1932

Abstract

Mitochondria are essential organelles performing important cellular functions ranging from bioenergetics and metabolism to apoptotic signaling and immune responses. They are highly dynamic at different structural and functional levels. Mitochondria have been shown to constantly undergo fusion and fission processes and dynamically interact with other organelles such as the endoplasmic reticulum, peroxisomes, and lipid droplets. The field of mitochondrial dynamics has evolved hand in hand with technological achievements including advanced fluorescence super-resolution nanoscopy. Dynamic remodeling of the cristae membrane within individual mitochondria, discovered very recently, opens up a further exciting layer of mitochondrial dynamics. In this review, we discuss mitochondrial dynamics at the following levels: () within an individual mitochondrion, () among mitochondria, and () between mitochondria and other organelles. Although the three tiers of mitochondrial dynamics have in the past been classified in a hierarchical manner, they are functionally connected and must act in a coordinated manner to maintain cellular functions and thus prevent various human diseases.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-030822-020736
2024-07-16
2025-02-08
Loading full text...

Full text loading...

/deliver/fulltext/biophys/53/1/annurev-biophys-030822-020736.html?itemId=/content/journals/10.1146/annurev-biophys-030822-020736&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abrisch RG, Gumbin SC, Wisniewski BT, Lackner LL, Voeltz GK. 2020.. Fission and fusion machineries converge at ER contact sites to regulate mitochondrial morphology. . J. Cell Biol. 219::e201911122
    [Crossref] [Google Scholar]
  2. 2.
    Alavi MV, Bette S, Schimpf S, Schuettauf F, Schraermeyer U, et al. 2007.. A splice site mutation in the murine Opa1 gene features pathology of autosomal dominant optic atrophy. . Brain 130::102942
    [Crossref] [Google Scholar]
  3. 3.
    Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, et al. 2000.. OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. . Nat. Genet. 26::21115
    [Crossref] [Google Scholar]
  4. 4.
    Anand R, Strecker V, Urbach J, Wittig I, Reichert AS. 2016.. Mic13 is essential for formation of crista junctions in mammalian cells. . PLOS ONE 11::e0160258
    [Crossref] [Google Scholar]
  5. 5.
    Arguello T, Peralta S, Antonicka H, Gaidosh G, Diaz F, et al. 2021.. ATAD3A has a scaffolding role regulating mitochondria inner membrane structure and protein assembly. . Cell Rep. 37::110139
    [Crossref] [Google Scholar]
  6. 6.
    Bannwarth S, Ait-El-Mkadem S, Chaussenot A, Genin EC, Lacas-Gervais S, et al. 2014.. A mitochondrial origin for frontotemporal dementia and amyotrophic lateral sclerosis through CHCHD10 involvement. . Brain 137::232945
    [Crossref] [Google Scholar]
  7. 7.
    Barbot M, Jans DC, Schulz C, Denkert N, Kroppen B, et al. 2015.. Mic10 oligomerizes to bend mitochondrial inner membranes at cristae junctions. . Cell Metab. 21::75663
    [Crossref] [Google Scholar]
  8. 8.
    Barrera M, Koob S, Dikov D, Vogel F, Reichert AS. 2016.. OPA1 functionally interacts with MIC60 but is dispensable for crista junction formation. . FEBS Lett. 590::330922
    [Crossref] [Google Scholar]
  9. 9.
    Benador IY, Veliova M, Mahdaviani K, Petcherski A, Wikstrom JD, et al. 2018.. Mitochondria bound to lipid droplets have unique bioenergetics, composition, and dynamics that support lipid droplet expansion. . Cell Metab. 27::86985.e6 9. Identified two distinct classes of lipid droplets with unique bioenergetic signatures.
    [Crossref] [Google Scholar]
  10. 10.
    Beninca C, Zanette V, Brischigliaro M, Johnson M, Reyes A, et al. 2021.. Mutation in the MICOS subunit gene APOO (MIC26) associated with an X-linked recessive mitochondrial myopathy, lactic acidosis, cognitive impairment and autistic features. . J. Med. Genet. 58::15567
    [Crossref] [Google Scholar]
  11. 11.
    Bereiter-Hahn J. 1978.. Intracellular motility of mitochondria: role of the inner compartment in migration and shape changes of mitochondria in XTH-cells. . J. Cell Sci. 30::99115
    [Crossref] [Google Scholar]
  12. 12.
    Bereiter-Hahn J, Voth M. 1994.. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. . Microsc. Res. Tech. 27::198219 12. Showed that mitochondria undergo putative fusion and fission events.
    [Crossref] [Google Scholar]
  13. 13.
    Bock-Bierbaum T, Funck K, Wollweber F, Lisicki E, von der Malsburg K, et al. 2022.. Structural insights into crista junction formation by the Mic60-Mic19 complex. . Sci. Adv. 8::eabo4946
    [Crossref] [Google Scholar]
  14. 14.
