NDUFAF7 methylates arginine 85 in the NDUFS2 subunit of human complex i

Journal of Biological Chemistry

Volumn 288, Issue 46, 2013, Pages 33016-33026

  Rhein, Virginie F ^a   Carroll, Joe ^a   Ding, Shujing ^a   Fearnley, Ian M ^a   Walker, John E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERMEMBRANE SPACE; IRON-SULFUR CLUSTERS; METHYLTRANSFERASES; MITOCHONDRIAL MATRIX; OXIDOREDUCTASES; PRIMARY ELECTRONS; PROTON-MOTIVE FORCES; TERMINAL ELECTRON ACCEPTORS;

ALKYLATION; AMINO ACIDS; MAMMALS; MITOCHONDRIA; PROTONS;

PROTEINS;

ARGININE; NITROGEN; PROTEIN METHYLTRANSFERASE; PROTEIN NDUFAF7; PROTEIN NDUFS2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REPRESSION; HUMAN; HUMAN CELL; MITOCHONDRION; MOLECULAR SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN PROTEIN INTERACTION;

ASSEMBLY; BIOENERGETICS; COMPLEX I; DIMETHYLARGININE; ELECTRON TRANSPORT; METHYLTRANSFERASE; MITOCHONDRIA; PROTEIN METHYLATION; RESPIRATORY CHAIN;

ARGININE; CELL LINE, TUMOR; HUMANS; METHYLATION; METHYLTRANSFERASES; NADH DEHYDROGENASE; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN-ARGININE N-METHYLTRANSFERASES;

EID: 84887844998     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.518803     Document Type: Article

References (84)

