Central Role of Mic10 in the Mitochondrial Contact Site and Cristae Organizing System (original) (raw)

Abstract

Graphical Abstract Highlights d MICOS core subunit Mic10 is targeted into mitochondria by a charged internal loop d Two conserved glycine motifs are required to form large Mic10 oligomers d Overexpression of Mic10 strongly alters inner membrane extent and architecture d Mic10 oligomers play a central role in the formation of crista junctions

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References (32)

  1. Alavian, K.N., Beutner, G., Lazrove, E., Sacchetti, S., Park, H.-A., Licznerski, P., Li, H., Nabili, P., Hockensmith, K., Graham, M., et al. (2014). An uncou- pling channel within the c-subunit ring of the F 1 F O ATP synthase is the mito- chondrial permeability transition pore. Proc. Natl. Acad. Sci. USA 111, 10580-10585.
  2. Alkhaja, A.K., Jans, D.C., Nikolov, M., Vukotic, M., Lytovchenko, O., Ludewig, F., Schliebs, W., Riedel, D., Urlaub, H., Jakobs, S., and Deckers, M. (2012). MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Mol. Biol. Cell 23, 247-257.
  3. Bohnert, M., Wenz, L.-S., Zerbes, R.M., Horvath, S.E., Stroud, D.A., von der Malsburg, K., Mu ¨ller, J.M., Oeljeklaus, S., Perschil, I., Warscheid, B., et al. (2012). Role of mitochondrial inner membrane organizing system in protein biogenesis of the mitochondrial outer membrane. Mol. Biol. Cell 23, 3948- 3956.
  4. Darshi, M., Mendiola, V.L., Mackey, M.R., Murphy, A.N., Koller, A., Perkins, G.A., Ellisman, M.H., and Taylor, S.S. (2011). ChChd3, an inner mitochondrial membrane protein, is essential for maintaining crista integrity and mitochon- drial function. J. Biol. Chem. 286, 2918-2932.
  5. Davies, K.M., Anselmi, C., Wittig, I., Faraldo-Go ´mez, J.D., and Ku ¨hlbrandt, W. (2012). Structure of the yeast F 1 F o -ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. USA 109, 13602-13607.
  6. Frey, T.G., and Mannella, C.A. (2000). The internal structure of mitochondria. Trends Biochem. Sci. 25, 319-324.
  7. Frezza, C., Cipolat, S., Martins de Brito, O., Micaroni, M., Beznoussenko, G.V., Rudka, T., Bartoli, D., Polishuck, R.S., Danial, N.N., De Strooper, B., and Scorrano, L. (2006). OPA1 controls apoptotic cristae remodeling indepen- dently from mitochondrial fusion. Cell 126, 177-189.
  8. Harner, M., Ko ¨rner, C., Walther, D., Mokranjac, D., Kaesmacher, J., Welsch, U., Griffith, J., Mann, M., Reggiori, F., and Neupert, W. (2011). The mitochon- drial contact site complex, a determinant of mitochondrial architecture. EMBO J. 30, 4356-4370.
  9. Head, B.P., Zulaika, M., Ryazantsev, S., and van der Bliek, A.M. (2011). A novel mitochondrial outer membrane protein, MOMA-1, that affects cristae morphology in Caenorhabditis elegans. Mol. Biol. Cell 22, 831-841.
  10. Hoppins, S., Collins, S.R., Cassidy-Stone, A., Hummel, E., Devay, R.M., Lackner, L.L., Westermann, B., Schuldiner, M., Weissman, J.S., and Nunnari, J. (2011). A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochon- dria. J. Cell Biol. 195, 323-340.
  11. Jans, D.C., Wurm, C.A., Riedel, D., Wenzel, D., Stagge, F., Deckers, M., Rehling, P., and Jakobs, S. (2013). STED super-resolution microscopy reveals an array of MINOS clusters along human mitochondria. Proc. Natl. Acad. Sci. USA 110, 8936-8941.
  12. John, G.B., Shang, Y., Li, L., Renken, C., Mannella, C.A., Selker, J.M.L., Rangell, L., Bennett, M.J., and Zha, J. (2005). The mitochondrial inner mem- brane protein mitofilin controls cristae morphology. Mol. Biol. Cell 16, 1543- 1554.
  13. Ko ¨rner, C., Barrera, M., Dukanovic, J., Eydt, K., Harner, M., Rabl, R., Vogel, F., Rapaport, D., Neupert, W., and Reichert, A.S. (2012). 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 23, 2143-2155.
  14. Meeusen, S., DeVay, R., Block, J., Cassidy-Stone, A., Wayson, S., McCaffery, J.M., and Nunnari, J. (2006). Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell 127, 383-395.
