SPG7 Is an Essential and Conserved Component of the Mitochondrial Permeability Transition Pore

Molecular Cell

Volumn 60, Issue 1, 2015, Pages 47-62

  Shanmughapriya, Santhanam ^a   Rajan, Sudarsan ^a   Hoffman, Nicholas E ^a   Higgins, Andrew M ^a   Tomar, Dhanendra ^a   Nemani, Neeharika ^a   Hines, Kevin J ^a   Smith, Dylan J ^a   Eguchi, Akito ^a   Vallem, Sandhya ^a   Shaikh, Farah ^a   Cheung, Maggie ^a   Leonard, Nicole J ^a   Stolakis, Ryan S ^a   Wolfers, Matthew P ^a   Ibetti, Jessica ^a   Chuprun, J Kurt ^a   Jog, Neelakshi R ^a   Houser, Steven R ^a   Koch, Walter J ^a   Elrod, John W ^a   Madesh, Muniswamy ^a   more..

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLOPHILIN D; CYTOCHROME C; MESSENGER RNA; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REACTIVE OXYGEN METABOLITE; SEPHAROSE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; SPASTIC PARAPLEGIA 7; TETRAMETHYLRHODAMINE ETHYL ESTER; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1; CALCIUM; CYCLOPHILIN; METALLOPROTEINASE; PPID PROTEIN, HUMAN; SPG7 PROTEIN, HUMAN; VDAC1 PROTEIN, HUMAN;

ARTICLE; BIOCHEMICAL ANALYSIS; CELL DEATH; CELL PERMEABILIZATION; FEMALE; GENE DISRUPTION; GENE MAPPING; GENE SILENCING; HUMAN; HUMAN CELL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; BINDING SITE; CHEMISTRY; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION;

BINDING SITES; CALCIUM; CELL DEATH; CYCLOPHILINS; HEK293 CELLS; HELA CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; METALLOENDOPEPTIDASES; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 84952871175     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.08.009     Document Type: Article

References (46)

