The m-AAA Protease Associated with Neurodegeneration Limits MCU Activity in Mitochondria

Molecular Cell

Volumn 64, Issue 1, 2016, Pages 148-162

  König, Tim ^a   Tröder, Simon E ^a   Bakka, Kavya ^a   Korwitz, Anne ^a   Richter Dennerlein, Ricarda ^a   Lampe, Philipp A ^a   Patron, Maria ^a   Mühlmeister, Mareike ^b   Guerrero Castillo, Sergio ^b   Brandt, Ulrich ^b   Decker, Thorsten ^a   Lauria, Ines ^a   Paggio, Angela ^c,d   Rizzuto, Rosario ^c,d   Rugarli, Elena I ^a   De Stefani, Diego ^c,d   Langer, Thomas ^a,e  

^a UNIVERSITY OF COLOGNE   (Germany)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF PADOVA   (Italy)

^d CNR   (Italy)

^e MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PROTEINASE; ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; AFG3L2 PROTEIN, MOUSE; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CHANNEL; CARRIER PROTEIN; M-AAA PROTEASES; METALLOPROTEINASE; MITOCHONDRIAL CALCIUM UNIPORTER;

ARTICLE; BIOGENESIS; CALCIUM TRANSPORT; CELL DEATH; CELL INTERACTION; ENZYME SUBSTRATE; HUMAN; MITOCHONDRION; NERVE DEGENERATION; PROTEIN DEGRADATION; ANIMAL; C57BL MOUSE; CEREBELLUM; CORPUS STRIATUM; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HIPPOCAMPUS; HOMEOSTASIS; ION TRANSPORT; METABOLISM; MOUSE; NERVE CELL; PATHOLOGY; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; ATP-DEPENDENT PROTEASES; CALCIUM; CALCIUM CHANNELS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL DEATH; CEREBELLUM; CORPUS STRIATUM; GENE EXPRESSION REGULATION; HEK293 CELLS; HIPPOCAMPUS; HOMEOSTASIS; HUMANS; ION TRANSPORT; METALLOENDOPEPTIDASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NEURONS; PROTEIN INTERACTION MAPPING; SIGNAL TRANSDUCTION;

EID: 84994082431     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.08.020     Document Type: Article

References (46)