    Bohnert M, Zerbes RM, Davies KM, Muhleip AW, Rampelt H, et al. 2015.. Central role of Mic10 in the mitochondrial contact site and cristae organizing system. . Cell Metab. 21::74755
    [Crossref] [Google Scholar]
  15. 15.
    Burstein SR, Valsecchi F, Kawamata H, Bourens M, Zeng R, et al. 2018.. In vitro and in vivo studies of the ALS-FTLD protein CHCHD10 reveal novel mitochondrial topology and protein interactions. . Hum. Mol. Genet. 27::16077
    [Crossref] [Google Scholar]
  16. 16.
    Chan DC. 2012.. Fusion and fission: interlinked processes critical for mitochondrial health. . Annu. Rev. Genet. 46::26587
    [Crossref] [Google Scholar]
  17. 17.
    Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. 2003.. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. . J. Cell Biol. 160::189200
    [Crossref] [Google Scholar]
  18. 18.
    Chen H, McCaffery JM, Chan DC. 2007.. Mitochondrial fusion protects against neurodegeneration in the cerebellum. . Cell 130::54862
    [Crossref] [Google Scholar]
  19. 19.
    Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, et al. 2010.. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. . Cell 141::28089
    [Crossref] [Google Scholar]
  20. 20.
    Chen L, Dong J, Liao S, Wang S, Wu Z, et al. 2022.. Loss of Sam50 in hepatocytes induces cardiolipin-dependent mitochondrial membrane remodeling to trigger mtDNA release and liver injury. . Hepatology 76::1389408
    [Crossref] [Google Scholar]
  21. 21.
    Chen L, Liu T, Tran A, Lu X, Tomilov AA, et al. 2012.. OPA1 mutation and late-onset cardiomyopathy: mitochondrial dysfunction and mtDNA instability. . J. Am. Heart Assoc. 1::e003012
    [Crossref] [Google Scholar]
  22. 22.
    Chen Y, Liu Y, Dorn GW 2nd. 2011.. Mitochondrial fusion is essential for organelle function and cardiac homeostasis. . Circ. Res. 109::132731
    [Crossref] [Google Scholar]
  23. 23.
    Cipolat S, Martins de Brito O, Dal Zilio B, Scorrano L. 2004.. OPA1 requires mitofusin 1 to promote mitochondrial fusion. . PNAS 101::1592732
    [Crossref] [Google Scholar]
  24. 24.
    Cogliati S, Frezza C, Soriano ME, Varanita T, Quintana-Cabrera R, et al. 2013.. Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. . Cell 155::16071
    [Crossref] [Google Scholar]
  25. 25.
    Covill-Cooke C, Toncheva VS, Drew J, Birsa N, López-Doménech G, Kittler JT. 2020.. Peroxisomal fission is modulated by the mitochondrial Rho-GTPases, Miro1 and Miro2. . EMBO Rep. 21::e49865
    [Crossref] [Google Scholar]
  26. 26.
    Daems WT, Wisse E. 1966.. Shape and attachment of the cristae mitochondriales in mouse hepatic cell mitochondria. . J. Ultrastruct. Res. 16::12340
    [Crossref] [Google Scholar]
  27. 27.
    Davies KM, Strauss M, Daum B, Kief JH, Osiewacz HD, et al. 2011.. Macromolecular organization of ATP synthase and complex I in whole mitochondria. . PNAS 108::1412126
    [Crossref] [Google Scholar]
  28. 28.
    Davies VJ, Hollins AJ, Piechota MJ, Yip W, Davies JR, et al. 2007.. Opa1 deficiency in a mouse model of autosomal dominant optic atrophy impairs mitochondrial morphology, optic nerve structure and visual function. . Hum. Mol. Genet. 16::130718
    [Crossref] [Google Scholar]
  29. 29.
    de Brito OM, Scorrano L. 2008.. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. . Nature 456::60510
    [Crossref] [Google Scholar]
  30. 30.
    Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, et al. 2000.. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. . Nat. Genet. 26::20710
    [Crossref] [Google Scholar]
  31. 31.
    Deshwal S, Fiedler KU, Langer T. 2020.. Mitochondrial proteases: multifaceted regulators of mitochondrial plasticity. . Annu. Rev. Biochem. 89::50128
    [Crossref] [Google Scholar]
  32. 32.
    Duvezin-Caubet S, Jagasia R, Wagener J, Hofmann S, Trifunovic A, et al. 2006.. Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. . J. Biol. Chem. 281::3797279
    [Crossref] [Google Scholar]
  33. 33.
    Faelber K, Dietrich L, Noel JK, Wollweber F, Pfitzner AK, et al. 2019.. Structure and assembly of the mitochondrial membrane remodelling GTPase Mgm1. . Nature 571::42933 33. Used s-Mgm1 (OPA1 homolog) crystal cryo-ET structures to explain how OPA1 operates in fusion and cristae remodeling.