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. An uncoupling channel within the c-subunit ring of the F1FO ATP synthase is the mitochondrial permeability transition pore. Proc. Natl. Acad. Sci. USA 2014, 111:10580-10585.
2. Anflous K., Armstrong D.D., Craigen W.J. Altered mitochondrial sensitivity for ADP and maintenance of creatine-stimulated respiration in oxidative striated muscles from VDAC1-deficient mice. J. Biol. Chem. 2001, 276:1954-1960.
3. 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. 2003, 163:777-787.
4. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., Brunskill E.W., Sayen M.R., Gottlieb R.A., Dorn G.W., et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434:658-662.
5. Baines C.P., Kaiser R.A., Sheiko T., Craigen W.J., Molkentin J.D. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell Biol. 2007, 9:550-555.
6. Basso E., Fante L., Fowlkes J., Petronilli V., Forte M.A., Bernardi P. Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D. J. Biol. Chem. 2005, 280:18558-18561.
7. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev. 1999, 79:1127-1155.
8. Bonora M., Bononi A., De Marchi E., Giorgi C., Lebiedzinska M., Marchi S., Patergnani S., Rimessi A., Suski J.M., Wojtala A., et al. Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition. Cell Cycle 2013, 12:674-683.
9. 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 1998, 93:973-983.
10. Cereghetti G.M., Stangherlin A., Martins de Brito O., Chang C.R., Blackstone C., Bernardi P., Scorrano L. Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl. Acad. Sci. USA 2008, 105:15803-15808.
11. Cheng E.H., Sheiko T.V., Fisher J.K., Craigen W.J., Korsmeyer S.J. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 2003, 301:513-517.
12. Colombini M. VDAC structure, selectivity, and dynamics. Biochim. Biophys. Acta 2012, 1818:1457-1465.
13. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 1999, 341:233-249.
14. Duchen M.R. Mitochondria and calcium: from cell signalling to cell death. J. Physiol. 2000, 529:57-68.
15. Elrod J.W., Wong R., Mishra S., Vagnozzi R.J., Sakthievel B., Goonasekera S.A., Karch J., Gabel S., Farber J., Force T., et al. Cyclophilin D controls mitochondrial pore-dependent Ca(2+) exchange, metabolic flexibility, and propensity for heart failure in mice. J. Clin. Invest. 2010, 120:3680-3687.
16. 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. 2004, 113:231-242.
17. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 2001, 1:515-525.
18. 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 2013, 110:5887-5892.
19. Halestrap A.P. Mitochondrial calcium in health and disease. Biochim. Biophys. Acta 2009, 1787:1289-1290.
20. Halestrap A.P., Griffiths E.J., Connern C.P. Mitochondrial calcium handling and oxidative stress. Biochem. Soc. Trans. 1993, 21:353-358.
21. Hiller S., Garces R.G., Malia T.J., Orekhov V.Y., Colombini M., Wagner G. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 2008, 321:1206-1210.
22. Hoffman N.E., Chandramoorthy H.C., Shamugapriya S., Zhang X., Rajan S., Mallilankaraman K., Gandhirajan R.K., Vagnozzi R.J., Ferrer L.M., Sreekrishnanilayam K., et al. MICU1 motifs define mitochondrial calcium uniporter binding and activity. Cell Rep. 2013, 5:1576-1588.
23. Hung Y.P., Albeck J.G., Tantama M., Yellen G. Imaging cytosolic NADH-NAD(+) redox state with a genetically encoded fluorescent biosensor. Cell Metab. 2011, 14:545-554.
24. Ichas F., Jouaville L.S., Mazat J.P. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 1997, 89:1145-1153.
25. 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. 2007, 27:758-767.
26. Kroemer G., Galluzzi L., Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87:99-163.
27. Luvisetto S., Basso E., Petronilli V., Bernardi P., Forte M. Enhancement of anxiety, facilitation of avoidance behavior, and occurrence of adult-onset obesity in mice lacking mitochondrial cyclophilin D. Neuroscience 2008, 155:585-596.
28. Mallilankaraman K., Cárdenas C., Doonan P.J., Chandramoorthy H.C., Irrinki K.M., Golenár T., Csordás G., Madireddi P., Yang J., Müller M., et al. MCUR1 is an essential component of mitochondrial Ca2+ uptake that regulates cellular metabolism. Nat. Cell Biol. 2012, 14:1336-1343.
29. 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 2012, 151:630-644.
30. Mouri A., Noda Y., Shimizu S., Tsujimoto Y., Nabeshima T. The role of cyclophilin D in learning and memory. Hippocampus 2010, 20:293-304.
31. Nakagawa T., Shimizu S., Watanabe T., Yamaguchi O., Otsu K., Yamagata H., Inohara H., Kubo T., Tsujimoto Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005, 434:652-658.
32. Newmeyer D.D., Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003, 112:481-490.
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 2005, 123:277-289.
34. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
35. Park C.Y., Hoover P.J., Mullins F.M., Bachhawat P., Covington E.D., Raunser S., Walz T., Garcia K.C., Dolmetsch R.E., Lewis R.S. STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 2009, 136:876-890.
36. Riley W.W., Pfeiffer D.R. Relationships between Ca2+ release, Ca2+ cycling, and Ca2+-mediated permeability changes in mitochondria. J. Biol. Chem. 1985, 260:12416-12425.
37. Rugarli E.I., Langer T. Translating m-AAA protease function in mitochondria to hereditary spastic paraplegia. Trends Mol. Med. 2006, 12:262-269.
38. Schinzel A.C., Takeuchi O., Huang Z., Fisher J.K., Zhou Z., Rubens J., Hetz C., Danial N.N., Moskowitz M.A., Korsmeyer S.J. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc. Natl. Acad. Sci. USA 2005, 102:12005-12010.
39. Shanmughapriya S., Rajan S., Hoffman N.E., Zhang X., Guo S., Kolesar J.E., Hines K.J., Ragheb J., Jog N.R., Caricchio R., et al. Ca2+ signals regulate mitochondrial metabolism by stimulating CREB-mediated expression of the mitochondrial Ca2+ uniporter gene MCU. Sci. Signal. 2015, 8:ra23.
40. Smirnova E., Griparic L., Shurland D.L., van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 2001, 12:2245-2256.
41. Smith A.C., Blackshaw J.A., Robinson A.J. MitoMiner: a data warehouse for mitochondrial proteomics data. Nucleic Acids Res. 2012, 40:D1160-D1167.
42. Tait S.W., Green D.R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 2010, 11:621-632.
43. Tanveer A., Virji S., Andreeva L., Totty N.F., Hsuan J.J., Ward J.M., Crompton M. Involvement of cyclophilin D in the activation of a mitochondrial pore by Ca2+ and oxidant stress. Eur. J. Biochem. 1996, 238:166-172.
44. Vaseva A.V., Marchenko N.D., Ji K., Tsirka S.E., Holzmann S., Moll U.M. p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 2012, 149:1536-1548.
45. Weeber E.J., Levy M., Sampson M.J., Anflous K., Armstrong D.L., Brown S.E., Sweatt J.D., Craigen W.J. The role of mitochondrial porins and the permeability transition pore in learning and synaptic plasticity. J. Biol. Chem. 2002, 277:18891-18897.
46. Williams G.S., Boyman L., Chikando A.C., Khairallah R.J., Lederer W.J. Mitochondrial calcium uptake. Proc. Natl. Acad. Sci. USA 2013, 110:10479-10486.