1. Almajan, E.R., Richter, R., Paeger, L., Martinelli, P., Barth, E., Decker, T., Larsson, N.G., Kloppenburg, P., Langer, T., Rugarli, E.I., AFG3L2 supports mitochondrial protein synthesis and Purkinje cell survival. J. Clin. Invest. 122 (2012), 4048–4058.
2. Antony, A.N., Paillard, M., Moffat, C., Juskeviciute, E., Correnti, J., Bolon, B., Rubin, E., Csordás, G., Seifert, E.L., Hoek, J.B., Hajnóczky, G., MICU1 regulation of mitochondrial Ca(2+) uptake dictates survival and tissue regeneration. Nat. Commun., 7, 2016, 10955.
3. Arlt, H., Tauer, R., Feldmann, H., Neupert, W., Langer, T., The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria. Cell 85 (1996), 875–885.
4. Atorino, L., Silvestri, L., Koppen, M., Cassina, L., Ballabio, A., Marconi, R., Langer, T., Casari, G., Loss of m-AAA protease in mitochondria causes complex I deficiency and increased sensitivity to oxidative stress in hereditary spastic paraplegia. J. Cell Biol. 163 (2003), 777–787.
5. Augustin, S., Gerdes, F., Lee, S., Tsai, F.T., Langer, T., Tatsuta, T., An intersubunit signaling network coordinates ATP hydrolysis by m-AAA proteases. Mol. Cell 35 (2009), 574–585.
6. Baker, M.J., Tatsuta, T., Langer, T., Quality control of mitochondrial proteostasis. Cold Spring Harb. Perspect. Biol., 3, 2011, 3.
7. Baker, M.J., Lampe, P.A., Stojanovski, D., Korwitz, A., Anand, R., Tatsuta, T., Langer, T., Stress-induced OMA1 activation and autocatalytic turnover regulate OPA1-dependent mitochondrial dynamics. EMBO J. 33 (2014), 578–593.
8. Banerjee, R., Gladkova, C., Mapa, K., Witte, G., Mokranjac, D., Protein translocation channel of mitochondrial inner membrane and matrix-exposed import motor communicate via two-domain coupling protein. eLife, 4, 2015, e11897.
9. Bernardi, P., Rasola, A., Forte, M., Lippe, G., The mitochondrial permeability transition pore: channel formation by F-ATP synthase, integration in signal transduction, and role in pathophysiology. Physiol. Rev. 95 (2015), 1111–1155.
10. Bohovych, I., Chan, S.S., Khalimonchuk, O., Mitochondrial protein quality control: the mechanisms guarding mitochondrial health. Antioxid. Redox Signal. 22 (2015), 977–994.
11. Casari, G., De Fusco, M., Ciarmatori, S., Zeviani, M., Mora, M., Fernandez, P., De Michele, G., Filla, A., Cocozza, S., Marconi, R., et al. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell 93 (1998), 973–983.
12. Collins, T.J., Lipp, P., Berridge, M.J., Bootman, M.D., Mitochondrial Ca(2+) uptake depends on the spatial and temporal profile of cytosolic Ca(2+) signals. J. Biol. Chem. 276 (2001), 26411–26420.
13. 2+ uniporter. Cell Metab. 17 (2013), 976–987.
14. De Stefani, D., Patron, M., Rizzuto, R., Structure and function of the mitochondrial calcium uniporter complex. Biochim. Biophys. Acta 1853 (2015), 2006–2011.
15. Di Bella, D., Lazzaro, F., Brusco, A., Plumari, M., Battaglia, G., Pastore, A., Finardi, A., Cagnoli, C., Tempia, F., Frontali, M., et al. Mutations in the mitochondrial protease gene AFG3L2 cause dominant hereditary ataxia SCA28. Nat. Genet. 42 (2010), 313–321.
16. Duchen, M.R., Mitochondria, calcium-dependent neuronal death and neurodegenerative disease. Pflugers Arch. 464 (2012), 111–121.
17. Ehses, S., Raschke, I., Mancuso, G., Bernacchia, A., Geimer, S., Tondera, D., Martinou, J.C., Westermann, B., Rugarli, E.I., Langer, T., Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell Biol. 187 (2009), 1023–1036.