    [Crossref] [Google Scholar]
  34. 34.
    Fahrner JA, Liu R, Perry MS, Klein J, Chan DC. 2016.. A novel de novo dominant negative mutation in DNM1L impairs mitochondrial fission and presents as childhood epileptic encephalopathy. . Am. J. Med. Genet. A 170::200211
    [Crossref] [Google Scholar]
  35. 35.
    Fonseca TB, Sanchez-Guerrero A, Milosevic I, Raimundo N. 2019.. Mitochondrial fission requires DRP1 but not dynamins. . Nature 570::E3442
    [Crossref] [Google Scholar]
  36. 36.
    Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, et al. 2001.. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. . Dev. Cell 1::51525
    [Crossref] [Google Scholar]
  37. 37.
    Frey TG, Renken CW, Perkins GA. 2002.. Insight into mitochondrial structure and function from electron tomography. . Biochim. Biophys. Acta 1555::196203
    [Crossref] [Google Scholar]
  38. 38.
    Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, et al. 2006.. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. . Cell 126::17789 38. Showed that OPA1 forms regulate cristae remodeling by keeping the CJs tight, apart from mitochondrial fusion.
    [Crossref] [Google Scholar]
  39. 39.
    Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. 2011.. ER tubules mark sites of mitochondrial division. . Science 334::35862 39. Showed that MERCs are hotspots of mitochondrial division due to local recruitment of DRP1.
    [Crossref] [Google Scholar]
  40. 40.
    Gandre-Babbe S, van der Bliek AM. 2008.. The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. . Mol. Biol. Cell 19::240212
    [Crossref] [Google Scholar]
  41. 41.
    Genin EC, Plutino M, Bannwarth S, Villa E, Cisneros-Barroso E, et al. 2015.. CHCHD10 mutations promote loss of mitochondrial cristae junctions with impaired mitochondrial genome maintenance and inhibition of apoptosis. . EMBO Mol. Med. 8::5872
    [Crossref] [Google Scholar]
  42. 42.
    Gilkerson RW, Selker JM, Capaldi RA. 2003.. The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. . FEBS Lett. 546::35558
    [Crossref] [Google Scholar]
  43. 43.
    Glancy B, Kim Y, Katti P, Willingham TB. 2020.. The functional impact of mitochondrial structure across subcellular scales. . Front. Physiol. 11::541040
    [Crossref] [Google Scholar]
  44. 44.
    Golombek M, Tsigaras T, Schaumkessel Y, Hänsch S, Weidtkamp-Peters S, et al. 2023.. Cristae dynamics is modulated in bioenergetically compromised mitochondria. . Life Sci. Alliance 7:e202302386
    [Google Scholar]
  45. 45.
    Gottschalk B, Klec C, Leitinger G, Bernhart E, Rost R, et al. 2019.. MICU1 controls cristae junction and spatially anchors mitochondrial Ca2+ uniporter complex. . Nat. Commun. 10::3732
    [Crossref] [Google Scholar]
  46. 46.
    Guarani V, McNeill EM, Paulo JA, Huttlin EL, Frohlich F, et al. 2015.. QIL1 is a novel mitochondrial protein required for MICOS complex stability and cristae morphology. . eLife 4::e06265
    [Crossref] [Google Scholar]
  47. 47.
    Guo X, Hu J, He G, Chen J, Yang Y, et al. 2023.. Loss of APOO (MIC26) aggravates obesity-related whitening of brown adipose tissue via PPARα-mediated functional interplay between mitochondria and peroxisomes. . Metabolism 144::155564
    [Crossref] [Google Scholar]
  48. 48.
    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 175::143042.e17
    [Crossref] [Google Scholar]
  49. 49.
    Guyard V, Monteiro-Cardoso VF, Omrane M, Sauvanet C, Houcine A, et al. 2022.. ORP5 and ORP8 orchestrate lipid droplet biogenesis and maintenance at ER-mitochondria contact sites. . J. Cell Biol. 221::e202112107
    [Crossref] [Google Scholar]
  50. 50.
    Harner M, Körner C, Walther D, Mokranjac D, Kaesmacher J, et al. 2011.. The mitochondrial contact site complex, a determinant of mitochondrial architecture. . EMBO J. 30::435670
    [Crossref] [Google Scholar]
  51. 51.
    He B, Yu H, Liu S, Wan H, Fu S, et al. 2022.. Mitochondrial cristae architecture protects against mtDNA release and inflammation. . Cell Rep. 41::111774
    [Crossref] [Google Scholar]
  52. 52.
    Hermann GJ, Shaw JM. 1998.. Mitochondrial dynamics in yeast. . Annu. Rev. Cell Dev. Biol. 14::265303
    [Crossref] [Google Scholar]
  53. 53.