1. Carroll, J., Fearnley, I. M., Shannon, R. J., Hirst, J., and Walker, J. E. (2003) Analysis of the subunit composition of complex I from bovine heart mitochondria. Mol. Cell. Proteomics 2, 117-126
2. Carroll, J., Fearnley, I. M., Skehel, J. M., Shannon, R. J., Hirst, J., and Walker, J. E. (2006) Bovine complex I is a complex of 45 different subunits. J. Biol. Chem. 281, 32724-32727
3. Balsa, E., Marco, R., Perales-Clemente, E., Szklarczyk, R., Calvo, E., Landázuri, M. O., and Enríquez, J. A. (2012) NDUFA4 is a subunit of complex IV of the mammalian electron transport chain. Cell Metab. 16, 378-386
4. Grigorieff, N. (1998) Three-dimensional structure of bovine NADH:ubiquinone oxidoreductase (complex I) at 22 Å in ice. J. Mol. Biol. 277, 1033-1046
5. Angerer, H., Nasiri, H. R., Niedergesäß, V., Kerscher, S., Schwalbe, H., and Brandt, U. (2012) Tracing the tail of ubiquinone in mitochondrial complex I. Biochim. Biophys. Acta 1817, 1776-1784
6. Baradaran, R., Berrisford, J. M., Minhas, G. S., and Sazanov, L. A. (2013) Crystal structure of the entire respiratory complex I. Nature 494, 443-448
7. Wikström, M. (1984) Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett. 169, 300-304
8. Galkin, A. S., Grivennikova, V. G., and Vinogradov, A. D. (1999) H+/2e- stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles. FEBS Lett. 451, 157-161
9. Walker, J. E. (1992) The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains. Q. Rev. Biophys. 25, 253-324
10. Efremov, R. G., and Sazanov, L. A. (2011) Respiratory complex I. 'Steam engine' of the cell? Curr. Opin. Struct. Biol. 21, 532-540
11. Hirst, J., Carroll, J., Fearnley, I. M., Shannon, R. J., and Walker, J. E. (2003) The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim. Biophys. Acta 1604, 135-150
12. Scacco, S., Petruzzella, V., Budde, S., Vergari, R., Tamborra, R., Panelli, D., van den Heuvel, L. P., Smeitink, J. A., and Papa, S. (2003) Pathological mutations of the human NDUFS4 gene of the 18-kDa (AQDQ) subunit of complex I affect the expression of the protein and the assembly and function of the complex. J. Biol. Chem. 278, 44161-44167
13. Kirby, D. M., Salemi, R., Sugiana, C., Ohtake, A., Parry, L., Bell, K. M., Kirk, E. P., Boneh, A., Taylor, R. W., Dahl, H.-H. M., Ryan, M. T., and Thorburn, D. R. (2004) NDUFS6 mutations are a novel cause of lethal neonatal mitochondrial complex I deficiency. J. Clin. Invest. 114, 837-845
14. Hoefs, S. J., Dieteren, C. E., Distelmaier, F., Janssen, R. J., Epplen, A., Swarts, H. G., Forkink, M., Rodenburg, R. J., Nijtmans, L. G., Willems, P. H., Smeitink, J. A., and van den Heuvel, L. P. (2008) NDUFA2 complex I mutation leads to Leigh disease. Am. J. Hum. Genet. 82, 1306-1315
15. Hoefs, S. J., van Spronsen, F. J., Lenssen, E. W., Nijtmans, L. G., Rodenburg, R. J., Smeitink, J. A., and van den Heuvel, L. P. (2011) NDUFA10 mutations cause complex I deficiency in a patient with Leigh disease. Eur. J. Hum. Genet. 19, 270-274
16. Mimaki, M., Wang, X., McKenzie, M., Thorburn, D. R., and Ryan, M. T. (2012) Understanding mitochondrial complex I assembly in health and disease. Biochim. Biophys. Acta 1817, 851-862
17. Calvo, S. E., Compton, A. G., Hershman, S. G., Lim, S. C., Lieber, D. S., Tucker, E. J., Laskowski, A., Garone, C., Liu, S., Jaffe, D. B., Christodoulou, J., Fletcher, J. M., Bruno, D. L., Goldblatt, J., Dimauro, S., Thorburn, D. R., and Mootha, V. K. (2012) Molecular diagnosis of infantile mitochondrial disease with targeted next-generation sequencing. Sci. Transl. Med. 4, 118ra10
18. Haack, T. B., Madignier, F., Herzer, M., Lamantea, E., Danhauser, K., Invernizzi, F., Koch, J., Freitag, M., Drost, R., Hillier, I., Haberberger, B., Mayr, J. A., Ahting, U., Tiranti, V., Rötig, A., Iuso, A., Horvath, R., Tesarova, M., Baric, I., Uziel, G., Rolinski, B., Sperl, W., Meitinger, T., Zeviani, M., Freisinger, P., and Prokisch, H. (2012) Mutation screening of 75 candidate genes in 152 complex I deficiency cases identifies pathogenic variants in 16 genes including NDUFB9. J. Med. Genet. 49, 83-89
19. van den Bosch, B. J., Gerards, M., Sluiter, W., Stegmann, A. P., Jongen, E. L., Hellebrekers, D. M., Oegema, R., Lambrichs, E. H., Prokisch, H., Danhauser, K., Schoonderwoerd, K., de Coo, I. F., and Smeets, H. J. (2012) Defective NDUFA9 as a novel cause of neonatally fatal complex I disease. J. Med. Genet. 49, 10-15
