fibers with DNA characteristics. I. Fixation and electron staining reactions. J. Cell Biol. 19593–611
  94. 94. 
    Nechushtan A, Smith CL, Lamensdorf I, Yoon SH, Youle RJ 2001. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J. Cell Biol. 1531265–76
  95. 95. 
    Neumann D, Bückers J, Kastrup L, Hell SW, Jakobs S 2010. Two-color STED microscopy reveals different degrees of colocalization between hexokinase-I and the three human VDAC isoforms. PMC Biophys 34
  96. 96. 
    Nunnari J, Marshall WF, Straight A, Murray A, Sedat JW, Walter P 1997. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol. Biol. Cell. 81233–42
  97. 97. 
    Nunnari J, Suomalainen A. 2012. Mitochondria: in sickness and in health. Cell 1481145–59
  98. 98. 
    Opstad IS, Wolfson DL, Øie CI, Ahluwalia BS 2018. Multi-color imaging of sub-mitochondrial structures in living cells using structured illumination microscopy. Nanophotonics 7935–47
  99. 99. 
    Palade GE. 1952. The fine structure of mitochondria. Anat. Rec. 114427–51
  100. 100. 
    Park CB, Larsson NG. 2011. Mitochondrial DNA mutations in disease and aging. J. Cell Biol. 193809–18
  101. 101. 
    Park S, Kang W, Kwon YD, Shim J, Kim S et al. 2018. Superresolution fluorescence microscopy for 3D reconstruction of thick samples. Mol. Brain 1117
  102. 102. 
    Pfanner N, van der Laan M, Amati P, Capaldi RA, Caudy AA et al. 2014. Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J. Cell Biol. 2041083–86
  103. 103. 
    Rabl R, Soubannier V, Scholz R, Vogel F, Mendl N et al. 2009. Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J. Cell Biol. 1851047–63
  104. 104. 
    Rajala N, Gerhold JM, Martinsson P, Klymov A, Spelbrink JN 2014. Replication factors transiently associate with mtDNA at the mitochondrial inner membrane to facilitate replication. Nucleic Acids Res 42952–67
  105. 105. 
    Rampelt H, Zerbes RM, van der Laan M, Pfanner N 2017. Role of the mitochondrial contact site and cristae organizing system in membrane architecture and dynamics. Biochim. Biophys. Acta 1864737–46
  106. 106. 
    Ratz M, Testa I, Hell SW, Jakobs S 2015. CRISPR/Cas9-mediated endogenous protein tagging for RESOLFT super-resolution microscopy of living human cells. Sci. Rep. 59592
  107. 107. 
    Richter KN, Revelo NH, Seitz KJ, Helm MS, Sarkar D et al. 2018. Glyoxal as an alternative fixative to formaldehyde in immunostaining and super-resolution microscopy. EMBO J 37139–59
  108. 108. 
    Riley JS, Quarato G, Cloix C, Lopez J, O'Prey J et al. 2018. Mitochondrial inner membrane permeabilisation enables mtDNA release during apoptosis. EMBO J 37e99238
  109. 109. 
    Rust M, Bates M, Zhuang X 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3793–95
  110. 110. 
    Sahl SJ, Hell SW, Jakobs S 2017. Fluorescence nanoscopy in cell biology. Nat. Rev. Mol. Cell Biol. 18685–701
  111. 111. 
    Salvador-Gallego R, Mund M, Cosentino K, Schneider J, Unsay J et al. 2016. Bax assembly into rings and arcs in apoptotic mitochondria is linked to membrane pores. EMBO J 35389–401
  112. 112. 
    Scheffler IE. 2008. Mitochondria Hoboken, NJ: Wiley, 2nd ed..
  113. 113. 
    Schermelleh L, Ferrand A, Huser T, Eggeling C, Sauer M et al. 2019. Super-resolution microscopy demystified. Nat. Cell Biol. 2172–84
  114. 114. 
    Schmidt R, Wurm CA, Jakobs S, Engelhardt J, Egner A, Hell SW 2008. Spherical nanosized focal spot unravels the interior of cells. Nat. Methods 5539–44
  115. 115. 
    Schmidt R, Wurm CA, Punge A, Egner A, Jakobs S, Hell SW 2009. Mitochondrial cristae revealed with focused light. Nano Lett 92508–10
  116. 116. 
    Schueder F, Lara-Gutierrez J, Beliveau BJ, Saka SK, Sasaki HM et al. 2017. Multiplexed 3D super-resolution imaging of whole cells using spinning disk confocal microscopy and DNA-PAINT. Nat. Commun. 82090
  117. 117. 
    Sesso A, Belizario JE, Marques MM, Higuchi ML, Schumacher RI et al. 2012. Mitochondrial swelling and incipient outer membrane rupture in preapoptotic and apoptotic cells. Anat. Rec. 2951647–59
  118. 118. 
    Shao L, Kner P, Rego EH, Gustafsson MG 2011. Super-resolution 3D microscopy of live whole cells using structured illumination. Nat. Methods 81044–46
  119. 119. 
    Sharonov A, Hochstrasser RM. 2006. Wide-field subdiffraction imaging by accumulated binding of diffusing probes. PNAS 10318911–16
  120. 120. 
    Sheppard CJR. 1988. Super-resolution in confocal imaging. Optik 8053–54
  121. 121. 
    Shim SH, Xia C, Zhong G, Babcock HP, Vaughan JC et al. 2012. Super-resolution fluorescence imaging of organelles in live cells with photoswitchable membrane probes. PNAS 10913978–83
  122. 122. 