    Hermann GJ, Thatcher JW, Mills JP, Hales KG, Fuller MT, et al. 1998.. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. . J. Cell Biol. 143::35973
    [Crossref] [Google Scholar]
  54. 54.
    Hessenberger M, Zerbes RM, Rampelt H, Kunz S, Xavier AH, et al. 2017.. Regulated membrane remodeling by Mic60 controls formation of mitochondrial crista junctions. . Nat. Commun. 8::15258
    [Crossref] [Google Scholar]
  55. 55.
    Hong Z, Adlakha J, Wan N, Guinn E, Giska F, et al. 2022.. Mitoguardin-2-mediated lipid transfer preserves mitochondrial morphology and lipid droplet formation. . J. Cell Biol. 221::e202207022
    [Crossref] [Google Scholar]
  56. 56.
    Hopfner KP, Hornung V. 2020.. Molecular mechanisms and cellular functions of cGAS-STING signalling. . Nat. Rev. Mol. Cell. Biol. 21::50121
    [Crossref] [Google Scholar]
  57. 57.
    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. 195::32340
    [Crossref] [Google Scholar]
  58. 58.
    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. 36::45159
    [Crossref] [Google Scholar]
  59. 59.
    Huang X, Wu BP, Nguyen D, Liu YT, Marani M, et al. 2018.. CHCHD2 accumulates in distressed mitochondria and facilitates oligomerization of CHCHD10. . Hum. Mol. Genet. 27::3881900
    [Google Scholar]
  60. 60.
    Huo Y, Sun W, Shi T, Gao S, Zhuang M. 2022.. The MFN1 and MFN2 mitofusins promote clustering between mitochondria and peroxisomes. . Commun. Biol. 5::423
    [Crossref] [Google Scholar]
  61. 61.
    Huynen MA, Muhlmeister M, Gotthardt K, Guerrero-Castillo S, Brandt U. 2016.. Evolution and structural organization of the mitochondrial contact site (MICOS) complex and the mitochondrial intermembrane space bridging (MIB) complex. . Biochim. Biophys. Acta 1863::91101
    [Crossref] [Google Scholar]
  62. 62.
    Ishihara N, Eura Y, Mihara K. 2004.. Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. . J. Cell Sci. 117::653546
    [Crossref] [Google Scholar]
  63. 63.
    Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, et al. 2009.. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. . Nat. Cell Biol. 11::95866
    [Crossref] [Google Scholar]
  64. 64.
    Ishihara T, Ban-Ishihara R, Maeda M, Matsunaga Y, Ichimura A, et al. 2015.. Dynamics of mitochondrial DNA nucleoids regulated by mitochondrial fission is essential for maintenance of homogeneously active mitochondria during neonatal heart development. . Mol. Cell. Biol. 35::21123
    [Crossref] [Google Scholar]
  65. 65.
    Ishihara T, Ban-Ishihara R, Ota A, Ishihara N. 2022.. Mitochondrial nucleoid trafficking regulated by the inner-membrane AAA-ATPase ATAD3A modulates respiratory complex formation. . PNAS 119::e2210730119
    [Crossref] [Google Scholar]
  66. 66.
    Jakobs S, Stephan T, Ilgen P, Bruser C. 2020.. Light microscopy of mitochondria at the nanoscale. . Annu. Rev. Biophys. 49::289308
    [Crossref] [Google Scholar]
  67. 67.
    Jakubke C, Roussou R, Maiser A, Schug C, Thoma F, et al. 2021.. Cristae-dependent quality control of the mitochondrial genome. . Sci. Adv. 7::eabi8886
    [Crossref] [Google Scholar]
  68. 68.
    Janer A, Prudent J, Paupe V, Fahiminiya S, Majewski J, et al. 2016.. SLC25A46 is required for mitochondrial lipid homeostasis and cristae maintenance and is responsible for Leigh syndrome. . EMBO Mol. Med. 8::101938
    [Crossref] [Google Scholar]
  69. 69.
    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 110::893641 69. Used SR microscopy to show that MICOS proteins are arranged in a discontinuous rail-like pattern in the IM.
    [Crossref] [Google Scholar]
  70. 70.
    Kalia R, Wang RY, Yusuf A, Thomas PV, Agard DA, et al. 2018.. Structural basis of mitochondrial receptor binding and constriction by DRP1. . Nature 558::4015
    [Crossref] [Google Scholar]
  71. 71.
    Kamerkar SC, Kraus F, Sharpe AJ, Pucadyil TJ, Ryan MT. 2018.. Dynamin-related protein 1 has membrane constricting and severing abilities sufficient for mitochondrial and peroxisomal fission. . Nat. Commun. 9::5239
    [Crossref] [Google Scholar]
  72. 72.
    Klecker T, Westermann B. 2021.. Pathways shaping the mitochondrial inner membrane. . Open Biol. 11::210238
    [Crossref] [Google Scholar]
  73. 73.
