MidA is a putative methyltransferase that is required for mitochondrial complex I function

Journal of Cell Science

Volumn 123, Issue 10, 2010, Pages 1674-1683

  Carilla Latorre, Sergio ^a   Gallardo, M Esther ^a,b   Annesley, Sarah J ^c   Calvo Garrido, Javier ^a   Graña, Osvaldo ^d   Accari, Sandra L ^c   Smith, Paige K ^c   Valencia, Alfonso ^d   Garesse, Rafael ^a,b   Fisher, Paul R ^c   Escalante, Ricardo ^a  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c LA TROBE UNIVERSITY   (Australia)

^d Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

C2orf56; Complex I; Dictyostelium; DUF185; LOC55471; MidA; PRO1853

Indexed keywords

METHYLTRANSFERASE; MITOCHONDRIAL PROTEIN; PROTEIN MIDA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG; AMP-ACTIVATED PROTEIN KINASE KINASE; MIDA PROTEIN, HUMAN; NDUFS2 PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN KINASE; PROTOZOAL PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SMALL INTERFERING RNA;

ARTICLE; BIOINFORMATICS; CATALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOPATHOLOGY; DICTYOSTELIUM; HUMAN; HUMAN CELL; NONHUMAN; PHENOTYPE; PHOTOTAXIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TWO HYBRID SYSTEM; YEAST; BIOLOGY; CELL MOTION; ENZYME ACTIVE SITE; GENETICS; METABOLISM; MITOCHONDRION; MUTATION;

CATALYTIC DOMAIN; CELL MOVEMENT; COMPUTATIONAL BIOLOGY; DICTYOSTELIUM; ELECTRON TRANSPORT COMPLEX I; HUMANS; METHYLTRANSFERASES; MITOCHONDRIA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NADH DEHYDROGENASE; PROTEIN BINDING; PROTEIN KINASES; PROTOZOAN PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

DICTYOSTELIUM;

EID: 77952349219     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.066076     Document Type: Article

References (65)

