Mitochondrial matrix proteostasis is linked to hereditary paraganglioma: LON-mediated turnover of the human flavinylation factor SDH5 is regulated by its interaction with SDHA

FASEB Journal

Volumn 28, Issue 4, 2014, Pages 1794-1804

  Bezawork Geleta, Ayenachew ^a,b   Saiyed, Tamanna ^a   Dougan, David A ^a   Truscott, Kaye N ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

Author keywords

Assembly factor; Organelle; Protein degradation; Succinate dehydrogenase

Indexed keywords

GLUTARALDEHYDE; MITOCHONDRIAL LON; MITOCHONDRIAL PROTEIN; OXIDOREDUCTASE; SUCCINATE DEHYDROGENASE 5; SUCCINATE DEHYDROGENASE SUBUNIT A; UNCLASSIFIED DRUG;

ARTICLE; FEMALE; FLAVINYLATION; GENE MUTATION; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MITOCHONDRION; PARAGANGLIOMA; PLASMID; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN HOMEOSTASIS; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; TURNOVER TIME;

AAA+ PROTEASE; ASSEMBLY FACTOR; ORGANELLE; PROTEIN DEGRADATION; SUCCINATE DEHYDROGENASE;

ELECTRON TRANSPORT COMPLEX II; ENZYME STABILITY; FLAVIN-ADENINE DINUCLEOTIDE; HELA CELLS; HUMANS; IMMUNOBLOTTING; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PARAGANGLIOMA; PROTEASE LA; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEOSTASIS DEFICIENCIES; SUBSTRATE SPECIFICITY;

EID: 84901044652     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-242420     Document Type: Article

References (37)