  15. Merkwirth, C., Dargazanli, S., Tatsuta, T., Geimer, S., Lo ¨wer, B., Wunderlich, F.T., von Kleist-Retzow, J.C., Waisman, A., Westermann, B., and Langer, T. (2008). Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev. 22, 476-488.
  16. Mun, J.Y., Lee, T.H.L., Kim, J.H., Yoo, B.H., Bahk, Y.Y., Koo, H.-S., and Han, S.S. (2010). Caenorhabditis elegans mitofilin homologs control the morphology of mitochondrial cristae and influence reproduction and physiology. J. Cell. Physiol. 224, 748-756.
  17. Ott, C., Ross, K., Straub, S., Thiede, B., Go ¨tz, M., Goosmann, C., Krischke, M., Mueller, M.J., Krohne, G., Rudel, T., and Kozjak-Pavlovic, V. (2012). Sam50 functions in mitochondrial intermembrane space bridging and biogenesis of respiratory complexes. Mol. Cell. Biol. 32, 1173-1188.
  18. Paumard, P., Vaillier, J., Coulary, B., Schaeffer, J., Soubannier, V., Mueller, D.M., Bre `thes, D., di Rago, J.-P., and Velours, J. (2002). The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21, 221-230.
  19. 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. (2014). Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J. Cell Biol. 204, 1083-1086.
  20. Rabl, R., Soubannier, V., Scholz, R., Vogel, F., Mendl, N., Vasiljev-Neumeyer, A., Ko ¨rner, C., Jagasia, R., Keil, T., Baumeister, W., et al. (2009). Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J. Cell Biol. 185, 1047-1063.
  21. Russ, W.P., and Engelman, D.M. (2000). The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 296, 911-919.
  22. Senes, A., Engel, D.E., and DeGrado, W.F. (2004). Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14, 465-479.
  23. Strauss, M., Hofhaus, G., Schro ¨der, R.R., and Ku ¨hlbrandt, W. (2008). Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J. 27, 1154-1160.
  24. van der Laan, M., Bohnert, M., Wiedemann, N., and Pfanner, N. (2012). Role of MINOS in mitochondrial membrane architecture and biogenesis. Trends Cell Biol. 22, 185-192.
  25. Vogel, F., Bornho ¨vd, C., Neupert, W., and Reichert, A.S. (2006). Dynamic sub- compartmentalization of the mitochondrial inner membrane. J. Cell Biol. 175, 237-247.
  26. von Ballmoos, C., Wiedenmann, A., and Dimroth, P. (2009). Essentials for ATP synthesis by F 1 F 0 ATP synthases. Annu. Rev. Biochem. 78, 649-672. von der Malsburg, K., Mu ¨ller, J.M., Bohnert, M., Oeljeklaus, S., Kwiatkowska, P., Becker, T., Loniewska-Lwowska, A., Wiese, S., Rao, S., Milenkovic, D., et al. (2011). Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev. Cell 21, 694-707.
  27. Vonck, J., von Nidda, T.K., Meier, T., Matthey, U., Mills, D.J., Ku ¨hlbrandt, W., and Dimroth, P. (2002). Molecular architecture of the undecameric rotor of a bacterial Na + -ATP synthase. J. Mol. Biol. 321, 307-316.
  28. Weber, T.A., Koob, S., Heide, H., Wittig, I., Head, B., van der Bliek, A., Brandt, U., Mittelbronn, M., and Reichert, A.S. (2013). APOOL is a cardiolipin-binding constituent of the Mitofilin/MINOS protein complex determining cristae morphology in mammalian mitochondria. PLoS ONE 8, e63683.
  29. Xie, J., Marusich, M.F., Souda, P., Whitelegge, J., and Capaldi, R.A. (2007). The mitochondrial inner membrane protein mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled-coil-helix coiled-coil-helix domain-contain- ing protein 3 and 6 and DnaJC11. FEBS Lett. 581, 3545-3549.
  30. Zerbes, R.M., Bohnert, M., Stroud, D.A., von der Malsburg, K., Kram, A., Oeljeklaus, S., Warscheid, B., Becker, T., Wiedemann, N., Veenhuis, M., et al. (2012a). Role of MINOS in mitochondrial membrane architecture: cristae morphology and outer membrane interactions differentially depend on mitofilin domains. J. Mol. Biol. 422, 183-191.
  31. Zerbes, R.M., van der Klei, I.J., Veenhuis, M., Pfanner, N., van der Laan, M., and Bohnert, M. (2012b). Mitofilin complexes: conserved organizers of mito- chondrial membrane architecture. Biol. Chem. 393, 1247-1261.
  32. Zick, M., Rabl, R., and Reichert, A.S. (2009). Cristae formation-linking ultra- structure and function of mitochondria. Biochim. Biophys. Acta 1793, 5-19.