The MICOS complex, a structural element of mitochondria with versatile functions

  • 1 Department of Cell Biology, Biomedical Center, Ludwig-Maximilians University Munich, Großhaderner Str. 9, Planegg/Martinsried, Munich, Germany
  • 2 Institute of Cardiovascular Physiology and Pathophysiology, Biomedical Center, Ludwig-Maximilians University Munich, Großhaderner Str. 9, Planegg/Martinsried, Munich, Germany
Siavash Khosravi
  • Department of Cell Biology, Biomedical Center, Ludwig-Maximilians University Munich, Großhaderner Str. 9, Planegg/Martinsried, Munich, D-82152, Germany
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  • Siavash Khosravi did his undergraduate study in biology at the Tarbiat Moalem University of Tehran (Kharazmi). Then, he perused his master study in Biology at the Ludwig-Maximilians University of Munich and wrote his master thesis on CRISPR-Cas9 genome modifying systems in C. elegans under supervision of Prof. Barbara Conradt. Currently, he is doing his doctoral study which he started under supervision of Prof. Walter Neupert. His research aims at analyzing the role of intra-mitochondrial contact sites in mitochondria biogenesis.
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and Max E. HarnerORCID iD: https://orcid.org/0000-0002-5513-1046
  • Corresponding author
  • Institute of Cardiovascular Physiology and Pathophysiology, Biomedical Center, Ludwig-Maximilians University Munich, Großhaderner Str. 9, Planegg/Martinsried, Munich, D-82152, Germany
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  • Max E. Harner did his studies in biology at the Technical University of Munich and finished his diploma in 2006. Afterwards he moved to Walter Neupert's lab to do his PhD thesis at the Ludwig-Maximilians University of Munich. He finished his PhD in 2012 and moved together with Walter Neupert to the MPI of Biochemistry in Planegg to continue his research on mitochondrial architecture as a Postdoc. In 2016 Max Harner did a second Postdoc in Bill Wickner's lab at the Geisel School of Medicine at Dartmouth to study the molecular mechanisms of membrane fusion using a reconstituted system. In 2017 Max Harner returned to Munich to pursue his research on mitochondrial biogenesis at the Biomedical Center of the Ludwig-Maximilians University.
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Abstract

Mitochondria perform a plethora of functions in various cells of different tissues. Their architecture differs remarkably, for instance in neurons versus steroidogenic cells. Furthermore, aberrant mitochondrial architecture results in mitochondrial dysfunction. This indicates strongly that mitochondrial architecture and function are intimately linked. Therefore, a deep knowledge about the determinants of mitochondrial architecture and their function on a molecular level is of utmost importance. In the past decades, various proteins and protein complexes essential for formation of mitochondrial architecture have been identified. Here we will review the current knowledge of the MICOS complex, one of the major structural elements of mitochondria. MICOS is a multi-subunit complex present in the inner mitochondrial membrane. Multiple interaction partners in the inner and outer mitochondrial membrane point to participation in a multitude of important processes, such as generation of mitochondrial architecture, lipid metabolism, and protein import into mitochondria. Since the MICOS complex is highly conserved in form and function throughout evolution, we will highlight the importance of MICOS for mammals. We will emphasize in particular the current knowledge of the association of MICOS with severe human diseases, including Charcot–Marie–Tooth disease type 2, Alzheimer's disease, Parkinson's disease, Frontotemporal Dementia and Amyotrophic Lateral Sclerosis.

  • Aaltonen, M. J.; Friedman, J. R.; Osman, C.; Salin, B.; di Rago, J. P.; Nunnari, J.; Langer, T.; Tatsuta, T. MICOS and phospholipid transfer by Ups2-Mdm35 organize membrane lipid synthesis in mitochondria. J. Cell Biol. 2016, 213, 525–534, https://doi.org/10.1083/jcb.201602007.

    • Crossref
    • PubMed
    • Export Citation
  • Akabane, S.; Uno, M.; Tani, N.; Shimazaki, S.; Ebara, N.; Kato, H.; Kosako, H.; Oka, T. PKA regulates PINK1 stability and parkin recruitment to damaged mitochondria through phosphorylation of MIC60. Mol. Cell 2016, 62, 371–384, https://doi.org/10.1016/j.molcel.2016.03.037.

    • Crossref
    • PubMed
    • Export Citation
  • Alkhaja, A. K.; Jans, D. C.; Nikolov, M.; Vukotic, M.; Lytovchenko, O.; Ludewig, F.; Schliebs, W.; Riedel, D.; Urlaub, H.; Jakobs, S., et al. MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Mol. Biol. Cell 2012, 23, 247–257, https://doi.org/10.1091/mbc.e11-09-0774.

    • Crossref
    • PubMed
    • Export Citation
  • An, J.; Shi, J.; He, Q.; Lui, K.; Liu, Y.; Huang, Y.; Sheikh, M. S. CHCM1/CHCHD6, novel mitochondrial protein linked to regulation of mitofilin and mitochondrial cristae morphology. J. Cell Biol. 2012, 287, 7411–7426, https://doi.org/10.1074/jbc.m111.277103.

  • Anand, R.; Strecker, V.; Urbach, J.; Wittig, I.; Reichert, A. S. Mic13 is essential for formation of crista junctions in mammalian cells. PLoS One 2016, 11, e0160258, https://doi.org/10.1371/journal.pone.0160258.

    • PubMed
    • Export Citation
  • Attwell, D.; Laughlin, S. B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 2001, 21, 1133–1145, https://doi.org/10.1097/00004647-200110000-00001.

    • Crossref
    • PubMed
    • Export Citation
  • Auranen, M.; Ylikallio, E.; Shcherbii, M; Paetau, A.; Kiuru-Enari, S; Toppila, J. P.; Tyynismaa, H. CHCHD10 variant p.(Gly66Val) causes axonal Charcot-Marie-Tooth disease. Neurol Genet. 2015, 1, e1, https://doi.org/10.1212/nxg.0000000000000003.

    • Crossref
    • PubMed
    • Export Citation
  • Baile, M. G.; Lu, Y. W.; Claypool, S. M. The topology and regulation of cardiolipin biosynthesis and remodeling in yeast. Chem. Phys. Lipids. 2014, 179, 25–31, https://doi.org/10.1016/j.chemphyslip.2013.10.008.

    • Crossref
    • PubMed
    • Export Citation
  • Bannwarth, S.; Ait-El-Mkadem, S.; Chaussenot, A.; Genin, E. C.; Lacas-Gervais, S.; Fragaki, K.; Berg-Alonso, L.; Kageyama, Y; Serre, V.; Moore, D. G., et al. A mitochondrial origin for frontotemporal dementia and amyotrophic lateral sclerosis through CHCHD10 involvement. Brain 2014, 137, 2329–2345, https://doi.org/10.1093/med/9780199590674.003.0008.

    • Crossref
    • PubMed
    • Export Citation
  • Barbot, M.; Jans, D. C.; Schulz, C.; Denkert, N.; Kroppen, B; Hoppert, M.; Jakobs, S.; Meinecke, M. Mic10 oligomerizes to bend mitochondrial inner membranes at cristae junctions. Cell Metab. 2015, 21, 756–763, https://doi.org/10.1016/j.cmet.2015.04.006.