18. Ferreirinha, F., Quattrini, A., Pirozzi, M., Valsecchi, V., Dina, G., Broccoli, V., Auricchio, A., Piemonte, F., Tozzi, G., Gaeta, L., et al. Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. J. Clin. Invest. 113 (2004), 231–242.
19. Giorgio, V., von Stockum, S., Antoniel, M., Fabbro, A., Fogolari, F., Forte, M., Glick, G.D., Petronilli, V., Zoratti, M., Szabó, I., et al. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc. Natl. Acad. Sci. USA 110 (2013), 5887–5892.
20. Heide, H., Bleier, L., Steger, M., Ackermann, J., Dröse, S., Schwamb, B., Zörnig, M., Reichert, A.S., Koch, I., Wittig, I., Brandt, U., Complexome profiling identifies TMEM126B as a component of the mitochondrial complex I assembly complex. Cell Metab. 16 (2012), 538–549.
21. Kamer, K.J., Mootha, V.K., The molecular era of the mitochondrial calcium uniporter. Nat. Rev. Mol. Cell Biol. 16 (2015), 545–553.
22. Kasumu, A., Bezprozvanny, I., Deranged calcium signaling in Purkinje cells and pathogenesis in spinocerebellar ataxia 2 (SCA2) and other ataxias. Cerebellum 11 (2012), 630–639.
23. 2 causes mitochondrial transport defects and tau hyperphosphorylation. EMBO J. 33 (2014), 1011–1026.
24. Koppen, M., Metodiev, M.D., Casari, G., Rugarli, E.I., Langer, T., Variable and tissue-specific subunit composition of mitochondrial m-AAA protease complexes linked to hereditary spastic paraplegia. Mol. Cell. Biol. 27 (2007), 758–767.
25. Kovács-Bogdán, E., Sancak, Y., Kamer, K.J., Plovanich, M., Jambhekar, A., Huber, R.J., Myre, M.A., Blower, M.D., Mootha, V.K., Reconstitution of the mitochondrial calcium uniporter in yeast. Proc. Natl. Acad. Sci. USA 111 (2014), 8985–8990.
26. Liu, J.C., Liu, J., Holmström, K.M., Menazza, S., Parks, R.J., Fergusson, M.M., Yu, Z.X., Springer, D.A., Halsey, C., Liu, C., et al. MICU1 serves as a molecular gatekeeper to prevent in vivo mitochondrial calcium overload. Cell Rep. 16 (2016), 1561–1573.
27. Logan, C.V., Szabadkai, G., Sharpe, J.A., Parry, D.A., Torelli, S., Childs, A.M., Kriek, M., Phadke, R., Johnson, C.A., Roberts, N.Y., et al., UK10K Consortium. Loss-of-function mutations in MICU1 cause a brain and muscle disorder linked to primary alterations in mitochondrial calcium signaling. Nat. Genet. 46 (2014), 188–193.
28. Mallilankaraman, K., Doonan, P., Cárdenas, C., Chandramoorthy, H.C., Müller, M., Miller, R., Hoffman, N.E., Gandhirajan, R.K., Molgó, J., Birnbaum, M.J., et al. MICU1 is an essential gatekeeper for MCU-mediated mitochondrial Ca(2+) uptake that regulates cell survival. Cell 151 (2012), 630–644.
29. Maltecca, F., Magnoni, R., Cerri, F., Cox, G.A., Quattrini, A., Casari, G., Haploinsufficiency of AFG3L2, the gene responsible for spinocerebellar ataxia type 28, causes mitochondria-mediated Purkinje cell dark degeneration. J. Neurosci. 29 (2009), 9244–9254.
30. Maltecca, F., Baseggio, E., Consolato, F., Mazza, D., Podini, P., Young, S.M. Jr., Drago, I., Bahr, B.A., Puliti, A., Codazzi, F., et al. Purkinje neuron Ca2+ influx reduction rescues ataxia in SCA28 model. J. Clin. Invest. 125 (2015), 263–274.
31. Merkwirth, C., Dargazanli, S., Tatsuta, T., Geimer, S., Löwer, B., Wunderlich, F.T., von Kleist-Retzow, J.C., Waisman, A., Westermann, B., Langer, T., Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev. 22 (2008), 476–488.
32. Minichiello, L., Korte, M., Wolfer, D., Kühn, R., Unsicker, K., Cestari, V., Rossi-Arnaud, C., Lipp, H.P., Bonhoeffer, T., Klein, R., Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24 (1999), 401–414.
33. Nolden, M., Ehses, S., Koppen, M., Bernacchia, A., Rugarli, E.I., Langer, T., The m-AAA protease defective in hereditary spastic paraplegia controls ribosome assembly in mitochondria. Cell 123 (2005), 277–289.
