The AAA⁺ ATPase ATAD3A Controls Mitochondrial Dynamics at the Interface of the Inner and Outer Membranes

REFERENCES

• Babst, M., B. Wendland, E. J. Estepa, and S. D. Emr. 1998. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17:2982–2993.
   PubMed Web of Science ®Google Scholar
• Bieniossek, C., T. Schalch, M. Bumann, M. Meister, R. Meier, and U. Baumann. 2006. The molecular architecture of the metalloprotease FtsH. Proc. Natl. Acad. Sci. U. S. A. 103:3066–3071.
   PubMedGoogle Scholar
• Bird, I. M., N. A. Hanley, R. A. Word, J. M. Mathis, J. L. McCarthy, J. I. Mason, and W. E. Rainey. 1993. Human NCI-H295 adrenocortical carcinoma cells: a model for angiotensin-II-responsive aldosterone secretion. Endocrinology 133:1555–1561.
   PubMed Web of Science ®Google Scholar
• Bogenhagen, D. F., D. Rousseau, and S. Burke. 2008. The layered structure of human mitochondrial DNA nucleoids. J. Biol. Chem. 283:3665–3675.
   PubMed Web of Science ®Google Scholar
• Boldogh, I. R., and L. A. Pon. 2007. Mitochondria on the move. Trends Cell Biol. 17:502–510.
   PubMedGoogle Scholar
• Chen, Y. I., R. E. Moore, H. Y. Ge, M. K. Young, T. D. Lee, and S. W. Stevens. 2007. Proteomic analysis of in vivo-assembled pre-mRNA splicing complexes expands the catalog of participating factors. Nucleic Acids Res. 35:3928–3944.
   PubMed Web of Science ®Google Scholar
• Cherradi, N., M. F. Rossier, M. B. Vallotton, and A. M. Capponi. 1996. Calcium stimulates intramitochondrial cholesterol transfer in bovine adrenal glomerulosa cells. J. Biol. Chem. 271:25971–25975.
   PubMedGoogle Scholar
• Da Cruz, S., I. Xenarios, J. Langridge, F. Vilbois, P. A. Parone, and J. C. Martinou. 2003. Proteomic analysis of the mouse liver mitochondrial inner membrane. J. Biol. Chem. 278:41566–41571.
   PubMed Web of Science ®Google Scholar
• Detmer, S. A., and D. C. Chan. 2007. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell. Biol. 8:870–879.
   PubMed Web of Science ®Google Scholar
• DeVay, R. M., L. Dominguez-Ramirez, L. L. Lackner, S. Hoppins, H. Stahlberg, and J. Nunnari. 2009. Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion. J. Cell Biol. 186:793–803.
   PubMedGoogle Scholar
• Dietzl, G., D. Chen, F. Schnorrer, K. C. Su, Y. Barinova, M. Fellner, B. Gasser, K. Kinsey, S. Oppel, S. Scheiblauer, A. Couto, V. Marra, K. Keleman, and B. J. Dickson. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151–156.
   PubMed Web of Science ®Google Scholar
• Errico, A., A. Ballabio, and E. I. Rugarli. 2002. Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. Hum. Mol. Genet. 11:153–163.
   PubMed Web of Science ®Google Scholar
• Erzberger, J. P., and J. M. Berger. 2006. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 35:93–114.
   PubMedGoogle Scholar
• Folsch, H., B. Guiard, W. Neupert, and R. A. Stuart. 1996. Internal targeting signal of the BCS1 protein: a novel mechanism of import into mitochondria. EMBO J. 15:479–487.
   PubMedGoogle Scholar
• Gandre-Babbe, S., and A. M. van der Bliek. 2008. The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell 19:2402–2412.
   PubMed Web of Science ®Google Scholar
• Geuijen, C. A., N. Bijl, R. C. Smit, F. Cox, M. Throsby, T. J. Visser, M. A. Jongeneelen, A. B. Bakker, A. M. Kruisbeek, J. Goudsmit, and J. de Kruif. 2005. A proteomic approach to tumour target identification using phage display, affinity purification and mass spectrometry. Eur. J. Cancer 41:178–187.