    • Crossref
    • PubMed
    • Export Citation
  • Becker, T.; Horvath, S. E.; Bottinger, L.; Gebert, N; Daum, G.; Pfanner, N. Role of phosphatidylethanolamine in the biogenesis of mitochondrial outer membrane proteins. J. Cell Biol. 2013, 288, 16451–16459, https://doi.org/10.1074/jbc.m112.442392.

  • Bohnert, M.; Wenz, L. S.; Zerbes, R. M.; Horvath, S. E.; Stroud, D. A; von der Malsburg, K.; Muller, J. M.; Oeljeklaus, S.; Perschil, I.; Warscheid, B., et al. Role of mitochondrial inner membrane organizing system in protein biogenesis of the mitochondrial outer membrane. Mol. Biol. Cell 2012, 23, 3948–3956, https://doi.org/10.1091/mbc.e12-04-0295.

    • Crossref
    • PubMed
    • Export Citation
  • Bohnert, M.; Zerbes, R. M.; Davies, K. M.; Muhleip, A. W.; Rampelt, H.; Horvath, S. E.; Boenke, T.; Kram, A.; Perschil, I; Veenhuis, M., et al. Central role of Mic10 in the mitochondrial contact site and cristae organizing system. Cell Metab. 2015, 21, 747–755, https://doi.org/10.1016/j.cmet.2015.04.007.

    • Crossref
    • PubMed
    • Export Citation
  • Burstein, S. R.; Valsecchi, F.; Kawamata, H.; Bourens, M.; Zeng, R.; Zuberi, A.; Milner, T. A.; Cloonan, S. M.; Lutz, C.; Barrientos, A., et al. In vitro and in vivo studies of the ALS-FTLD protein CHCHD10 reveal novel mitochondrial topology and protein interactions. Hum. Mol. Genet. 2018, 27, 160–177, https://doi.org/10.1093/hmg/ddx397.

    • Crossref
    • PubMed
    • Export Citation
  • Callegari, S.; Muller, T.; Schulz, C; Lenz, C.; Jans, D. C.; Wissel, M.; Opazo, F.; Rizzoli, S. O.; Jakobs, S; Urlaub, H., et al. A MICOS-TIM22 association promotes carrier import into human mitochondria. J. Mol. Biol. 2019, 431, 2835–2851, https://doi.org/10.1016/j.jmb.2019.05.015.

    • Crossref
    • PubMed
    • Export Citation
  • Chatzispyrou, I. A.; Guerrero-Castillo, S.; Held, N. M.; Ruiter, J. P. N.; Denis, S. W.; Ijlst, L.; Wanders, R. J.; van Weeghel, M.; Ferdinandusse, S.; Vaz, F. M., et al. Barth syndrome cells display widespread remodeling of mitochondrial complexes without affecting metabolic flux distribution. Biochim Biophys Acta Mol Basis Dis 2018, 1864, 3650–3658, https://doi.org/10.1016/j.bbadis.2018.08.041.

    • Crossref
    • PubMed
    • Export Citation
  • Chaussenot, A.; Le Ber, I.; Ait-El-Mkadem, S.; Camuzat, A.; de Septenville, A.; Bannwarth, S.; Genin, E. C.; Serre, V.; Auge, G.; French research network on, F. T. D., et al. 2014.Screening of CHCHD10 in a French cohort confirms the involvement of this gene in frontotemporal dementia with amyotrophic lateral sclerosis patients. Neurobiol. Aging 2014, 35, 2884 e2881-2884 e2884, https://doi.org/10.1016/j.neurobiolaging.2014.07.022.

  • Chio, A.; Mora, G.; Sabatelli, M.; Caponnetto, C.; Traynor, B. J.; Johnson, J. O.; Nalls, M. A.; Calvo, A.; Moglia, C.; Borghero, G., et al. CHCH10 mutations in an Italian cohort of familial and sporadic amyotrophic lateral sclerosis patients. Neurobiol. Aging 2015, 36, 1767 e1763-1767 e1766, https://doi.org/10.1016/j.neurobiolaging.2015.01.017.

  • Chojnacka, M.; Gornicka, A.; Oeljeklaus, S.; Warscheid, B.; Chacinska, A. Cox17 protein is an auxiliary factor involved in the control of the mitochondrial contact site and cristae organizing system. J. Cell Biol. 2015, 290, 15304–15312, https://doi.org/10.1074/jbc.m115.645069.

  • Cipolat, S.; Martins de Brito, O.; Dal Zilio, B.; Scorrano, L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. USA 2004, 101, 15927–15932, https://doi.org/10.1073/pnas.0407043101.

    • Crossref
    • Export Citation
  • Connerth, M.; Tatsuta, T.; Haag, M; Klecker, T.; Westermann, B.; Langer, T. Intramitochondrial transport of phosphatidic acid in yeast by a lipid transfer protein. Science 2012, 338, 815–818, https://doi.org/10.1126/science.1225625.

    • Crossref
    • PubMed
    • Export Citation
  • Darshi, M.; Mendiola, V. L.; Mackey, M. R.; Murphy, A. N; Koller, A.; Perkins, G. A.; Ellisman, M. H.; Taylor, S. S. ChChd3, an inner mitochondrial membrane protein, is essential for maintaining crista integrity and mitochondrial function. J. Cell Biol. 2011, 286, 2918–2932, https://doi.org/10.1074/jbc.m110.171975.

  • Darshi, M.; Trinh, K. N.; Murphy, A. N.; Taylor, S. S. Targeting and import mechanism of coiled-coil helix coiled-coil helix domain-containing protein 3 (ChChd3) into the mitochondrial intermembrane space. J. Cell Biol. 2012, 287, 39480–39491, https://doi.org/10.1074/jbc.m112.387696.

  • Daum, G. Lipids of mitochondria. Biochim Biophys Acta 1985, 822, 1–42, https://doi.org/10.1111/j.1753-4887.1979.tb02191.x.

    • Crossref
    • PubMed
    • Export Citation
  • Daum, G.; Vance, J. E. Import of lipids into mitochondria. Prog. Lipid Res. 1997, 36, 103–130, https://doi.org/10.1016/s0163-7827(97)00006-4.

    • Crossref
    • PubMed
    • Export Citation
  • Davies, K. M.; Anselmi, C.; Wittig, I.; Faraldo-Gomez, J. D.; Kuhlbrandt, W. Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. USA 2012, 109, 13602–13607, https://doi.org/10.3410/f.717957339.793463819.

    • Crossref
    • Export Citation
  • Di Domenico, F.; Sultana, R.; Barone, E.; Perluigi, M.; Cini, C.; Mancuso, C.; Cai, J.; Pierce, W. M.; Butterfield, D. A. Quantitative proteomics analysis of phosphorylated proteins in the hippocampus of Alzheimer's disease subjects. J. Proteomics 2011, 74, 1091–1103, https://doi.org/10.1016/j.jprot.2011.03.033.