1. Agrimi, G., Di Noia, M. A., Marobbio, C. M., Fiermonte, G., Lasorsa, F. M. and Palmieri, F. (2004). Identification of the human mitochondrial S-adenosylmethionine transporter: bacterial expression, reconstitution, functional characterization and tissue distribution. Biochem. J. 379, 183-190. (Pubitemid 38491373)
2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
3. Andreeva, A., Howorth, D., Chandonia, J. M., Brenner, S. E., Hubbard, T. J., Chothia, C. and Murzin, A. G. (2008). Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res. 36, D419-D425.
4. Annesley, S. J. and Fisher, P. R. (2009a). Dictyostelium discoideum-a model for many reasons. Mol. Cell Biochem. 329, 73-91.
5. Annesley, S. J. and Fisher, P. R. (2009b). Dictyostelium slug phototaxis. Methods Mol. Biol. 571, 67-76.
6. Barth, C., Greferath, U., Kotsifas, M., Tanaka, Y., Alexander, S., Alexander, H. and Fisher, P. R. (2001). Transcript mapping and processing of mitochondrial RNA in Dictyostelium discoideum. Curr. Genet. 39, 355-364.
7. Barth, C., Le P. and Fisher, P. R. (2007). Mitochondrial biology and disease in Dictyostelium. Int. Rev. Cytol. 263, 207-252.
8. Bokko, P. B., Francione, L., Bandala-Sanchez, E., Ahmed, A. U., Annesley, S. J., Huang, X., Khurana, T., Kimmel, A. R. and Fisher, P. R. (2007). Diverse cytopathologies in mitochondrial disease are caused by AMP-activated protein kinase signaling. Mol. Biol. Cell 18, 1874-1886. (Pubitemid 46717567)
9. Bych, K., Kerscher, S., Netz, D. J., Pierik, A. J., Zwicker, K., Huynen, M. A., Lill, R., Brandt, U. and Balk, J. (2008). The iron-sulphur protein Ind1 is required for effective complex I assembly. EMBO J. 27, 1736-1746.
10. Calvaruso, M. A., Smeitink, J. and Nijtmans, L. (2008). Electrophoresis techniques to investigate defects in oxidative phosphorylation. Methods 46, 281-287.
11. Carroll, J., Fearnley, I. M., Skehel, J. M., Runswick, M. J., Shannon, R. J., Hirst, J. and Walker, J. E. (2005). The post-translational modifications of the nuclear encoded subunits of complex I from bovine heart mitochondria. Mol. Cell Proteomics 4, 693-699.
12. Chida, J., Yamaguchi, H., Amagai, A. and Maeda, Y. (2004). The necessity of mitochondrial genome DNA for normal development of Dictyostelium cells. J. Cell Sci. 117, 3141-3152.
13. Darcy, P. K., Wilczynska, Z. and Fisher, P. R. (1994). Genetic analysis of Dictyostelium slug phototaxis mutants. Genetics 137, 977-985.
14. Debray, F. G., Lambert, M. and Mitchell, G. A. (2008). Disorders of mitochondrial function. Curr. Opin. Pediatr. 20, 471-482.
15. DiMauro, S. and Schon, E. A. (2008). Mitochondrial disorders in the nervous system. Annu. Rev. Neurosci. 31, 91-123.
16. Eichinger, L., Pachebat, J. A., Glockner, G., Rajandream, M. A., Sucgang, R., Berriman, M., Song, J., Olsen, R., Szafranski, K., Xu, Q. et al. (2005). The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43-57. (Pubitemid 40655903)
17. Escalante, R. and Vicente, J. J. (2000). Dictyostelium discoideum: a model system for differentiation and patterning. Int. J. Dev. Biol. 44, 819-835.
18. Fearnley, I. M., Carroll, J. and Walker, J. E. (2007). Proteomic analysis of the subunit composition of complex I (NADH:ubiquinone oxidoreductase) from bovine heart mitochondria. Methods. Mol. Biol. 357, 103-125.
19. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H. R., Ceric, G., Forslund, K., Eddy, S. R., Sonnhammer, E. L. et al. (2008). The Pfam protein families database. Nucleic Acids Res. 36, D281-D288.
20. Fisher, P. R., Smith, E. and Williams, K. L. (1981). An extracellular chemical signal controlling phototactic behavior by D. discoideum slugs. Cell 23, 799-807.
21. Gerards, M., Sluiter, W., van den Bosch, B. J., de Wit, E., Calis, C. M., Frentzen, M., Akbari, H., Schoonderwoerd, K., Scholte, H. R., Jongbloed, R. J. et al. (2009). Defective complex I assembly due to C20orf7 mutations as a new cause of Leigh syndrome. J. Med. Genet. PMID: 19452079.
22. Helm, M., Brule, H., Degoul, F., Cepanec, C., Leroux, J. P., Giege, R. and Florentz, C. (1998). The presence of modified nucleotides is required for cloverleaf folding of a human mitochondrial tRNA. Nucleic Acids Res. 26, 1636-1643.
23. Hoefs, S. J., Dieteren, C. E., Rodenburg, R. J., Naess, K., Bruhn, H., Wibom, R., Wagena, E., Willems, P. H., Smeitink, J. A., Nijtmans, L. G. et al. (2009). Baculovirus complementation restores a novel NDUFAF2 mutation causing complex I deficiency. Hum. Mutat. 30, E728-E736.