   PubMedGoogle Scholar
• Grandemange, S., S. Herzig, and J. C. Martinou. 2009. Mitochondrial dynamics and cancer. Semin. Cancer Biol. 19:50–56.
   PubMed Web of Science ®Google Scholar
• Griparic, L., N. N. van der Wel, I. J. Orozco, P. J. Peters, and A. M. van der Bliek. 2004. Loss of the intermembrane space protein Mgm1/OPA1 induces swelling and localized constrictions along the lengths of mitochondria. J. Biol. Chem. 279:18792–18798.
   PubMed Web of Science ®Google Scholar
• Guertin, D. A., K. V. Guntur, G. W. Bell, C. C. Thoreen, and D. M. Sabatini. 2006. Functional genomics identifies TOR-regulated genes that control growth and division. Curr. Biol. 16:958–970.
   PubMed Web of Science ®Google Scholar
• Hackenbrock, C. R., and K. J. Miller. 1975. The distribution of anionic sites on the surfaces of mitochondrial membranes. Visual probing with polycationic ferritin. J. Cell Biol. 65:615–630.
   PubMedGoogle Scholar
• He, J., C. C. Mao, A. Reyes, H. Sembongi, M. Di Re, C. Granycome, A. B. Clippingdale, I. M. Fearnley, M. Harbour, A. J. Robinson, S. Reichelt, J. N. Spelbrink, J. E. Walker, and I. J. Holt. 2007. The AAA+ protein ATAD3 has displacement loop binding properties and is involved in mitochondrial nucleoid organization. J. Cell Biol. 176:141–146.
   PubMed Web of Science ®Google Scholar
• Hoffmann, M., N. Bellance, R. Rossignol, W. J. Koopman, P. H. Willems, E. Mayatepek, O. Bossinger, and F. Distelmaier. 2009. Caenorhabditis elegans ATAD-3 is essential for mitochondrial activity and development. PLoS One 4:e7644.
   PubMedGoogle Scholar
• Hubstenberger, A., G. Labourdette, J. Baudier, and D. Rousseau. 2008. ATAD 3A and ATAD 3B are distal 1p-located genes differentially expressed in human glioma cell lines and present in vitro anti-oncogenic and chemoresistant properties. Exp. Cell Res. 314:2870–2883.
   PubMedGoogle Scholar
• Jefcoate, C. 2002. High-flux mitochondrial cholesterol trafficking, a specialized function of the adrenal cortex. J. Clin. Invest. 110:881–890.
   PubMed Web of Science ®Google Scholar
• Langer, T. 2000. AAA proteases: cellular machines for degrading membrane proteins. Trends Biochem. Sci. 25:247–251.
   PubMed Web of Science ®Google Scholar
• Langer, T., M. Kaser, C. Klanner, and K. Leonhard. 2001. AAA proteases of mitochondria: quality control of membrane proteins and regulatory functions during mitochondrial biogenesis. Biochem. Soc. Trans. 29:431–436.
   PubMed Web of Science ®Google Scholar
• McBride, H. M., M. Neuspiel, and S. Wasiak. 2006. Mitochondria: more than just a powerhouse. Curr. Biol. 16:R551–R560.
   PubMed Web of Science ®Google Scholar
• Mootha, V. K., J. Bunkenborg, J. V. Olsen, M. Hjerrild, J. R. Wisniewski, E. Stahl, M. S. Bolouri, H. N. Ray, S. Sihag, M. Kamal, N. Patterson, E. S. Lander, and M. Mann. 2003. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115:629–640.
   PubMed Web of Science ®Google Scholar
• Ogura, T., and A. J. Wilkinson. 2001. AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 6:575–597.
   PubMed Web of Science ®Google Scholar
• Okamoto, K., and J. M. Shaw. 2005. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 39:503–536.