    • Crossref
    • PubMed
    • Export Citation
  • Ding, C.; Wu, Z.; Huang, L.; Wang, Y.; Xue, J.; Chen, S.; Deng, Z.; Wang, L.; Song, Z.; Chen, S. Mitofilin and CHCHD6 physically interact with Sam50 to sustain cristae structure. Sci. Rep. 2015, 5, 16064, https://doi.org/10.1038/srep16064.

    • Crossref
    • PubMed
    • Export Citation
  • Eydt, K.; Davies, K. M.; Behrendt, C.; Wittig, I.; Reichert, A. S. Cristae architecture is determined by an interplay of the MICOS complex and the F1FO ATP synthase via Mic27 and Mic10. Microb. Cell 2017, 4, 259–272, https://doi.org/10.15698/mic2017.08.585.

    • Crossref
    • PubMed
    • Export Citation
  • Fawcett, D. W. Mitochondria. 1981, In Saunders, WB (ed): “The Cell.” Philadelphia.

  • Friedman, J. R.; Mourier, A.; Yamada, J.; McCaffery, J. M.; Nunnari, J. MICOS coordinates with respiratory complexes and lipids to establish mitochondrial inner membrane architecture. eLife 2015, 4, https://doi.org/10.7554/elife.07739.024.

    • PubMed
    • Export Citation
  • Fukada, K; Zhang, F; Vien, A; Cashman, N. R.; Zhu, H. Mitochondrial proteomic analysis of a cell line model of familial amyotrophic lateral sclerosis. Mol. Cell Proteomics. 2004, 3, 1211–1223, https://doi.org/10.1074/mcp.m400094-mcp200.

    • Crossref
    • PubMed
    • Export Citation
  • Furukawa, A.; Kawamoto, Y.; Chiba, Y.; Takei, S.; Hasegawa-Ishii, S.; Kawamura, N.; Yoshikawa, K.; Hosokawa, M.; Oikawa, S.; Kato, M., et al. Proteomic identification of hippocampal proteins vulnerable to oxidative stress in excitotoxin-induced acute neuronal injury. Neurobiol. Dis. 2011, 43, 706–714, https://doi.org/10.1016/j.nbd.2011.05.024.

    • Crossref
    • PubMed
    • Export Citation
  • Gebert, N.; Joshi, A. S.; Kutik, S.; Becker, T.; McKenzie, M.; Guan, X. L.; Mooga, V. P.; Stroud, D. A.; Kulkarni, G.; Wenk, M. R., et al. Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome. Curr. Biol. 2009, 19, 2133–2139, https://doi.org/10.1016/j.cub.2009.10.074.

    • Crossref
    • PubMed
    • Export Citation
  • Genin, E.C; Plutino, M.; Bannwarth, S.; Villa, E.; Cisneros-Barroso, E.; Roy, M.; Ortega-Vila, B.; Fragaki, K.; Lespinasse, F.; Pinero-Martos, E., et al. CHCHD10 mutations promote loss of mitochondrial cristae junctions with impaired mitochondrial genome maintenance and inhibition of apoptosis. EMBO Mol. Med. 2016, 8, 58–72, https://doi.org/10.15252/emmm.201505496.

    • Crossref
    • PubMed
    • Export Citation
  • Gieffers, C.; Korioth, F.; Heimann, P.; Ungermann, C.; Frey, J. Mitofilin is a transmembrane protein of the inner mitochondrial membrane expressed as two isoforms. Exp. Cell Res. 1997, 232, 395–399, https://doi.org/10.1006/excr.1997.3539.

    • Crossref
    • PubMed
    • Export Citation
  • Godiker, J.; Gruneberg, M.; DuChesne, I.; Reunert, J.; Rust, S.; Westermann, C.; Wada, Y.; Classen, G.; Langhans, C. D.; Schlingmann, K. P., et al. QIL1-dependent assembly of MICOS complex-lethal mutation in C19ORF70 resulting in liver disease and severe neurological retardation. J. Hum. Genet. 2018, 63, 707–716, https://doi.org/10.1038/s10038-018-0442-y.

    • Crossref
    • PubMed
    • Export Citation
  • Gold, V. A.; Ieva, R.; Walter, A.; Pfanner, N; van der Laan, M.; Kuhlbrandt, W. Visualizing active membrane protein complexes by electron cryotomography. Nat. Commun. 2014, 5, 4129, https://doi.org/10.1038/ncomms5129.

    • Crossref
    • PubMed
    • Export Citation
  • Guarani, V.; Jardel, C.; Chretien, D.; Lombes, A.; Benit, P.; Labasse, C.; Lacene, E.; Bourillon, A.; Imbard, A.; Benoist, J. F., et al. QIL1 mutation causes MICOS disassembly and early onset fatal mitochondrial encephalopathy with liver disease. eLife 2016, 5, https://doi.org/10.7554/elife.17163.

    • PubMed
    • Export Citation
  • Guarani, V.; McNeill, E. M.; Paulo, J. A.; Huttlin, E. L.; Frohlich, F.; Gygi, S. P.; Van Vactor, D.: Harper, J. W. QIL1 is a novel mitochondrial protein required for MICOS complex stability and cristae morphology. eLife 2015, 4, https://doi.org/10.7554/elife.06265.014.

    • PubMed
    • Export Citation
  • Habersetzer, J.; Larrieu, I.; Priault, M.; Salin, B.; Rossignol, R.; Brethes, D.; Paumard, P. Human F1F0 ATP synthase, mitochondrial ultrastructure and OXPHOS impairment: a (super-)complex matter? PLoS One 2013, 8, e75429, https://doi.org/10.1371/journal.pone.0075429.

    • PubMed
    • Export Citation
  • Hales, K. G.; Fuller, M. T. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 1997, 90, 121–129, https://doi.org/10.1016/s0092-8674(00)80319-0.

    • Crossref
    • PubMed
    • Export Citation
  • Harner, M.; Korner, C.; Walther, D.; Mokranjac, D.; Kaesmacher, J.; Welsch, U.; Griffith, J.; Mann, M.; Reggiori, F.; Neupert, W. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J. 2011, 30, 4356–4370, https://doi.org/10.1038/emboj.2011.379.

    • Crossref
    • PubMed
    • Export Citation
  • Harner, M. E.; Unger, A. K.; Geerts, W. J.; Mari, M.; Izawa, T.; Stenger, M.; Geimer, S.; Reggiori, F.; Westermann, B.; Neupert, W. An evidence based hypothesis on the existence of two pathways of mitochondrial crista formation. eLife 2016, 5, https://doi.org/10.7554/elife.18853.

    • PubMed
    • Export Citation
  • Harner, M. E.; Unger, A. K.; Izawa, T.; Walther, D. M.; Ozbalci, C.; Geimer, S.; Reggiori, F.; Brugger, B.; Mann, M.; Westermann, B., et al. Aim24 and MICOS modulate respiratory function, tafazzin-related cardiolipin modification and mitochondrial architecture. eLife 2014, 3, e01684, https://doi.org/10.7554/elife.01684.015.