34. Pan, X., Liu, J., Nguyen, T., Liu, C., Sun, J., Teng, Y., Fergusson, M.M., Rovira, I.I., Allen, M., Springer, D.A., et al. The physiological role of mitochondrial calcium revealed by mice lacking the mitochondrial calcium uniporter. Nat. Cell Biol. 15 (2013), 1464–1472.
35. Patron, M., Checchetto, V., Raffaello, A., Teardo, E., Vecellio Reane, D., Mantoan, M., Granatiero, V., Szabò, I., De Stefani, D., Rizzuto, R., MICU1 and MICU2 finely tune the mitochondrial Ca2+ uniporter by exerting opposite effects on MCU activity. Mol. Cell 53 (2014), 726–737.
36. Petrungaro, C., Zimmermann, K.M., Küttner, V., Fischer, M., Dengjel, J., Bogeski, I., Riemer, J., The Ca(2+)-dependent release of the Mia40-induced MICU1-MICU2 dimer from MCU regulates mitochondrial Ca(2+) uptake. Cell Metab. 22 (2015), 721–733.
37. Pierson, T.M., Adams, D., Bonn, F., Martinelli, P., Cherukuri, P.F., Teer, J.K., Hansen, N.F., Cruz, P., Mullikin For The Nisc Comparative Sequencing Program, J.C., Blakesley, R.W., et al. Whole-exome sequencing identifies homozygous AFG3L2 mutations in a spastic ataxia-neuropathy syndrome linked to mitochondrial m-AAA proteases. PLoS Genet., 7, 2011, e1002325.
38. Plovanich, M., Bogorad, R.L., Sancak, Y., Kamer, K.J., Strittmatter, L., Li, A.A., Girgis, H.S., Kuchimanchi, S., De Groot, J., Speciner, L., et al. MICU2, a paralog of MICU1, resides within the mitochondrial uniporter complex to regulate calcium handling. PLoS ONE, 8, 2013, e55785.
39. Preuss, M., Leonhard, K., Hell, K., Stuart, R.A., Neupert, W., Herrmann, J.M., Mba1, a novel component of the mitochondrial protein export machinery of the yeast Saccharomyces cerevisiae. J. Cell Biol. 153 (2001), 1085–1096.
40. Qiu, J., Tan, Y.W., Hagenston, A.M., Martel, M.A., Kneisel, N., Skehel, P.A., Wyllie, D.J., Bading, H., Hardingham, G.E., Mitochondrial calcium uniporter Mcu controls excitotoxicity and is transcriptionally repressed by neuroprotective nuclear calcium signals. Nat. Commun., 4, 2013, 2034.
41. Quirós, P.M., Langer, T., López-Otín, C., New roles for mitochondrial proteases in health, ageing and disease. Nat. Rev. Mol. Cell Biol. 16 (2015), 345–359.
42. Richter-Dennerlein, R., Korwitz, A., Haag, M., Tatsuta, T., Dargazanli, S., Baker, M., Decker, T., Lamkemeyer, T., Rugarli, E.I., Langer, T., DNAJC19, a mitochondrial cochaperone associated with cardiomyopathy, forms a complex with prohibitins to regulate cardiolipin remodeling. Cell Metab. 20 (2014), 158–171.
43. Sancak, Y., Markhard, A.L., Kitami, T., Kovács-Bogdán, E., Kamer, K.J., Udeshi, N.D., Carr, S.A., Chaudhuri, D., Clapham, D.E., Li, A.A., et al. EMRE is an essential component of the mitochondrial calcium uniporter complex. Science 342 (2013), 1379–1382.
44. Shanmughapriya, S., Rajan, S., Hoffman, N.E., Higgins, A.M., Tomar, D., Nemani, N., Hines, K.J., Smith, D.J., Eguchi, A., Vallem, S., et al. SPG7 is an essential and conserved component of the mitochondrial permeability transition pore. Mol. Cell 60 (2015), 47–62.
45. Tsai, M.F., Phillips, C.B., Ranaghan, M., Tsai, C.W., Wu, Y., Willliams, C., Miller, C., Dual functions of a small regulatory subunit in the mitochondrial calcium uniporter complex. eLife, 5, 2016, 5.
46. Yamamoto, T., Yamagoshi, R., Harada, K., Kawano, M., Minami, N., Ido, Y., Kuwahara, K., Fujita, A., Ozono, M., Watanabe, A., et al. Analysis of the structure and function of EMRE in a yeast expression system. Biochim. Biophys. Acta 1857 (2016), 831–839.