    Kleele T, Rey T, Winter J, Zaganelli S, Mahecic D, et al. 2021.. Distinct fission signatures predict mitochondrial degradation or biogenesis. . Nature 593::43539
    [Crossref] [Google Scholar]
  74. 74.
    Koch A, Thiemann M, Grabenbauer M, Yoon Y, McNiven MA, Schrader M. 2003.. Dynamin-like protein 1 is involved in peroxisomal fission. . J. Biol. Chem. 278::8597605
    [Crossref] [Google Scholar]
  75. 75.
    Koch A, Yoon Y, Bonekamp NA, McNiven MA, Schrader M. 2005.. A role for Fis1 in both mitochondrial and peroxisomal fission in mammalian cells. . Mol. Biol. Cell 16::507786
    [Crossref] [Google Scholar]
  76. 76.
    Kondadi AK, Anand R, Hansch S, Urbach J, Zobel T, et al. 2020.. Cristae undergo continuous cycles of membrane remodelling in a MICOS-dependent manner. . EMBO Rep. 21::e49776 76. Demonstrated MICOS-dependent cristae remodeling events using SR microscopy in living cells.
    [Crossref] [Google Scholar]
  77. 77.
    Kondadi AK, Anand R, Reichert AS. 2019.. Functional interplay between cristae biogenesis, mitochondrial dynamics and mitochondrial DNA integrity. . Int. J. Mol. Sci. 20::4311
    [Crossref] [Google Scholar]
  78. 78.
    Kondadi AK, Anand R, Reichert AS. 2020.. Cristae membrane dynamics—a paradigm change. . Trends Cell Biol. 30::92336
    [Crossref] [Google Scholar]
  79. 79.
    Korobova F, Ramabhadran V, Higgs HN. 2013.. An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. . Science 339::46467
    [Crossref] [Google Scholar]
  80. 80.
    Lee JE, Westrate LM, Wu H, Page C, Voeltz GK. 2016.. Multiple dynamin family members collaborate to drive mitochondrial division. . Nature 540::13943
    [Crossref] [Google Scholar]
  81. 81.
    Lee SJ, Zhang J, Choi AM, Kim HP. 2013.. Mitochondrial dysfunction induces formation of lipid droplets as a generalized response to stress. . Oxid. Med. Cell Longev. 2013::327167
    [Google Scholar]
  82. 82.
    Lewis MR, Lewis WH. 1914.. Mitochondria in tissue culture. . Science 39::33033
    [Crossref] [Google Scholar]
  83. 83.
    Lewis SC, Uchiyama LF, Nunnari J. 2016.. ER-mitochondria contacts couple mtDNA synthesis with mitochondrial division in human cells. . Science 353::aaf5549
    [Crossref] [Google Scholar]
  84. 84.
    Li L, Conradson DM, Bharat V, Kim MJ, Hsieh CH, et al. 2021.. A mitochondrial membrane-bridging machinery mediates signal transduction of intramitochondrial oxidation. . Nat. Metab. 3::124258
    [Crossref] [Google Scholar]
  85. 85.
    Liu T, Stephan T, Chen P, Keller-Findeisen J, Chen J, et al. 2022.. Multi-color live-cell STED nanoscopy of mitochondria with a gentle inner membrane stain. . PNAS 119::e2215799119
    [Crossref] [Google Scholar]
  86. 86.
    Loson OC, Song Z, Chen H, Chan DC. 2013.. Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. . Mol. Biol. Cell 24::65967
    [Crossref] [Google Scholar]
  87. 87.
    Lubeck M, Derkum NH, Naha R, Strohm R, Driessen MD, et al. 2023.. MIC26 and MIC27 are bona fide subunits of the MICOS complex in mitochondria and do not exist as glycosylated apolipoproteins. . PLOS ONE 18::e0286756
    [Crossref] [Google Scholar]
  88. 88.
    Mannella CA, Lederer WJ, Jafri MS. 2013.. The connection between inner membrane topology and mitochondrial function. . J. Mol. Cell Cardiol. 62::5157
    [Crossref] [Google Scholar]
  89. 89.
    Marco-Hernández AV, Tomás-Vila M, Montoya-Filardi A, Barranco-González H, Vilchez Padilla JJ, et al. 2022.. Mitochondrial developmental encephalopathy with bilateral optic neuropathy related to homozygous variants in IMMT gene. . Clin. Genet. 101::23341
    [Crossref] [Google Scholar]
  90. 90.
    Modi S, Lopez-Domenech G, Halff EF, Covill-Cooke C, Ivankovic D, et al. 2019.. Miro clusters regulate ER-mitochondria contact sites and link cristae organization to the mitochondrial transport machinery. . Nat. Commun. 10::4399
    [Crossref] [Google Scholar]
  91. 91.
    Mohanty A, McBride HM. 2013.. Emerging roles of mitochondria in the evolution, biogenesis, and function of peroxisomes. . Front. Physiol. 4::268
    [Crossref] [Google Scholar]
  92. 92.