    • PubMed
    • Export Citation
  • Head, B. P.; Zulaika, M.; Ryazantsev, S.; van der Bliek, A. M. A novel mitochondrial outer membrane protein, MOMA-1, that affects cristae morphology in Caenorhabditis elegans. Mol. Biol. Cell 2011, 22, 831–841, https://doi.org/10.1091/mbc.e10-07-0600.

    • Crossref
    • PubMed
    • Export Citation
  • Hermann, G. J.; Thatcher, J. W.; Mills, J. P.; Hales, K. G.; Fuller, M. T.; Nunnari, J.; Shaw, J. M. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J. Cell Biol. 1998, 143, 359–373, https://doi.org/10.1083/jcb.143.2.359.

    • Crossref
    • PubMed
    • Export Citation
  • Hessenberger, M.; Zerbes, R. M; Rampelt, H; Kunz, S; Xavier, A. H.; Purfurst, B.; Lilie, H., Pfanner, N; van der Laan, M.; Daumke, O. Regulated membrane remodeling by Mic60 controls formation of mitochondrial crista junctions. Nat. Commun. 2017, 8, 15258, https://doi.org/10.1038/ncomms15258.

    • Crossref
    • PubMed
    • Export Citation
  • Hoppins, S.; Collins, S. R.; Cassidy-Stone, A.; Hummel, E.; Devay, R. M.; Lackner, L. L.; Westermann, B.; Schuldiner, M.; Weissman, J. S.; Nunnari, J. A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J. Cell Biol. 2011, 195, 323–340, https://doi.org/10.1083/jcb.201107053.

    • Crossref
    • PubMed
    • Export Citation
  • Ioakeimidis, F.; Ott, C.; Kozjak-Pavlovic, V.; Violitzi, F.; Rinotas, V.; Makrinou, E.; Eliopoulos, E.; Fasseas, C.; Kollias, G.; Douni, E. A splicing mutation in the novel mitochondrial protein DNAJC11 causes motor neuron pathology associated with cristae disorganization, and lymphoid abnormalities in mice. PLoS One 2014, 9, e104237, https://doi.org/10.1371/journal.pone.0104237.

    • PubMed
    • Export Citation
  • Jans, D. C.; Wurm, C. A.; Riedel, D.; Wenzel, D.; Stagge, F.; Deckers, M.; Rehling, P.; Jakobs, S. STED super-resolution microscopy reveals an array of MINOS clusters along human mitochondria. Proc. Natl. Acad. Sci. USA 2013, 110, 8936–8941, https://doi.org/10.1073/pnas.1301820110.

    • Crossref
    • Export Citation
  • Jiang, F.; Ryan, M. T.; Schlame, M.; Zhao, M; Gu, Z.; Klingenberg, M.; Pfanner, N.; Greenberg, M.L. Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J. Cell Biol. 2000, 275, 22387–22394, https://doi.org/10.1074/jbc.m909868199.

  • John, G.B.; Shang, Y.; Li, L.; Renken, C.; Mannella, C.A.; Selker, J.M.; Rangell, L.; Bennett, M.J.; Zha, J. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol. Biol. Cell 2005, 16, 1543–1554, https://doi.org/10.1091/mbc.e04-08-0697.

    • Crossref
    • PubMed
    • Export Citation
  • Johnson, J.O.; Glynn, S.M.; Gibbs, J.R.; Nalls, M.A.; Sabatelli, M.; Restagno, G.; Drory, V.E.; Chio, A.; Rogaeva, E.; Traynor, B.J. Mutations in the CHCHD10 gene are a common cause of familial amyotrophic lateral sclerosis. Brain 2014, 137, e311, https://doi.org/10.1093/brain/awu265.

    • Crossref
    • PubMed
    • Export Citation
  • Jones, B.A.; Fangman, W.L. Mitochondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin. Genes Dev. 1992, 6, 380–389, https://doi.org/10.1101/gad.6.3.380.

    • Crossref
    • PubMed
    • Export Citation
  • Kim, H.Y.; Lee, K.Y; Lu, Y.; Wang, J.; Cui, L.; Kim, S.J.; Chung, J.M.; Chung, K. Mitochondrial Ca(2+) uptake is essential for synaptic plasticity in pain. J. Neurosci. 2011, 31, 12982–12991, https://doi.org/10.1016/j.jpain.2011.02.149.

    • Crossref
    • PubMed
    • Export Citation
  • Kojima, R.; Kakimoto, Y.; Furuta, S.; Itoh, K.; Sesaki, H.; Endo, T.; Tamura, Y. Maintenance of cardiolipin and crista structure requires cooperative functions of mitochondrial dynamics and phospholipid transport. Cell Rep. 2019, 26, 518–528 e516, https://doi.org/10.1016/j.celrep.2018.12.070.

    • Crossref
    • PubMed
    • Export Citation
  • Koob, S.; Barrera, M.; Anand, R.; Reichert, A. S. The non-glycosylated isoform of MIC26 is a constituent of the mammalian MICOS complex and promotes formation of crista junctions. Biochim. Biophys. Acta 2015, 1853, 1551–1563, https://doi.org/10.1016/j.bbamcr.2015.03.004.

    • Crossref
    • PubMed
    • Export Citation
  • Korner, C.; Barrera, M.; Dukanovic, J.; Eydt, K.; Harner, M.; Rabl, R.; Vogel, F.; Rapaport, D.; Neupert, W.; Reichert, A. S. The C-terminal domain of Fcj1 is required for formation of crista junctions and interacts with the TOB/SAM complex in mitochondria. Mol. Biol. Cell 2012, 23, 2143–2155, https://doi.org/10.1091/mbc.e11-10-0831.

    • Crossref
    • PubMed
    • Export Citation
  • Koshiba, T.; Detmer, S. A.; Kaiser, J. T.; Chen, H.; McCaffery, J. M.; Chan, D. C. Structural basis of mitochondrial tethering by mitofusin complexes. Science 2004, 305, 858–862, https://doi.org/10.1126/science.1099793.

    • Crossref
    • PubMed
    • Export Citation
  • Kutik, S.; Rissler, M.; Guan, X. L.; Guiard, B.; Shui, G.; Gebert, N.; Heacock, P. N.; Rehling, P.; Dowhan, W.; Wenk, M. R., et al. The translocator maintenance protein Tam41 is required for mitochondrial cardiolipin biosynthesis. J. Cell Biol. 2008, 183, 1213–1221, https://doi.org/10.1083/jcb.200806048.

    • Crossref
    • PubMed
    • Export Citation
  • Kwon, S. K.; Sando, R.3rd; Lewis, T. L.; Hirabayashi, Y.; Maximov, A.; Polleux, F. LKB1 Regulates mitochondria-dependent presynaptic calcium clearance and neurotransmitter release properties at excitatory synapses along cortical axons. PLoS Biol. 2016, 14, e1002516, https://doi.org/10.1371/journal.pbio.1002516.