    Sigal YM, Zhou R, Zhuang X 2018. Visualizing and discovering cellular structures with super-resolution microscopy. Science 361880–87
  123. 123. 
    Silva Ramos E, Motori E, Bruser C, Kuhl I, Yeroslaviz A et al. 2019. Mitochondrial fusion is required for regulation of mitochondrial DNA replication. PLOS Genet 15e1008085
  124. 124. 
    Sjöstrand FS. 1953. Electron microscopy of mitochondria and cytoplasmic double membranes. Nature 17130–32
  125. 125. 
    Smirnova E, Griparic L, Shurland DL, van der Bliek AM 2001. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 122245–56
  126. 126. 
    Stephan T, Roesch A, Riedel D, Jakobs S 2019. Live-cell STED nanoscopy of mitochondrial cristae. Sci. Rep. 912419
  127. 127. 
    Stoldt S, Stephan T, Jans DC, Brüser C, Lange F et al. 2019. Mic60 exhibits a coordinated clustered distribution along and across yeast and mammalian mitochondria. PNAS 1169853–58
  128. 128. 
    Stoldt S, Wenzel D, Hildenbeutel M, Wurm CA, Herrmann JM, Jakobs S 2012. The inner-mitochondrial distribution of Oxa1 depends on the growth conditions and on the availability of substrates. Mol. Biol. Cell 232292–301
  129. 129. 
    Stoldt S, Wenzel D, Kehrein K, Riedel D, Ott M, Jakobs S 2018. Spatial orchestration of mitochondrial translation and OXPHOS complex assembly. Nat. Cell Biol. 20528–34
  130. 130. 
    Suppanz IE, Wurm CA, Wenzel D, Jakobs S 2009. The m-AAA protease processes cytochrome c peroxidase preferentially at the inner boundary membrane of mitochondria. Mol. Biol. Cell 20572–80
  131. 131. 
    Tait SW, Green DR. 2010. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11621–32
  132. 132. 
    Tatsuta T, Model K, Langer T 2005. Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol. Biol. Cell 16248–59
  133. 133. 
    van de Linde S, Sauer M, Heilemann M 2008. Subdiffraction-resolution fluorescence imaging of proteins in the mitochondrial inner membrane with photoswitchable fluorophores. J. Struct. Biol. 164250–54
  134. 134. 
    Vangindertael J, Camacho R, Sempels W, Mizuno H, Dedecker P, Janssen KPF 2018. An introduction to optical super-resolution microscopy for the adventurous biologist. Methods Appl. Fluoresc. 6022003
  135. 135. 
    Vogel F, Bornhövd C, Neupert W, Reichert AS 2006. Dynamic subcompartmentalization of the mitochondrial inner membrane. J. Cell Biol. 175237–47
  136. 136. 
    von der Malsburg K, Muller JM, Bohnert M, Oeljeklaus S, Kwiatkowska P et al. 2011. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev. Cell 21694–707
  137. 137. 
    Wäldchen S, Lehmann J, Klein T, van de Linde S, Sauer M 2015. Light-induced cell damage in live-cell super-resolution microscopy. Sci. Rep. 515348
  138. 138. 
    Wang C, Taki M, Sato Y, Tamura Y, Yaginuma H et al. 2019. A photostable fluorescent marker for the superresolution live imaging of the dynamic structure of the mitochondrial cristae. PNAS 11615817–22
  139. 139. 
    Wassie AT, Zhao Y, Boyden ES 2019. Expansion microscopy: principles and uses in biological research. Nat. Methods 1633–41
  140. 140. 
    Werner S, Neupert W. 1972. Functional and biogenetical heterogeneity of the inner membrane of rat-liver mitochondria. Eur. J. Biochem. 25379–96
  141. 141. 
    Westermann B. 2010. Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 11872–84
  142. 142. 
    Whelan DR, Bell TD. 2015. Image artifacts in single molecule localization microscopy: why optimization of sample preparation protocols matters. Sci. Rep. 57924
  143. 143. 
    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 38e101056
  144. 144. 
    Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ 1997. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 1391281–92
  145. 145. 
    Wong YC, Ysselstein D, Krainc D 2018. Mitochondria-lysosome contacts regulate mitochondrial fission via RAB7 GTP hydrolysis. Nature 554382–86
  146. 146. 
    Wurm CA, Jakobs S. 2006. Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast. FEBS Lett 5805628–34
  147. 147. 
    Wurm CA, Neumann D, Lauterbach MA, Harke B, Egner A et al. 2011. Nanoscale distribution of mitochondrial import receptor Tom20 is adjusted to cellular conditions and exhibits an inner-cellular gradient. PNAS 10813546–51
  148. 148. 
    Wurm CA, Neumann D, Schmidt R, Egner A, Jakobs S 2010. Sample preparation for STED microscopy. Live Cell Imaging: Methods and Protocols DB Papkovsky 185–99 Berlin: Springer
  149. 149. 
    Zhou W, Ma D, Sun AX, Tran HD, Ma DL et al. 2019. PD-linked CHCHD2 mutations impair CHCHD10 and MICOS complex leading to mitochondria dysfunction. Hum. Mol. Genet. 281100–16
  150. 150. 
    Zick M, Rabl R, Reichert AS 2009. Cristae formation-linking ultrastructure and function of mitochondria. Biochim. Biophys. Acta 17935–19
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