20. 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
21. 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., and Nijtmans, L. G. (2005) Human mitochondrial complex I assembly is mediated by NDUFAF1. FEBS J. 272, 5317-5326
22. 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., and Nijtmans L. G. (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
23. 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., Shohat, M., Huynen, M. A., Smeitink, J. A., van den Heuvel, L. P., and Nijtmans, L. G. (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
24. Mckenzie, M., and Ryan, M. T. (2010) Assembly factors of human mitochondrial complex I and their defects in disease. IUBMB Life 62, 497-502
25. Nouws, J., Nijtmans, L., Houten, S. M., van den Brand, M., Huynen, M., Venselaar, H., Hoefs, S., Gloerich, J., Kronick, J., Hutchin, T., Willems, P., Rodenburg, R., Wanders, R., van den Heuvel, L., Smeitink, J., and Vogel, R. O. (2010) Acyl-CoA dehydrogenase 9 is required for the biogenesis of oxidative phosphorylation complex I. Cell Metab. 12, 283-294
26. 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., Hill, D. E., Vidal, M., Evans, J. G., Thorburn, D. R., Carr, S. A., and Mootha V. K. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123
27. 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., Newbold, R. F., Christodoulou, J., Calvo, S., Mootha, V. K., Ryan, M. T., and Thorburn, D. R. (2008) Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Am. J. Hum. Genet. 83, 468-478
28. Sheftel, A. D., Stehling, O., Pierik, A. J., Netz, D. J., Kerscher, S., Elsässer, H. P., Wittig, I., Balk, J., Brandt, U., and Lill, R. (2009) Human ind1, an iron-sulfur cluster assembly factor for respiratory complex I. Mol. Cell. Biol. 29, 6059-6073
29. Calvo, S. E., Tucker, E. J., Compton, A. G., Kirby, D. M., Crawford, G., Burtt, N. P., Rivas, M., Guiducci, C., Bruno, D. L., Goldberger, O. A., Redman, M. C., Wiltshire, E., Wilson, C. J., Altshuler, D., Gabriel, S. B., Daly, M. J., Thorburn, D. R., and Mootha, V. K. (2010) High-throughput, pooled sequencing identifies mutations in NUBPL and FOXRED1 in human complex I deficiency. Nat. Genet. 42, 851-858
30. Carilla-Latorre, S., Gallardo, M. E., Annesley, S. J., Calvo-Garrido, J., Graña, O., Accari, S. L., Smith, P. K., Valencia, A., Garesse, R., Fisher, P. R., and Escalante, R. (2010) MidA is a putative methyltransferase that is required for mitochondrial complex I function. J. Cell Sci. 123, 1674-1683
31. Heide, H., Bleier, L., Steger, M., Ackermann, J., Dröse, S., Schwamb, B., Zörnig, M., Reichert, A. S., Koch, I., Wittig, I., and Brandt, U. (2012) Complexome profiling identifies TMEM126B as a component of the mitochondrial complex I assembly complex. Cell Metab. 16, 538-549
32. Dunning, C. J., McKenzie, M., Sugiana, C., Lazarou, M., Silke, J., Connelly, A., Fletcher, J. M., Kirby, D. M., Thorburn, D. R., and Ryan M. T. (2007) Human CIA30 is involved in the early assembly of mitochondrial complex I and mutations in its gene cause disease. EMBO J. 26, 3227-3237
33. Saada, A., Edvardson, S., Rapoport, M., Shaag, A., Amry, K., Miller, C., Lorberboum-Galski, H., and Elpeleg, O. (2008) C6ORF66 is an assembly factor of mitochondrial complex I. Am. J. Hum. Genet. 82, 32-38
34. McKenzie, M., Tucker, E. J., Compton, A. G., Lazarou, M., George, C., Thorburn, D. R., and Ryan, M. T. (2011) Mutations in the gene encoding C8orf38 block complex I assembly by inhibiting production of the mitochondriaencoded subunit ND1. J. Mol. Biol. 414, 413-426
35. Rendón, O. Z., and Shoubridge, E. A. (2012) Early complex I assembly defects result in rapid turnover of the ND1 subunit. Hum. Mol. Genet. 21, 3815-3824
36. Petrossian, T. C., and Clarke, S. G. (2011) Uncovering the human methyltransferasome. Mol. Cell. Proteomics 10.1074/mcp.M110.000976
37. Carroll, J., Ding, S., Fearnley, I. M., and Walker, J. E. (2013) Posttransla-tional modifications near the quinone binding site of mammalian complex
38. I. J. Biol. Chem. 288, 24799-24808
39. Claros, M. G., and Vincens, P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241, 779-786
40. Bannai, H., Tamada, Y., Maruyama, O., Nakai, K., and Miyano, S. (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18, 298-305
41. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their Nterminal amino acid sequence. J. Mol. Biol. 300, 1005-1016