    • PubMed
    • Export Citation
  • Lehmer, C.; Schludi, M. H.; Ransom, L.; Greiling, J.; Junghanel, M.; Exner, N.; Riemenschneider, H.; van der Zee, J.; Van Broeckhoven, C.; Weydt, P., et al. A novel CHCHD10 mutation implicates a Mia40-dependent mitochondrial import deficit in ALS. EMBO Mol. Med. 2018, 10, https://doi.org/10.15252/emmm.201708558.

    • PubMed
    • Export Citation
  • Liotta, A.; Rosner, J.; Huchzermeyer, C.; Wojtowicz, A.; Kann, O.; Schmitz, D.; Heinemann, U.; Kovacs, R. Energy demand of synaptic transmission at the hippocampal Schaffer-collateral synapse. J. Cereb. Blood Flow Metab. 2012, 32, 2076–2083, https://doi.org/10.1038/jcbfm.2012.116.

    • Crossref
    • PubMed
    • Export Citation
  • Malhotra, K.; Modak, A.; Nangia, S.; Daman, T. H.; Gunsel, U.; Robinson, V. L.; Mokranjac, D.; May, E. R.; Alder, N. N. Cardiolipin mediates membrane and channel interactions of the mitochondrial TIM23 protein import complex receptor Tim50. Sci. Adv. 2017, 3, e1700532, https://doi.org/10.1126/sciadv.1700532.

    • PubMed
    • Export Citation
  • Mannella, C. A. Structural diversity of mitochondria: functional implications. Ann. N. Y. Acad. Sci. 2008, 1147, 171–179, https://doi.org/10.1196/annals.1427.020.

    • Crossref
    • PubMed
    • Export Citation
  • Marland, J. R.; Hasel, P.; Bonnycastle, K.; Cousin, M. A. Mitochondrial calcium uptake modulates synaptic vesicle endocytosis in central nerve terminals. J. Cell Biol. 2016, 291, 2080–2086, https://doi.org/10.1074/jbc.m115.686956.

  • Meeusen, S.; DeVay, R.; Block, J.; Cassidy-Stone, A.; Wayson, S.; McCaffery, J. M.; Nunnari, J. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell 2006, 127, 383–395, https://doi.org/10.1016/j.cell.2006.09.021.

    • Crossref
    • PubMed
    • Export Citation
  • Michaud, M.; Gros, V.; Tardif, M.; Brugiere, S.; Ferro, M.; Prinz, W. A.; Toulmay, A.; Mathur, J.; Wozny, M.; Falconet, D., et al. AtMic60 is involved in plant mitochondria lipid trafficking and is part of a large complex. Curr. Biol. 2016, 26, 627–639, https://doi.org/10.1016/j.cub.2016.01.011.

    • Crossref
    • PubMed
    • Export Citation
  • Miyata, N.; Watanabe, Y.; Tamura, Y.; Endo, T.; Kuge, O. Phosphatidylserine transport by Ups2-Mdm35 in respiration-active mitochondria. J. Cell Biol. 2016, 214, 77–88, https://doi.org/10.1083/jcb.201601082.

    • Crossref
    • PubMed
    • Export Citation
  • Modi, S.; Lopez-Domenech, G.; Halff, E. F.; Covill-Cooke, C.; Ivankovic, D.; Melandri, D.; Arancibia-Carcamo, I. L.; Burden, J. J.; Lowe, A. R.; Kittler, J. T. Miro clusters regulate ER-mitochondria contact sites and link cristae organization to the mitochondrial transport machinery. Nat. Commun. 2019, 10, 4399, https://doi.org/10.1038/s41467-019-12382-4.

    • Crossref
    • PubMed
    • Export Citation
  • Muller, K.; Andersen, P. M.; Hubers, A.; Marroquin, N.; Volk, A. E.; Danzer, K. M.; Meitinger, T.; Ludolph, A. C.; Strom, T. M.; Weishaupt, J. H. Two novel mutations in conserved codons indicate that CHCHD10 is a gene associated with motor neuron disease. Brain 2014, 137, e309, https://doi.org/10.1093/brain/awu227.

    • Crossref
    • PubMed
    • Export Citation
  • Mun, J. Y.; Lee, T. H.; Kim, J. H.; Yoo, B. H.; Bahk, Y. Y.; Koo, H. S.; Han, S. S. Caenorhabditis elegans mitofilin homologs control the morphology of mitochondrial cristae and influence reproduction and physiology. J. Cell. Physiol. 2010, 224, 748–756, https://doi.org/10.1002/jcp.22177.

    • Crossref
    • PubMed
    • Export Citation
  • Myung, J.; Gulesserian, T.; Fountoulakis, M.; Lubec, G. Deranged hypothetical proteins Rik protein, Nit protein 2 and mitochondrial inner membrane protein, Mitofilin, in fetal Down syndrome brain. Cell Mol. Biol. (Noisy-le-grand) 2003, 49, 739–746.

    • PubMed
    • Export Citation
  • Neupert, W. A perspective on transport of proteins into mitochondria: a myriad of open questions. J. Mol. Biol. 2015, 427, 1135–1158, https://doi.org/10.1016/j.jmb.2015.02.001.

    • Crossref
    • PubMed
    • Export Citation
  • Odgren, P. R.; Toukatly, G.; Bangs, P. L.; Gilmore, R.; Fey, E. G. Molecular characterization of mitofilin (HMP), a mitochondria-associated protein with predicted coiled coil and intermembrane space targeting domains. J. Cell Sci. 1996, 109, 2253–2264.

    • PubMed
    • Export Citation
  • Omori, A.; Ichinose, S.; Kitajima, S.; Shimotohno, K. W.; Murashima, Y. L.; Shimotohno, K.; Seto-Ohshima, A. Gerbils of a seizure-sensitive strain have a mitochondrial inner membrane protein with different isoelectric points from those of a seizure-resistant strain. Electrophoresis 2002, 23, 4167–4174, https://doi.org/10.1002/elps.200290034.

    • Crossref
    • PubMed
    • Export Citation
  • Ott, C.; Dorsch, E.; Fraunholz, M.; Straub, S.; Kozjak-Pavlovic, V. Detailed analysis of the human mitochondrial contact site complex indicate a hierarchy of subunits. PLoS One 2015, 10, e0120213, https://doi.org/10.1371/journal.pone.0120213.

    • PubMed
    • Export Citation
  • Ott, C.; Ross, K.; Straub, S.; Thiede, B.; Gotz, M.; Goosmann, C.; Krischke, M.; Mueller, M. J.; Krohne, G.; Rudel, T., et al. Sam50 functions in mitochondrial intermembrane space bridging and biogenesis of respiratory complexes. Mol. Cell Biol. 2012, 32, 1173–1188.

    • Crossref
    • PubMed
    • Export Citation
  • Park, Y. U.; Jeong, J.; Lee, H.; Mun, J. Y.; Kim, J. H.; Lee, J. S.; Nguyen, M. D.; Han, S. S.; Suh, P. G.; Park, S. K. Disrupted-in-schizophrenia 1 (DISC1) plays essential roles in mitochondria in collaboration with Mitofilin. Proc. Natl. Acad. Sci. USA 2010, 107, 17785–17790, https://doi.org/10.1073/pnas.1004361107.