24. Janssen, R. J., Nijtmans, L. G., van den Heuvel, L. P. and Smeitink, J. A. (2006). Mitochondrial complex I: structure, function and pathology. J. Inherit. Metab. Dis. 29, 499-515. (Pubitemid 44193264)
25. Kagan, R. M. and Clarke, S. (1994). Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. Arch. Biochem. Biophys. 310, 417-427. (Pubitemid 2070415)
26. Kakebeeke, P. I. J., de Wit, R. J. W., Kohtz, S. D. and Konijn, T. M. (1979). Negative chemotaxis in Dictyostelium and Polysphondylium. Exp. Cell Res. 124, 429-433.
27. Kelley, L. A. and Sternberg, M. J. (2009). Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371.
28. Kirchmair, J., Markt, P., Distinto, S., Schuster, D., Spitzer, G. M., Liedl, K. R., Langer, T. and Wolber, G. (2008). The Protein Data Bank (PDB), its related services and software tools as key components for in silico guided drug discovery. J. Med. Chem. 51, 7021-7040.
29. Klein, G. and Satre, M. (1986). Kinetics of fluid-phase pinocytosis in Dictyostelium discoideum amoebae. Biochem. Biophys. Res. Commun. 138, 1146-1152.
30. Koopman, W. J., Nijtmans, L. G., Dieteren, C. E., Roestenberg, P., Valsecchi, F., Smeitink, J. A. and Willems, P. H. (2010). Mammalian mitochondrial complex I: biogenesis, regulation and reactive oxygen species generation. Antioxid. Redox Signal. PMID: 19803744.
31. Kotsifas, M., Barth, C., De Lozanne, A., Lay, S. T. and Fisher, P. R. (2002). Chaperonin 60 and mitochondrial disease in Dictyostelium. J. Muscle Res. Cell Motil. 23, 839-852.
32. Lazarou, M., Thorburn, D. R., Ryan, M. T. and McKenzie, M. (2009). Assembly of mitochondrial complex I and defects in disease. Biochim. Biophys. Acta. 1793, 78-88.
33. Loeffen, J., Elpeleg, O., Smeitink, J., Smeets, R., Stockler-Ipsiroglu, S., Mandel, H., Sengers, R., Trijbels, F. and van den Heuvel, L. (2001). Mutations in the complex I NDUFS2 gene of patients with cardiomyopathy and encephalomyopathy. Ann. Neurol. 49, 195-201.
34. Loenen, W. A. (2006). S-adenosylmethionine: jack of all trades and master of everything? Biochem. Soc. Trans. 34, 330-333.
35. Lopez, G., Valencia, A. and Tress, M. L. (2007). firestar-prediction of functionally important residues using structural templates and alignment reliability. Nucleic Acids Res. 35, W573-W577.
36. Martin, J. L. and McMillan, F. M. (2002). SAM (dependent) I AM: the S-adenosylmethionine-dependent methyltransferase fold. Curr. Opin. Struct. Biol. 12, 783-793.
37. Maselli, A., Laevsky, G. and Knecht, D. A. (2002). Kinetics of binding, uptake and degradation of live fluorescent (DsRed) bacteria by Dictyostelium discoideum. Microbiology 148, 413-420.
38. Niewmierzycka, A. and Clarke, S. (1999). S-Adenosylmethionine-dependent methylation in Saccharomyces cerevisiae. Identification of a novel protein arginine methyltransferase. J. Biol. Chem. 274, 814-824. (Pubitemid 129535240)
39. Ogawa, S., Yoshino, R., Angata, K., Iwamoto, M., Pi, M., Kuroe, K., Matsuo, K., Morio, T., Urushihara, H., Yanagisawa, K. et al. (2000). The mitochondrial DNA of Dictyostelium discoideum: complete sequence, gene content and genome organization. Mol. Gen. Genet. 263, 514-519.
40. Ogilvie, I., Kennaway, N. G. and Shoubridge, E. A. (2005). A molecular chaperone for mitochondrial complex I assembly is mutated in a progressive encephalopathy. J. Clin. Invest. 115, 2784-2792.
41. 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. (2008). A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123.
42. Pang, K. M., Lynes, M. A. and Knecht, D. A. (1999). Variables controlling the expression level of exogenous genes in Dictyostelium. Plasmid 41, 187-197.
43. Pathak, R. U. and Davey, G. P. (2008). Complex I and energy thresholds in the brain. Biochim. Biophys. Acta 1777, 777-782.
44. Pintard, L., Bujnicki, J. M., Lapeyre, B. and Bonnerot, C. (2002). MRM2 encodes a novel yeast mitochondrial 21S rRNA methyltransferase. EMBO J. 21, 1139-1147.
45. Porter, C. T., Bartlett, G. J. and Thornton, J. M. (2004). The Catalytic Site Atlas: a resource of catalytic sites and residues identified in enzymes using structural data. Nucleic Acids Res. 32, D129-D133.