    Ngo J, Choi DW, Stanley IA, Stiles L, Molina AJA, et al. 2023.. Mitochondrial morphology controls fatty acid utilization by changing CPT1 sensitivity to malonyl-CoA. . EMBO J. 42::e111901
    [Crossref] [Google Scholar]
  93. 93.
    Nguyen TT, Voeltz GK. 2022.. An ER phospholipid hydrolase drives ER-associated mitochondrial constriction for fission and fusion. . eLife 11::e84279
    [Crossref] [Google Scholar]
  94. 94.
    Otera H, Miyata N, Kuge O, Mihara K. 2016.. Drp1-dependent mitochondrial fission via MiD49/51 is essential for apoptotic cristae remodeling. . J. Cell Biol. 212::53144
    [Crossref] [Google Scholar]
  95. 95.
    Otera H, Wang C, Cleland MM, Setoguchi K, Yokota S, et al. 2010.. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. . J. Cell Biol. 191::114158
    [Crossref] [Google Scholar]
  96. 96.
    Ott C, Dorsch E, Fraunholz M, Straub S, Kozjak-Pavlovic V. 2015.. Detailed analysis of the human mitochondrial contact site complex indicate a hierarchy of subunits. . PLOS ONE 10::e0120213
    [Crossref] [Google Scholar]
  97. 97.
    Ott C, Ross K, Straub S, Thiede B, Gotz M, et al. 2012.. Sam50 functions in mitochondrial intermembrane space bridging and biogenesis of respiratory complexes. . Mol. Cell. Biol. 32::117388
    [Crossref] [Google Scholar]
  98. 98.
    Palade GE. 1952.. The fine structure of mitochondria. . Anat. Rec. 114::42751
    [Crossref] [Google Scholar]
  99. 99.
    Palmer CS, Osellame LD, Laine D, Koutsopoulos OS, Frazier AE, Ryan MT. 2011.. MiD49 and MiD51, new components of the mitochondrial fission machinery. . EMBO Rep. 12::56573
    [Crossref] [Google Scholar]
  100. 100.
    Pape JK, Stephan T, Balzarotti F, Buchner R, Lange F, et al. 2020.. Multicolor 3D MINFLUX nanoscopy of mitochondrial MICOS proteins. . PNAS 117::2060714
    [Crossref] [Google Scholar]
  101. 101.
    Peifer-Weiß L, Kurban M, David C, Lubeck M, Kondadi AK, et al. 2023.. A X-linked nonsense APOO/MIC26 variant causes a lethal mitochondrial disease with progeria-like phenotypes. . Clin. Genet. 104::65968
    [Crossref] [Google Scholar]
  102. 102.
    Perkins G, Renken C, Martone ME, Young SJ, Ellisman M, Frey T. 1997.. Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts. . J. Struct. Biol. 119::26072
    [Crossref] [Google Scholar]
  103. 103.
    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. 204::108386
    [Crossref] [Google Scholar]
  104. 104.
    Phillips MJ, Voeltz GK. 2016.. Structure and function of ER membrane contact sites with other organelles. . Nat. Rev. Mol. Cell Biol. 17::6982
    [Crossref] [Google Scholar]
  105. 105.
    Qin J, Guo Y, Xue B, Shi P, Chen Y, et al. 2020.. ER-mitochondria contacts promote mtDNA nucleoids active transportation via mitochondrial dynamic tubulation. . Nat. Commun. 11::4471
    [Crossref] [Google Scholar]
  106. 106.
    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. 185::104763
    [Crossref] [Google Scholar]
  107. 107.
    Rambold AS, Cohen S, Lippincott-Schwartz J. 2015.. Fatty acid trafficking in starved cells: regulation by lipid droplet lipolysis, autophagy, and mitochondrial fusion dynamics. . Dev. Cell 32::67892
    [Crossref] [Google Scholar]
  108. 108.
    Rizzuto R, Brini M, Pizzo P, Murgia M, Pozzan T. 1995.. Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. . Curr. Biol. 5::63542
    [Crossref] [Google Scholar]
  109. 109.
    Rojo M, Legros F, Chateau D, Lombes A. 2002.. Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. . J. Cell Sci. 115::166374
    [Crossref] [Google Scholar]
  110. 110.
    Schrader M, Costello JL, Godinho LF, Azadi AS, Islinger M. 2016.. Proliferation and fission of peroxisomes—an update. . Biochim. Biophys. Acta 1863::97183
    [Crossref] [Google Scholar]
  111. 111.
    Schrader TA, Carmichael RE, Islinger M, Costello JL, Hacker C, et al. 2022.. PEX11β and FIS1 cooperate in peroxisome division independently of mitochondrial fission factor. . J. Cell Sci. 135::jcs259924
    [Crossref] [Google Scholar]
  112. 112.