    • Crossref
    • Export Citation
  • Paumard, P.; Vaillier, J.; Coulary, B.; Schaeffer, J.; Soubannier, V.; Mueller, D. M.; Brethes, D.; di Rago, J. P.; Velours, J. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 2002, 21, 221–230, https://doi.org/10.3410/f.1005091.59955.

    • Crossref
    • PubMed
    • Export Citation
  • Penttila, S.; Jokela, M.; Bouquin, H.; Saukkonen, A. M.; Toivanen, J.; Udd, B. Late onset spinal motor neuronopathy is caused by mutation in CHCHD10. Ann. Neurol. 2015, 77, 163–172, https://doi.org/10.1002/ana.24319.

    • Crossref
    • PubMed
    • Export Citation
  • Perkins, G. A.; Ellisman, M. H. Mitochondrial configurations in peripheral nerve suggest differential ATP production. J. Struct. Biol. 2011, 173, 117–127, https://doi.org/10.1016/j.jsb.2010.06.017.

    • Crossref
    • PubMed
    • Export Citation
  • Perkins, G. A.; Tjong, J.; Brown, J. M.; Poquiz, P. H.; Scott, R. T.; Kolson, D. R.; Ellisman, M. H.; Spirou, G. A. The micro-architecture of mitochondria at active zones: electron tomography reveals novel anchoring scaffolds and cristae structured for high-rate metabolism. J. Neurosci. 2010, 30, 1015–1026, https://doi.org/10.1523/jneurosci.1517-09.2010.

    • Crossref
    • PubMed
    • Export Citation
  • Pfanner, N.; van der Laan, M.; Amati, P.; Capaldi, R. A.; Caudy, A. A.; Chacinska, A.; Darshi, M.; Deckers, M.; Hoppins, S.; Icho, T., et al. Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J. Cell Biol. 2014, 204, 1083–1086, https://doi.org/10.1083/jcb.201401006.

    • Crossref
    • PubMed
    • Export Citation
  • Pfeiffer, K.; Gohil, V.; Stuart, R. A.; Hunte, C.; Brandt, U.; Greenberg, M. L.; Schagger, H. Cardiolipin stabilizes respiratory chain supercomplexes. J. Cell Biol. 2003, 278, 52873–52880, https://doi.org/10.1074/jbc.m308366200.

  • Potting, C.; Tatsuta, T.; Konig, T.; Haag, M.; Wai, T.; Aaltonen, M. J.; Langer, T. TRIAP1/PRELI complexes prevent apoptosis by mediating intramitochondrial transport of phosphatidic acid. Cell Metab. 2013, 18, 287–295, https://doi.org/10.1016/j.cmet.2013.07.008.

    • Crossref
    • PubMed
    • Export Citation
  • Potting, C.; Wilmes, C.; Engmann, T.; Osman, C.; Langer, T. Regulation of mitochondrial phospholipids by Ups1/PRELI-like proteins depends on proteolysis and Mdm35. EMBO J. 2010, 29, 2888–2898, https://doi.org/10.1038/emboj.2010.169.

    • Crossref
    • PubMed
    • Export Citation
  • Qiu, J.; Wenz, L. S.; Zerbes, R. M.; Oeljeklaus, S.; Bohnert, M.; Stroud, D. A.; Wirth, C.; Ellenrieder, L.; Thornton, N.; Kutik, S., et al. Coupling of mitochondrial import and export translocases by receptor-mediated supercomplex formation. Cell 2013, 154, 596–608.

    • Crossref
    • PubMed
    • Export Citation
  • Rabl, R.; Soubannier, V.; Scholz, R.; Vogel, F.; Mendl, N.; Vasiljev-Neumeyer, A.; Korner, C.; Jagasia, R.; Keil, T.; Baumeister, W., et al. Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J. Cell Biol. 2009, 185, 1047–1063, https://doi.org/10.1083/jcb.200811099.

    • Crossref
    • Export Citation
  • Rampelt, H.; Bohnert, M.; Zerbes, R. M.; Horvath, S. E.; Warscheid, B.; Pfanner, N.; van der Laan, M. Mic10, a core subunit of the mitochondrial contact site and cristae organizing system, interacts with the dimeric F1Fo-ATP synthase. J. Mol. Biol. 2017, 429, 1162–1170, https://doi.org/10.1016/j.jmb.2017.03.006.

    • Crossref
    • PubMed
    • Export Citation
  • Rampelt, H.; Wollweber, F.; Gerke, C.; de Boer, R.; van der Klei, I. J.; Bohnert, M.; Pfanner, N.; van der Laan, M. Assembly of the mitochondrial cristae organizer Mic10 is regulated by Mic26-Mic27 antagonism and cardiolipin. J. Mol. Biol. 2018, 430, 1883–1890, https://doi.org/10.1016/j.jmb.2018.04.037.

    • Crossref
    • PubMed
    • Export Citation
  • Ronchi, D.; Riboldi, G.; Del Bo, R.; Ticozzi, N.; Scarlato, M.; Galimberti, D.; Corti, S.; Silani, V.; Bresolin, N.; Comi, G. P. CHCHD10 mutations in Italian patients with sporadic amyotrophic lateral sclerosis. Brain 2015, 138, e372, https://doi.org/10.1093/brain/awu384.

    • Crossref
    • PubMed
    • Export Citation
  • Rujiviphat, J.; Wong, M. K.; Won, A.; Shih, Y. L.; Yip, C. M.; McQuibban, G. A. Mitochondrial genome maintenance 1 (Mgm1) protein alters membrane topology and promotes local membrane bending. J. Mol. Biol. 2015, 427, 2599–2609, https://doi.org/10.1016/j.jmb.2015.03.006.

    • Crossref
    • PubMed
    • Export Citation
  • Sakowska, P.; Jans, D. C.; Mohanraj, K.; Riedel, D.; Jakobs, S.; Chacinska, A. The oxidation status of Mic19 regulates MICOS assembly. Mol. Cell Biol. 2015, 35, 4222–4237, https://doi.org/10.1128/mcb.00578-15.

    • Crossref
    • PubMed
    • Export Citation
  • Schlame, M.; Haldar, D. Cardiolipin is synthesized on the matrix side of the inner membrane in rat liver mitochondria. J. Cell Biol. 1993, 268, 74–79, https://doi.org/10.1016/0005-2728(79)90105-1.

  • Serricchio, M.; Vissa, A.; Kim, P. K.; Yip, C. M.; McQuibban, G. A. Cardiolipin synthesizing enzymes form a complex that interacts with cardiolipin-dependent membrane organizing proteins. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2018, 1863, 447–457, https://doi.org/10.1016/j.bbalip.2018.01.007.

    • Crossref
    • Export Citation
  • Sesaki, H.; Southard, S. M.; Yaffe, M. P.; Jensen, R. E. Mgm1p, a dynamin-related GTPase, is essential for fusion of the mitochondrial outer membrane. Mol. Biol. Cell 2003, 14, 2342–2356, https://doi.org/10.1091/mbc.e02-12-0788.