1. Hoekstra, A. S., and Bayley, J. P. (2013) The role of complex II in disease. Biochim. Biophys. Acta 1827, 543-551
2. Sun, F., Huo, X., Zhai, Y., Wang, A., Xu, J., Su, D., Bartlam, M., and Rao, Z. (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121, 1043-1057
3. Astuti, D., Latif, F., Dallol, A., Dahia, P. L., Douglas, F., George, E., Skoldberg, F., Husebye, E. S., Eng, C., and Maher, E. R. (2001) Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am. J. Hum. Gen. 69, 49-54
4. Baysal, B. E., Ferrell, R. E., Willett-Brozick, J. E., Lawrence, E. C., Myssiorek, D., Bosch, A., van der Mey, A., Taschner, P. E., Rubinstein, W. S., Myers, E. N., Richard, C. W., 3rd, Cornelisse, C. J., Devilee, P., and Devlin, B. (2000) Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287, 848-851
5. Burnichon, N., Briere, J. J., Libe, R., Vescovo, L., Riviere, J., Tissier, F., Jouanno, E., Jeunemaitre, X., Benit, P., Tzagoloff, A., Rustin, P., Bertherat, J., Favier, J., and Gimenez-Roqueplo, A. P. (2010) SDHA is a tumor suppressor gene causing paraganglioma. Hum. Mol. Genet. 19, 3011-3020
6. Niemann, S., and Muller, U. (2000) Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat. Genet. 26, 268-270
7. Hao, H. X., Khalimonchuk, O., Schraders, M., Dephoure, N., Bayley, J. P., Kunst, H., Devilee, P., Cremers, C. W., Schiffman, J. D., Bentz, B. G., Gygi, S. P., Winge, D. R., Kremer, H., and Rutter, J. (2009) SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 325, 1139-1142
8. Chacinska, A., Koehler, C. M., Milenkovic, D., Lithgow, T., and Pfanner, N. (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138, 628-644
9. Mossmann, D., Meisinger, C., and Vogtle, F. N. (2012) Processing of mitochondrial presequences. Biochim. Biophys. Acta 1819, 1098-1106
10. Voos, W., Ward, L. A., and Truscott, K. N. (2013) The role of AAA-proteases in mitochondrial protein biogenesis, homeostasis and activity control. Subcell. Biochem. 66, 223-263
11. Truscott, K. N., Lowth, B. R., Strack, P. R., and Dougan, D. A. (2010) Diverse functions of mitochondrial AAA-proteins: protein activation, disaggregation, and degradation. Biochem. Cell Biol. 88, 97-108
12. Kang, S. G., Ortega, J., Singh, S. K., Wang, N., Huang, N. N., Steven, A. C., and Maurizi, M. R. (2002) Functional proteolytic complexes of the human mitochondrial ATP-dependent protease, hClpXP. J. Biol. Chem. 277, 21095-21102
13. Zhao, Q., Wang, J., Levichkin, I. V., Stasinopoulos, S., Ryan, M. T., and Hoogenraad, N. J. (2002) A mitochondrial specific stress response in mammalian cells. EMBO J. 21, 4411-4419
14. Bota, D. A., and Davies, K. J. (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol. 4, 674-680
15. Fukuda, R., Zhang, H., Kim, J. W., Shimoda, L., Dang, C. V., and Semenza, G. L. (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129, 111-122
16. Granot, Z., Kobiler, O., Melamed-Book, N., Eimerl, S., Bahat, A., Lu, B., Braun, S., Maurizi, M. R., Suzuki, C. K., Oppenheim, A. B., and Orly, J. (2007) Turnover of mitochondrial steroidogenic acute regulatory (StAR) protein by Lon protease: the unexpected effect of proteasome inhibitors. Mol. Endocrinol. 21, 2164-2177
17. Lu, B., Lee, J., Nie, X., Li, M., Morozov, Y. I., Venkatesh, S., Bogenhagen, D. F., Temiakov, D., and Suzuki, C. K. (2013) Phosphorylation of human TFAM in mitochondria impairs DNA binding and promotes degradation by the AAA-Lon protease. Mol. Cell 49, 121-132
18. Tian, Q., Li, T., Hou, W., Zheng, J., Schrum, L. W., and Bonkovsky, H. L. (2011) Lon peptidase 1 (LONP1)-dependent breakdown of mitochondrial 5-aminolevulinic acid synthase protein by heme in human liver cells. J. Biol. Chem. 286, 26424-26430
19. Lennon, G., Auffray, C., Polymeropoulos, M., and Soares, M. B. (1996) The I.M.A.G.E. Consortium: an integrated molecular analysis of genomes and their expression. Genomics 33, 151-152
20. Catanzariti, A. M., Soboleva, T. A., Jans, D. A., Board, P. G., and Baker, R. T. (2004) An efficient system for high-level expression and easy purification of authentic recombinant proteins. Prot. Sci. 13, 1331-1339
21. Truscott, K. N., Kovermann, P., Geissler, A., Merlin, A., Meijer, M., Driessen, A. J., Rassow, J., Pfanner, N., and Wagner, R. (2001) A presequence-and voltage-sensitive channel of the mitochondrial preprotein translocase formed by Tim23. Nat. Struct. Biol. 8, 1074-1082
22. Zheng, L., Baumann, U., and Reymond, J. L. (2004) An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 32, e115
23. Ninnis, R. L., Spall, S. K., Talbo, G. H., Truscott, K. N., and Dougan, D. A. (2009) Modification of PATase by L/F-transferase generates a ClpS-dependent N-end rule substrate in Escherichia coli. EMBO J. 28, 1732-1744
24. Lowth, B. R., Kirstein-Miles, J., Saiyed, T., Brotz-Oesterhelt, H., Morimoto, R. I., Truscott, K. N., and Dougan, D. A. (2012) Substrate recognition and processing by a Walker B mutant of the human mitochondrial AAA-protein CLPX. J. Struct. Biol. 179, 193-201
25. Johnston, A. J., Hoogenraad, J., Dougan, D. A., Truscott, K. N., Yano, M., Mori, M., Hoogenraad, N. J., and Ryan, M. T. (2002) Insertion and assembly of human tom7 into the preprotein translocase complex of the outer mitochondrial membrane. J. Biol. Chem. 277, 42197-42204
26. Stojanovski, D., Pfanner, N., and Wiedemann, N. (2007) Import of proteins into mitochondria. Methods Cell Biol. 80, 783-806
27. Tatsuta, T., and Langer, T. (2007) Studying proteolysis within mitochondria. Methods Mol. Biol. 372, 343-360
28. Schagger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379
29. Schagger, H., and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199, 223-231
30. Claros, M. G., and Vincens, P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241, 779-786
31. Gur, E., Ottofueling, R., and Dougan, D. A. (2013) Machines of destruction -AAA-proteases and the adaptors that control them. Subcell. Biochem. 66, 3-33
32. Gakh, O., Cavadini, P., and Isaya, G. (2002) Mitochondrial processing peptidases. Biochim. Biophys. Acta 1592, 63-77
33. Vogtle, F. N., Wortelkamp, S., Zahedi, R. P., Becker, D., Leidhold, C., Gevaert, K., Kellermann, J., Voos, W., Sickmann, A., Pfanner, N., and Meisinger, C. (2009) Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 139, 428-439
34. Lim, K., Doseeva, V., Demirkan, E. S., Pullalarevu, S., Krajewski, W., Galkin, A., Howard, A., and Herzberg, O. (2005) Crystal structure of the YgfY from Escherichia coli, a protein that may be involved in transcriptional regulation. Proteins 58, 759-763
35. Eletsky, A., Jeong, M. Y., Kim, H., Lee, H. W., Xiao, R., Pagliarini, D. J., Prestegard, J. H., Winge, D. R., Montelione, G. T., and Szyperski, T. (2012) Solution NMR structure of yeast succinate dehydrogenase flavinylation factor Sdh5 reveals a putative Sdh1 binding site. Biochemistry 51, 8475-8477
36. Rutter, J., Winge, D. R., and Schiffman, J. D. (2010) Succinate dehydrogenase -Assembly, regulation and role in human disease. Mitochondrion 10, 393-401
37. Yamaguchi, Y., Park, J. H., and Inouye, M. (2011) Toxinantitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45, 61-79