    Shaw JM, Nunnari J. 2002.. Mitochondrial dynamics and division in budding yeast. . Trends Cell Biol. 12::17884
    [Crossref] [Google Scholar]
  113. 113.
    Sheffer R, Douiev L, Edvardson S, Shaag A, Tamimi K, et al. 2016.. Postnatal microcephaly and pain insensitivity due to a de novo heterozygous DNM1L mutation causing impaired mitochondrial fission and function. . Am. J. Med. Genet. A 170::16037
    [Crossref] [Google Scholar]
  114. 114.
    Shi P, Ren X, Meng J, Kang C, Wu Y, et al. 2022.. Mechanical instability generated by Myosin 19 contributes to mitochondria cristae architecture and OXPHOS. . Nat. Commun. 13::2673
    [Crossref] [Google Scholar]
  115. 115.
    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. 15::e1008085
    [Crossref] [Google Scholar]
  116. 116.
    Smirnova E, Shurland DL, Ryazantsev SN, van der Bliek AM. 1998.. A human dynamin-related protein controls the distribution of mitochondria. . J. Cell Biol. 143::35158
    [Crossref] [Google Scholar]
  117. 117.
    Song Z, Chen H, Fiket M, Alexander C, Chan DC. 2007.. OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. . J. Cell Biol. 178::74955
    [Crossref] [Google Scholar]
  118. 118.
    Stefani DD, Rizzuto R, Pozzan T. 2016.. Enjoy the trip: calcium in mitochondria back and forth. . Annu. Rev. Biochem. 85::16192
    [Crossref] [Google Scholar]
  119. 119.
    Stephan T, Bruser C, Deckers M, Steyer AM, Balzarotti F, et al. 2020.. MICOS assembly controls mitochondrial inner membrane remodeling and crista junction redistribution to mediate cristae formation. . EMBO J. 39::e104105
    [Crossref] [Google Scholar]
  120. 120.
    Stephan T, Roesch A, Riedel D, Jakobs S. 2019.. Live-cell STED nanoscopy of mitochondrial cristae. . Sci. Rep. 9::12419
    [Crossref] [Google Scholar]
  121. 121.
    Straub IR, Janer A, Weraarpachai W, Zinman L, Robertson J, et al. 2018.. Loss of CHCHD10-CHCHD2 complexes required for respiration underlies the pathogenicity of a CHCHD10 mutation in ALS. . Hum. Mol. Genet. 27::17889
    [Crossref] [Google Scholar]
  122. 122.
    Sugiura A, Mattie S, Prudent J, McBride HM. 2017.. Newly born peroxisomes are a hybrid of mitochondrial and ER-derived pre-peroxisomes. . Nature 542::25154
    [Crossref] [Google Scholar]
  123. 123.
    Tanaka H, Okazaki T, Aoyama S, Yokota M, Koike M, et al. 2019.. Peroxisomes control mitochondrial dynamics and the mitochondrion-dependent apoptosis pathway. . J. Cell Sci. 132::jcs224766 123. Demonstrated the control of mitochondrial dynamics by peroxisomes.
    [Crossref] [Google Scholar]
  124. 124.
    Tang J, Zhang K, Dong J, Yan C, Hu C, et al. 2019.. Sam50-Mic19-Mic60 axis determines mitochondrial cristae architecture by mediating mitochondrial outer and inner membrane contact. . Cell Death Differ. 27::14660
    [Crossref] [Google Scholar]
  125. 125.
    Tarasenko D, Barbot M, Jans DC, Kroppen B, Sadowski B, et al. 2017.. The MICOS component Mic60 displays a conserved membrane-bending activity that is necessary for normal cristae morphology. . J. Cell Biol. 216::88999
    [Crossref] [Google Scholar]
  126. 126.
    Tezze C, Romanello V, Desbats MA, Fadini GP, Albiero M, et al. 2017.. Age-associated loss of OPA1 in muscle impacts muscle mass, metabolic homeostasis, systemic inflammation, and epithelial senescence. . Cell Metab. 25::137489.e6
    [Crossref] [Google Scholar]
  127. 127.
    Tirrell PS, Nguyen KN, Luby-Phelps K, Friedman JR. 2020.. MICOS subcomplexes assemble independently on the mitochondrial inner membrane in proximity to ER contact sites. . J. Cell Biol. 219::e202003024
    [Crossref] [Google Scholar]
  128. 128.
    Tomar D, Thomas M, Garbincius JF, Kolmetzky DW, Salik O, et al. 2023.. MICU1 regulates mitochondrial cristae structure and function independently of the mitochondrial Ca2+ uniporter channel. . Sci. Signal 16::eabi8948
    [Crossref] [Google Scholar]
  129. 129.
    Tsai PI, Lin CH, Hsieh CH, Papakyrikos AM, Kim MJ, et al. 2018.. PINK1 phosphorylates MIC60/mitofilin to control structural plasticity of mitochondrial crista junctions. . Mol. Cell 69::74456.e6
    [Crossref] [Google Scholar]
  130. 130.