   PubMed Web of Science ®Google Scholar
• Pignoni, F., and S. L. Zipursky. 1997. Induction of Drosophila eye development by decapentaplegic. Development 124:271–278.
   PubMedGoogle Scholar
• Pilling, A. D., D. Horiuchi, C. M. Lively, and W. M. Saxton. 2006. Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol. Biol. Cell 17:2057–2068.
   PubMed Web of Science ®Google Scholar
• Pon, L., T. Moll, D. Vestweber, B. Marshallsay, and G. Schatz. 1989. Protein import into mitochondria: ATP-dependent protein translocation activity in a submitochondrial fraction enriched in membrane contact sites and specific proteins. J. Cell Biol. 109:2603–2616.
   PubMedGoogle Scholar
• Reichert, A. S., and W. Neupert. 2002. Contact sites between the outer and inner membrane of mitochondria-role in protein transport. Biochim. Biophys. Acta 1592:41–49.
   PubMedGoogle Scholar
• Roll-Mecak, A., and R. D. Vale. 2008. Structural basis of microtubule severing by the hereditary spastic paraplegia protein spastin. Nature 451:363–367.
   PubMedGoogle Scholar
• Rone, M. B., J. Fan, and V. Papadopoulos. 2009. Cholesterol transport in steroid biosynthesis: role of protein-protein interactions and implications in disease states. Biochim. Biophys. Acta 1791:646–658.
   PubMed Web of Science ®Google Scholar
• Rouiller, I., V. M. Butel, M. Latterich, R. A. Milligan, and E. M. Wilson-Kubalek. 2000. A major conformational change in p97 AAA ATPase upon ATP binding. Mol. Cell 6:1485–1490.
   PubMedGoogle Scholar
• Scott, R. C., O. Schuldiner, and T. P. Neufeld. 2004. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 7:167–178.
   PubMed Web of Science ®Google Scholar
• Shiao, Y. J., B. Balcerzak, and J. E. Vance. 1998. A mitochondrial membrane protein is required for translocation of phosphatidylserine from mitochondria-associated membranes to mitochondria. Biochem. J. 331 (Pt. 1):217–223.
   PubMedGoogle Scholar
• Smirnova, E., L. Griparic, D. L. Shurland, and A. M. van der Bliek. 2001. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12:2245–2256.
   PubMed Web of Science ®Google Scholar
• Stan, T., J. Brix, J. Schneider-Mergener, N. Pfanner, W. Neupert, and D. Rapaport. 2003. Mitochondrial protein import: recognition of internal import signals of BCS1 by the TOM complex. Mol. Cell. Biol. 23:2239–2250.
   PubMedGoogle Scholar
• Thibault, S. T., M. A. Singer, W. Y. Miyazaki, B. Milash, N. A. Dompe, C. M. Singh, R. Buchholz, M. Demsky, R. Fawcett, H. L. Francis-Lang, L. Ryner, L. M. Cheung, A. Chong, C. Erickson, W. W. Fisher, K. Greer, S. R. Hartouni, E. Howie, L. Jakkula, D. Joo, K. Killpack, A. Laufer, J. Mazzotta, R. D. Smith, L. M. Stevens, C. Stuber, L. R. Tan, R. Ventura, A. Woo, I. Zakrajsek, L. Zhao, F. Chen, C. Swimmer, C. Kopczynski, G. Duyk, M. L. Winberg, and J. Margolis. 2004. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36:283–287.
   PubMed Web of Science ®Google Scholar
• Thomson, M. 2003. Does cholesterol use the mitochondrial contact site as a conduit to the steroidogenic pathway? Bioessays 25:252–258.
   PubMedGoogle Scholar
• Wang, Y., and D. F. Bogenhagen. 2006. Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane. J. Biol. Chem. 281:25791–25802.
   PubMed Web of Science ®Google Scholar
• Westermann, B. 2008. Molecular machinery of mitochondrial fusion and fission. J. Biol. Chem. 283:13501–13505.
   PubMed Web of Science ®Google Scholar