46. Rain, J. C., Selig, L., De Reuse, H., Battaglia, V., Reverdy, C., Simon, S., Lenzen, G., Petel, F., Wojcik, J., Schachter, V. et al. (2001). The protein-protein interaction map of Helicobacter pylori. Nature 409, 211-215. (Pubitemid 32144288)
47. Remacle, C., Barbieri, M. R., Cardol, P. and Hamel, P. P. (2008). Eukaryotic complex I: functional diversity and experimental systems to unravel the assembly process. Mol. Genet. Genomics 280, 93-110.
48. Saada, A., Vogel, R. O., Hoefs, S. J., van den Brand, M. A., Wessels, H. J., Willems, P. H., Venselaar, H., Shaag, A., Barghuti, F., Reish, O. et al. (2009). Mutations in NDUFAF3 (C3ORF60), encoding an NDUFAF4 (C6ORF66)- interacting complex I assembly protein, cause fatal neonatal mitochondrial disease. Am. J. Hum. Genet. 84, 718-727.
49. Sadreyev, R. I., Baker, D. and Grishin, N. V. (2003). Profile-profile comparisons by COMPASS predict intricate homologies between protein families. Protein Sci. 12, 2262-2272.
50. Schubert, H. L., Blumenthal, R. M. and Cheng, X. (2003). Many paths to methyltransfer: a chronicle of convergence. Trends Biochem. Sci. 28, 329-335.
51. Shaulsky, G. and Loomis, W. F. (1993). Cell type regulation in response to expression of ricin-A in Dictyostelium. Dev. Biol. 160, 85-98.
52. Sugiana, C., Pagliarini, D. J., McKenzie, M., Kirby, D. M., Salemi, R., Abu-Amero, K. K., Dahl, H. H., Hutchison, W. M., Vascotto, K. A., Smith, S. M. et al. (2008). Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Am. J. Hum. Genet. 83, 468-478.
53. Sussman, M. (1987). Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Meth. Cell Biol. 28, 9-29.
54. Tiranti, V., Chariot, P., Carella, F., Toscano, A., Soliveri, P., Girlanda, P., Carrara, F., Fratta, G. M., Reid, F. M., Mariotti, C. et al. (1995). Maternally inherited hearing loss, ataxia and myoclonus associated with a novel point mutation in mitochondrial tRNASer(UCN) gene. Hum. Mol. Genet. 4, 1421-1427.
55. Torija, P., Robles, A. and Escalante, R. (2006a). Optimization of a large-scale gene disruption protocol in Dictyostelium and analysis of conserved genes of unknown function. BMC Microbiol. 6, 75.
56. Torija, P., Vicente, J. J., Rodrigues, T. B., Robles, A., Cerdan, S., Sastre, L., Calvo, R. M. and Escalante, R. (2006b). Functional genomics in Dictyostelium: MidA, a new conserved protein, is required for mitochondrial function and development. J. Cell Sci. 119, 1154-1164.
57. Ugalde, C., Janssen, R. J., van den Heuvel, L. P., Smeitink, J. A. and Nijtmans, L. G. (2004). Differences in assembly or stability of complex I and other mitochondrial OXPHOS complexes in inherited complex I deficiency. Hum. Mol. Genet. 13, 659-667.
58. Vahsen, N., Cande, C., Briere, J. J., Benit, P., Joza, N., Larochette, N., Mastroberardino, P. G., Pequignot, M. O., Casares, N., Lazar, V. et al. (2004). AIF deficiency compromises oxidative phosphorylation. EMBO J. 23, 4679-4689.
59. Vogel, R. O., Janssen, R. J., Ugalde, C., Grovenstein, M., Huijbens, R. J., Visch, H. J., van den Heuvel, L. P., Willems, P. H., Zeviani, M., Smeitink, J. A. et al. (2005). Human mitochondrial complex I assembly is mediated by NDUFAF1. FEBS J. 272, 5317-5326.
60. Vogel, R. O., Janssen, R. J., van den Brand, M. A., Dieteren, C. E., Verkaart, S., Koopman, W. J., Willems, P. H., Pluk, W., van den Heuvel, L. P., Smeitink, J. A. et al. (2007). Cytosolic signaling protein Ecsit also localizes to mitochondria where it interacts with chaperone NDUFAF1 and functions in complex I assembly. Genes Dev. 21, 615-624.
61. Wallace, A. C., Laskowski, R. A. and Thornton, J. M. (1995). LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Prot. Eng. 8, 127-134.
62. Wilczynska, Z., Barth, C. and Fisher, P. R. (1997). Mitochondrial mutations impair signal transduction in Dictyostelium discoideum slugs. Biochem. Biophys. Res. Commun. 234, 39-43. (Pubitemid 27267527)
63. Williams, R. S., Boeckeler, K., Graf, R., Muller-Taubenberger, A., Li, Z., Isberg, R. R., Wessels, D., Soll, D. R., Alexander, H. and Alexander, S. (2006). Towards a molecular understanding of human diseases using Dictyostelium discoideum. Trends Mol. Med. 12, 415-424.
64. Wu, C. C., MacCoss, M. J., Howell, K. E. and Yates, J. R., 3rd. (2003). A method for the comprehensive proteomic analysis of membrane proteins. Nat. Biotechnol. 21, 532-538. (Pubitemid 36532018)
65. Zemla, A. (2003). LGA: a method for finding 3D similarities in protein structures. Nucleic Acids Res. 31, 3370-3374.