    • Crossref
    • PubMed
    • Export Citation
  • Shutov, L. P.; Kim, M. S.; Houlihan, P. R.; Medvedeva, Y. V.; Usachev, Y. M. Mitochondria and plasma membrane Ca2+-ATPase control presynaptic Ca2+ clearance in capsaicin-sensitive rat sensory neurons. J Physiol 2013, 591, 2443–2462, https://doi.org/10.1113/jphysiol.2012.249219.

    • Crossref
    • PubMed
    • Export Citation
  • Simbeni, R.; Paltauf, F.; Daum, G. Intramitochondrial transfer of phospholipids in the yeast, Saccharomyces cerevisiae. J. Cell Biol. 1990, 265, 281–285, https://doi.org/10.1016/b978-0-12-384730-0.00291-3.

  • Simbeni, R.; Pon, L.; Zinser, E.; Paltauf, F.; Daum, G. Mitochondrial membrane contact sites of yeast. Characterization of lipid components and possible involvement in intramitochondrial translocation of phospholipids. J. Cell Biol. 1991, 266, 10047–10049, https://doi.org/10.1007/978-981-10-4567-7_9.

  • Song, Z.; Ghochani, M.; McCaffery, J. M.; Frey, T. G.; Chan, D. C. Mitofusins and OPA1 mediate sequential steps in mitochondrial membrane fusion. Mol. Biol. Cell 2009, 20, 3525–3532, https://doi.org/10.1091/mbc.e09-03-0252.

    • Crossref
    • PubMed
    • Export Citation
  • Straub, I. R.; Janer, A.; Weraarpachai, W.; Zinman, L.; Robertson, J.; Rogaeva, E.; Shoubridge, E. A. Loss of CHCHD10-CHCHD2 complexes required for respiration underlies the pathogenicity of a CHCHD10 mutation in ALS. Hum. Mol. Genet. 2018, 27, 178–189, https://doi.org/10.1093/hmg/ddx393.

    • Crossref
    • PubMed
    • Export Citation
  • Strauss, M.; Hofhaus, G.; Schroder, R. R.; Kuhlbrandt, W. Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J. 2008, 27, 1154–1160, https://doi.org/10.1038/emboj.2008.35.

    • Crossref
    • PubMed
    • Export Citation
  • Sun, M. G.; Williams, J.; Munoz-Pinedo, C.; Perkins, G. A.; Brown, J. M.; Ellisman, M. H.; Green, D. R.; Frey, T. G. Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis. Nat. Cell Biol. 2007, 9, 1057–1065, https://doi.org/10.1038/ncb1630.

    • Crossref
    • PubMed
    • Export Citation
  • Tamura, Y.; Endo, T.; Iijima, M.; Sesaki, H. Ups1p and Ups2p antagonistically regulate cardiolipin metabolism in mitochondria. J. Cell Biol. 2009, 185, 1029–1045, https://doi.org/10.1083/jcb.200812018.

    • Crossref
    • PubMed
    • Export Citation
  • Tamura, Y.; Harada, Y.; Yamano, K.; Watanabe, K.; Ishikawa, D.; Ohshima, C.; Nishikawa, S.; Yamamoto, H.; Endo, T. Identification of Tam41 maintaining integrity of the TIM23 protein translocator complex in mitochondria. J. Cell Biol. 2006, 174, 631–637, https://doi.org/10.1083/jcb.200603087.

    • Crossref
    • PubMed
    • Export Citation
  • Tamura, Y.; Onguka, O.; Hobbs, A. E.; Jensen, R. E.; Iijima, M.; Claypool, S. M.; Sesaki, H. Role for two conserved intermembrane space proteins, Ups1p and Ups2p, [corrected] in intra-mitochondrial phospholipid trafficking. J. Cell Biol. 2012, 287, 15205–15218, https://doi.org/10.1074/jbc.a111.338665.

  • Tarasenko, D.; Barbot, M.; Jans, D. C.; Kroppen, B.; Sadowski, B.; Heim, G.; Mobius, W.; Jakobs, S.; Meinecke, M. The MICOS component Mic60 displays a conserved membrane-bending activity that is necessary for normal cristae morphology. J. Cell Biol. 2017, 216, 889–899, https://doi.org/10.1083/jcb.201609046.

    • Crossref
    • PubMed
    • Export Citation
  • Tasseva, G.; Bai, H. D.; Davidescu, M.; Haromy, A.; Michelakis, E.; Vance, J. E. Phosphatidylethanolamine deficiency in mammalian mitochondria impairs oxidative phosphorylation and alters mitochondrial morphology. J. Cell Biol. 2013, 288, 4158–4173, https://doi.org/10.1074/jbc.m112.434183.

  • Tsai, P. I.; Lin, C. H.; Hsieh, C. H.; Papakyrikos, A. M.; Kim, M. J.; Napolioni, V.; Schoor, C.; Couthouis, J.; Wu, R. M.; Wszolek, Z. K., et al. PINK1 phosphorylates MIC60/Mitofilin to control structural plasticity of mitochondrial crista junctions. Mol. Cell 2018, 69, 744–756 e746, https://doi.org/10.1016/j.molcel.2018.01.026.

    • Crossref
    • PubMed
    • Export Citation
  • Vaccaro, V.; Devine, M. J.; Higgs, N. F.; Kittler, J. T. Miro1-dependent mitochondrial positioning drives the rescaling of presynaptic Ca2+ signals during homeostatic plasticity. EMBO Rep. 2017, 18, 231–240, https://doi.org/10.15252/embr.201642710.

    • Crossref
    • PubMed
    • Export Citation
  • van Golde, L. M.; Raben, J.; Batenburg, J. J.; Fleischer, B.; Zambrano, F.; Fleischer, S. Biosynthesis of lipids in Golgi complex and other subcellular fractions from rat liver. Biochim. Biophys. Acta 1974, 360, 179–192, https://doi.org/10.1016/0005-2760(74)90168-4.

    • Crossref
    • PubMed
    • Export Citation
  • Van Laar, V. S.; Berman, S. B.; Hastings, T. G. Mic60/mitofilin overexpression alters mitochondrial dynamics and attenuates vulnerability of dopaminergic cells to dopamine and rotenone. Neurobiol. Dis. 2016, 91, 247–261, https://doi.org/10.1016/j.nbd.2016.03.015.

    • Crossref
    • PubMed
    • Export Citation
  • von der Malsburg, K.; Muller, J. M.; Bohnert, M.; Oeljeklaus, S.; Kwiatkowska, P.; Becker, T.; Loniewska-Lwowska, A.; Wiese, S.; Rao, S.; Milenkovic, D., et al. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev. Cell 2011, 21, 694–707, https://doi.org/10.1016/j.devcel.2011.08.026.