42. Skehan, P., Storeng, R., Scudiero, D., Monks, A., McMahon, J., Vistica, D., Warren, J. T., Bokesch H., Kenney S., and Boyd M. R. (1990) New colorimetric cytotoxicity assay for anticancer-drug screening. J. Natl. Cancer Inst. 82, 1107-1112
43. Klement, P., Nijtmans, L. G., Van den Bogert, C., and Houstěk, J. (1995) Analysis of oxidative phosphorylation complexes in cultured human fibroblasts and amniocytes by blue-native-electrophoresis using mitoplasts isolated with the help of digitonin. Anal. Biochem. 231, 218-224
44. Wilm, M., Shevchenko, A., Houthaeve, T., Breit, S., Schweigerer, L., Fotsis, T., and Mann, M. (1996) Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379, 466-469
45. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567
46. Rhee, H. W., Zou, P., Udeshi, N. D., Martell, J. D., Mootha, V. K., Carr, S. A., and Ting, A. Y. (2013) Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science 339, 1328-1331
47. Uhlmann, T., Geoghegan, V. L., Thomas, B., Ridlova, G., Trudgian, D. C., and Acuto, O. (2012) A method for large-scale identification of protein arginine methylation. Mol. Cell. Proteomics 11, 1489-1499
48. Bremang, M., Cuomo, A., Agresta, A. M., Stugiewicz, M., Spadotto, V., and Bonaldi, T. (2013) Mass spectrometry-based identification and characterisation of lysine and arginine methylation in the human proteome. Mol. Biosyst. 9, 2231-2247
49. Cao, X.-J., Arnaudo, A. M., and Garcia, B. A. (2013) Large-scale global identification of protein lysine methylation in vivo. Epigenetics 8, 477-485
50. Huang, J., and Berger, S. L. (2008) The emerging field of dynamic lysine methylation of non-histone proteins. Curr. Opin. Genet. Dev. 18, 152-158
51. Bedford, M. T., and Clarke, S. G. (2009) Protein arginine methylation in mammals. Who, what, and why. Mol. Cell 33, 1-13
52. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., Casero, R. A., and Shi, Y. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941-953
53. Tsukada, Y., Fang, J., Erdjument-Bromage, H., Warren, M. E., Borchers, C. H., Tempst, P., and Zhang, Y. (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439, 811-816
54. Kooistra, S. M., and Helin, K. (2012) Molecular mechanisms and potential functions of histone demethylases. Nat. Rev. Mol. Cell Biol. 13, 297-311
55. Jonassen, T., and Clarke, C. F. (2000) Isolation and functional expression of human COQ3, a gene encoding a methyltransferase required for ubiquinone biosynthesis. J. Biol. Chem. 275, 12381-12387
56. Dibrov, E., Robinson, K. M., and Lemire, B. D. (1997) The COQ5 gene encodes a yeast mitochondrial protein necessary for ubiquinone biosynthesis and the assembly of the respiratory chain. J. Biol. Chem. 272, 9175-9181
57. Bloxham, D. P., Parmelee, D. C., Kumar, S., Walsh, K. A., and Titani, K. (1982) Complete amino acid sequence of porcine heart citrate synthase. Biochemistry 21, 2028-2036
58. Aquila, H., Bogner, W., and Klingenberg, M. (1982) ADP/ATP-translocator from beef heart mitochondria. Amino acid sequence and surface labelling. Hoppe Seyler's Z. Physiol. Chem. 363, 894
59. Chen, R., Fearnley, I. M., Palmer, D. N., and Walker, J. E. (2004) Lysine 43 is trimethylated in subunit c from bovine mitochondrial ATP synthase and in storage bodies associated with Batten disease. J. Biol. Chem. 279, 21883-21887
60. Martzen, M. R., McCraith, S. M., Spinelli, S. L., Torres, F. M., Fields, S., Grayhack, E. J., and Phizicky, E. M. (1999) A biochemical genomics approach for identifying genes by the activity of their products. Science 286, 1153-1155
61. Polevoda, B., Martzen, M. R., Das, B., Phizicky, E. M., and Sherman, F. (2000) Cytochrome c methyltransferase, Ctm1p, of yeast. J. Biol. Chem. 275, 20508-20513
62. Evans, C. T., Owens, D. D., Slaughter, C. A., and Srere, P. A. (1988) Characterization of mutant TMK368K pig citrate synthase expressed in and isolated from Escherichia coli. Biochem. Biophys. Res. Commun. 157, 1231-1238
63. 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
64. Fisk, J. C., Li, J., Wang, H., Aletta, J. M., Qu, J., and Read, L. K. (2013) Proteomic analysis reveals diverse classes of arginine methylproteins in mitochondria of trypanosomes. Mol. Cell. Proteomics 12, 302-311