    Tsai PI, Papakyrikos AM, Hsieh CH, Wang X. 2017.. Drosophila MIC60/mitofilin conducts dual roles in mitochondrial motility and crista structure. . Mol. Biol. Cell 28::347179
    [Crossref] [Google Scholar]
  131. 131.
    Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, et al. 2008.. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. . EMBO J. 27::43346
    [Crossref] [Google Scholar]
  132. 132.
    Vanstone JR, Smith AM, McBride S, Naas T, Holcik M, et al. 2016.. DNM1L-related mitochondrial fission defect presenting as refractory epilepsy. . Eur. J. Hum. Genet. 24::108488
    [Crossref] [Google Scholar]
  133. 133.
    Veliova M, Petcherski A, Liesa M, Shirihai OS. 2020.. The biology of lipid droplet-bound mitochondria. . Semin. Cell Dev. Biol. 108::5564
    [Crossref] [Google Scholar]
  134. 134.
    Viana MP, Levytskyy RM, Anand R, Reichert AS, Khalimonchuk O. 2021.. Protease OMA1 modulates mitochondrial bioenergetics and ultrastructure through dynamic association with MICOS complex. . iScience 24::102119
    [Crossref] [Google Scholar]
  135. 135.
    Vogel F, Bornhövd C, Neupert W, Reichert AS. 2006.. Dynamic subcompartmentalization of the mitochondrial inner membrane. . J. Cell Biol. 175::23747 135. Showed that the mitochondrial IM is divided into subcompartments that can dynamically change their protein composition.
    [Crossref] [Google Scholar]
  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 21::694707
    [Crossref] [Google Scholar]
  137. 137.
    Wakabayashi J, Zhang Z, Wakabayashi N, Tamura Y, Fukaya M, et al. 2009.. The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. . J. Cell Biol. 186::80516
    [Crossref] [Google Scholar]
  138. 138.
    Wang C, Du W, Su QP, Zhu M, Feng P, et al. 2015.. Dynamic tubulation of mitochondria drives mitochondrial network formation. . Cell Res. 25::110820
    [Crossref] [Google Scholar]
  139. 139.
    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 116::1581722
    [Crossref] [Google Scholar]
  140. 140.
    Wang LJ, Hsu T, Lin HL, Fu CY. 2020.. Drosophila MICOS knockdown impairs mitochondrial structure and function and promotes mitophagy in muscle tissue. . Biol. Open 9::bio054262
    [Crossref] [Google Scholar]
  141. 141.
    Waterham HR, Koster J, van Roermund CW, Mooyer PA, Wanders RJ, Leonard JV. 2007.. A lethal defect of mitochondrial and peroxisomal fission. . N. Engl. J. Med. 356::173641
    [Crossref] [Google Scholar]
  142. 142.
    Weber TA, Koob S, Heide H, Wittig I, Head B, et al. 2013.. APOOL is a cardiolipin-binding constituent of the mitofilin/MINOS protein complex determining cristae morphology in mammalian mitochondria. . PLOS ONE 8::e63683
    [Crossref] [Google Scholar]
  143. 143.
    Westermann B. 2010.. Mitochondrial fusion and fission in cell life and death. . Nat. Rev. Mol. Cell Biol. 11::87284
    [Crossref] [Google Scholar]
  144. 144.
    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 144. Showed that individual cristae within a single mitochondrion have different membrane potentials acting as bioenergetic units.
    [Crossref] [Google Scholar]
  145. 145.
    Wong ED, Wagner JA, Gorsich SW, McCaffery JM, Shaw JM, Nunnari J. 2000.. The dynamin-related GTPase, Mgm1p, is an intermembrane space protein required for maintenance of fusion competent mitochondria. . J. Cell Biol. 151::34152
    [Crossref] [Google Scholar]
  146. 146.
    Wurm CA, Jakobs S. 2006.. Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast. . FEBS Lett. 580::562834
    [Crossref] [Google Scholar]
  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 108::1354651
    [Crossref] [Google Scholar]
  148. 148.
    Zhou J, Duan M, Wang X, Zhang F, Zhou H, et al. 2022.. A feedback loop engaging propionate catabolism intermediates controls mitochondrial morphology. . Nat. Cell Biol. 24::52637
    [Crossref] [Google Scholar]
  149. 149.
    Zick M, Rabl R, Reichert AS. 2009.. Cristae formation-linking ultrastructure and function of mitochondria. . Biochim. Biophys. Acta 1793::519
    [Crossref] [Google Scholar]
  150. 150.
    Zuchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, et al. 2004.. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. . Nat. Genet. 36::44951
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-biophys-030822-020736
Loading
/content/journals/10.1146/annurev-biophys-030822-020736
Loading

Data & Media loading...

  • Article Type: Review Article
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