    • Crossref
    • PubMed
    • Export Citation
  • Waagepetersen, H. S.; Sonnewald, U.; Gegelashvili, G.; Larsson, O. M.; Schousboe, A. Metabolic distinction between vesicular and cytosolic GABA in cultured GABAergic neurons using 13C magnetic resonance spectroscopy. J. Neurosci. Res. 2001, 63, 347–355, https://doi.org/10.1002/1097-4547(20010215)63:4%3C347::aid-jnr1029%3E3.0.co;2-g.

    • Crossref
    • PubMed
    • Export Citation
  • Wasilewski, M.; Semenzato, M.; Rafelski, S. M.; Robbins, J.; Bakardjiev, A. I.; Scorrano, L. Optic atrophy 1-dependent mitochondrial remodeling controls steroidogenesis in trophoblasts. Curr Biol 2012, 22, 1228–1234, https://doi.org/10.1016/j.cub.2012.04.054.

    • Crossref
    • PubMed
    • Export Citation
  • Weber, T. A.; Koob, S.; Heide, H.; Wittig, I.; Head, B.; van der Bliek, A.; Brandt, U.; Mittelbronn, M.; Reichert, A. S. APOOL is a cardiolipin-binding constituent of the Mitofilin/MINOS protein complex determining cristae morphology in mammalian mitochondria. PLoS One 2013, 8, e63683, https://doi.org/10.1371/journal.pone.0063683.

    • PubMed
    • Export Citation
  • Wenz, L. S.; Ellenrieder, L.; Qiu, J.; Bohnert, M.; Zufall, N.; van der Laan, M.; Pfanner, N.; Wiedemann, N.; Becker, T. Sam37 is crucial for formation of the mitochondrial TOM-SAM supercomplex, thereby promoting β-barrel biogenesis. J. Cell Biol. 2015, 210, 1047–1054, https://doi.org/10.1083/jcb.201504119.

    • Crossref
    • PubMed
    • Export Citation
  • Wenz, T.; Hielscher, R.; Hellwig, P.; Schagger, H.; Richers, S.; Hunte, C. Role of phospholipids in respiratory cytochrome bc1 complex catalysis and supercomplex formation. Biochim. Biophys. Acta 2009, 1787, 609–616, https://doi.org/10.1016/j.bbabio.2009.02.012.

    • Crossref
    • PubMed
    • Export Citation
  • Wishart, T. M.; Paterson, J. M.; Short, D. M.; Meredith, S.; Robertson, K. A.; Sutherland, C.; Cousin, M. A.; Dutia, M. B.; Gillingwater, T. H. Differential proteomics analysis of synaptic proteins identifies potential cellular targets and protein mediators of synaptic neuroprotection conferred by the slow Wallerian degeneration (Wlds) gene. Mol. Cell Proteomics. 2007, 6, 1318–1330, https://doi.org/10.24235/eduma.v1i1.278.

    • Crossref
    • PubMed
    • Export Citation
  • Wong, E. D.; Wagner, J. A.; Gorsich, S. W.; McCaffery, J. M.; Shaw, J. M.; Nunnari, J. The dynamin-related GTPase, Mgm1p, is an intermembrane space protein required for maintenance of fusion competent mitochondria. J. Cell Biol. 2000, 151, 341–352, https://doi.org/10.1083/jcb.151.2.341.

    • Crossref
    • PubMed
    • Export Citation
  • Woo, J. A.; Liu, T.; Trotter, C.; Fang, C. C.; De Narvaez, E.; LePochat, P.; Maslar, D.; Bukhari, A.; Zhao, X.; Deonarine, A., et al. Loss of function CHCHD10 mutations in cytoplasmic TDP-43 accumulation and synaptic integrity. Nat. Commun. 2017, 8, 15558, https://doi.org/10.1038/ncomms15558.

    • Crossref
    • PubMed
    • Export Citation
  • Xiao, T.; Jiao, B.; Zhang, W.; Pan, C.; Wei, J.; Liu, X.; Zhou, Y.; Zhou, L.; Tang, B.; Shen, L. Identification of CHCHD10 mutation in Chinese patients with Alzheimer disease. Mol. Neurobiol. 2017, 54, 5243–5247, https://doi.org/10.1007/s12035-016-0056-3.

    • Crossref
    • PubMed
    • Export Citation
  • Xie, J.; Marusich, M. F.; Souda, P.; Whitelegge, J.; Capaldi, R. A. The mitochondrial inner membrane protein mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled-coil-helix coiled-coil-helix domain-containing protein 3 and 6 and DnaJC11. FEBS Lett. 2007, 581, 3545–3549, https://doi.org/10.1016/j.febslet.2007.06.052.

    • Crossref
    • PubMed
    • Export Citation
  • Xu, Y.; Anjaneyulu, M.; Donelian, A.; Yu, W.; Greenberg, M. L.; Ren, M.; Owusu-Ansah, E.; Schlame, M. Assembly of the complexes of oxidative phosphorylation triggers the remodeling of cardiolipin. Proc. Natl. Acad. Sci. USA 2019, 116, 11235–11240, https://doi.org/10.1073/pnas.1900890116.

    • Crossref
    • Export Citation
  • Zborowski, J.; Dygas, A.; Wojtczak, L. Phosphatidylserine decarboxylase is located on the external side of the inner mitochondrial membrane. FEBS Lett 1983, 157, 179–182, https://doi.org/10.1016/0014-5793(83)81141-7.

    • Crossref
    • PubMed
    • Export Citation
  • Zeharia, A.; Friedman, J. R.; Tobar, A.; Saada, A.; Konen, O.; Fellig, Y.; Shaag, A.; Nunnari, J.; Elpeleg, O. Mitochondrial hepato-encephalopathy due to deficiency of QIL1/MIC13 (C19orf70), a MICOS complex subunit. Eur. J. Hum. Genet. 2016, 24, 1778–1782, https://doi.org/10.1038/ejhg.2016.83.

    • Crossref
    • PubMed
    • Export Citation
  • Zerbes, R. M.; Bohnert, M.; Stroud, D. A.; von der Malsburg, K.; Kram, A.; Oeljeklaus, S.; Warscheid, B.; Becker, T.; Wiedemann, N.; Veenhuis, M. Role of MINOS in mitochondrial membrane architecture: cristae morphology and outer membrane interactions differentially depend on mitofilin domains. J. Mol. Biol. 2012, 422, 183–191, https://doi.org/10.1016/j.jmb.2012.05.004.

    • Crossref
    • PubMed
    • Export Citation
  • Zerbes, R. M.; Hoss, P.; Pfanner, N.; van der Laan, M.; Bohnert, M., et al. Distinct roles of Mic12 and Mic27 in the mitochondrial contact site and cristae organizing system. J. Mol. Biol. 2016, 428, 1485–1492, https://doi.org/10.1016/j.jmb.2016.02.031.

    • Crossref
    • PubMed
    • Export Citation
  • Zhu, X. H.; Qiao, H.; Du, F.; Xiong, Q.; Liu, X.; Zhang, X.; Ugurbil, K.; Chen, W. Quantitative imaging of energy expenditure in human brain. Neuroimage 2012, 60, 2107–2117, https://doi.org/10.1016/j.neuroimage.2012.02.013.

    • Crossref
    • PubMed
    • Export Citation
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