65. Smith, A. C., and Robinson, A. J., (2009) MitoMiner, an integrated database for the storage and analysis of mitochondrial proteomics data. Mol. Cell. Proteomics 8, 1324-1337
66. Clason, T., Ruiz, T., Schägger, H., Peng, G., Zickermann, V., Brandt, U., Michel, H., and Radermacher, M. (2010) The structure of eukaryotic and prokaryotic complex I. J. Struct. Biol. 169, 81-88
67. Ching, Y. P., Zhou, H. J., Yuan, J. G., Qiang, B. Q., Kung, H. F., Jin, D. Y. (2002) Identification and characterization of FTSJ2, a novel human nucleolar protein homologous to bacterial ribosomal RNA methyltransferase. Genomics 79, 2-6
68. Zehmer, J. K., Bartz, R., Liu, P., Anderson, R. G. (2008) Identification of a novel N-terminal hydrophobic sequence that targets proteins to lipid droplets. J. Cell Sci. 121, 1852-1860
69. Zehmer, J. K., Bartz, R., Bisel, B., Liu, P., Seemann, J., Anderson, R. G. (2009) Targeting sequences of UBXD8 and AAM-B reveal that the ER has a direct role in the emergence and regression of lipid droplets. J. Cell Sci. 122, 3694-3702
70. Saveanu, C., Fromont-Racine, M., Harington, A., Ricard, F., Namane, A., and Jacquier, A. (2001) Identification of 12 new yeast mitochondrial ribosomal proteins including 6 that have no prokaryotic homologues. J. Biol. Chem. 276, 15861-15867
71. Cloutier, P., Lavallée-Adam, M., Faubert, D., Blanchette, M., and Coulombe, B. (2013). A newly uncovered group of distantly related lysine methyltransferases preferentially interact with molecular chaperones to regulate their activity. PLoS Genet. 9, e1003210
72. Cámara, Y., Asin-Cayuela, J., Park, C. B., Metodiev, M. D., Shi, Y., Ruzzenente, B., Kukat, C., Habermann, B., Wibom, R., Hultenby, K., Franz, T., Erdjument-Bromage, H., Tempst, P., Hallberg, B. M., Gustafsson, C. M., and Larsson, N. G. (2011) MTERF4 regulates translation by targeting the methyltransferase NSUN4 to the mammalian mitochondrial ribosome. Cell Metab. 13, 527-539
73. Lee, J., Sayegh, J., Daniel, J., Clarke, S., and Bedford M. T. (2005) PRMT8, a new membrane-bound tissue-specific member of the protein arginine methyltransferase family. J. Biol. Chem. 280, 32890-32896
74. McCulloch, V., Seidel-Rogol, B. L., and Shadel, G. S. (2002) A human mitochondrial transcription factor is related to RNA adenine methyltransferases and binds S-adenosylmethionine. Mol. Cell. Biol. 22, 1116-1125
75. Falkenberg, M., Gaspari, M., Rantanen, A., Trifunovic, A., Larsson, N.-G., and Gustafsson, C. M. (2002) Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet. 31, 289-294
76. Liu, J., and Straby K. B. (2000) The human tRNA(m22G26) dimethyltransferase. Functional expression and characterization of a cloned hTRM1 gene. Nucleic Acids Res. 28, 3445-3451
77. Brulé, H., Elliott, M., Redlak, M., Zehner, Z. E., and Holmes, W. M. (2004) Isolation and characterization of the human tRNA-(N1G37) methyltransferase (TRM5) and comparison to the Escherichia coli TrmD protein. Biochemistry 43, 9243-9255
78. Chujo, T., and Suzuki, T. (2012) Trmt61B is a methyltransferase responsible for 1-methyladenosine at position 58 of human mitochondrial tRNAs. RNA 18, 2269-2276
79. Margueron, R., Li, G., Sarma, K., Blais, A., Zavadil, J., Woodcock, C. L., Dynlacht, B. D., and ReinbergD(2008) Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol. Cell 32, 503-518
80. Nakamura, T., Mori, T., Tada, S., Krajewski, W., Rozovskaia, T., Wassell, R., Dubois, G., Mazo, A., Croce, C. M., and Canaani, E. (2002) ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol. Cell 10, 1119-1128
81. Hsieh, J. J.-D., Ernst, P., Erdjument-Bromage, H., Tempst, P., and Korsmeyer, S. J. (2003) Proteolytic cleavage of MLL generates a complex of Nand C-terminal fragments that confers protein stability and subnuclear localization. Mol. Cell. Biol. 23, 186-194
82. Demers, C., Chaturvedi, C.-P., Ranish, J. A., Juban, G., Lai, P., Morle, F., Aebersold, R., Dilworth, F. J., Groudine, M., and Brand, M. (2007) Activator-mediated recruitment of the MLL2 methyltransferase complex to the β-globin locus. Mol. Cell 27, 573-584
83. Young, M. J., and Court D. A. (2008) Effects of the S288c genetic background and common auxotrophic markers on mitochondrial DNA function in Saccharomyces cerevisiae. Yeast 25, 903-912
84. Holzmann, J., Frank, P., Löffler, E., Bennett, K. L., Gerner, C., and Rossmanith, W. (2008) RNase P without RNA. Identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 135, 462-474