Identification of novel modulators of mitochondrial function by a genome-wide RNAi screen in Drosophila melanogaster

Genome Research

Volumn 18, Issue 1, 2008, Pages 123-136

  Chen, Jian ^a   Shi, Xiaoying ^a   Padmanabhan, Ranjani ^a   Wang, Qiong ^a   Wu, Zhidan ^a   Stevenson, Susan C ^a   Hild, Marc ^a   Garza, Dan ^a   Li, Hao ^a  

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CITRATE SYNTHASE; DOUBLE STRANDED RNA;

ARTICLE; BARREN GENE; BIOGENESIS; CG3249 GENE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; EUKARYOTE; GENE; GENE IDENTIFICATION; GENOME ANALYSIS; HDAC6 GENE; IN VIVO STUDY; INSECT CELL; KLUMPFUSS GENE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; RPD3 GENE; SIGNAL TRANSDUCTION; SMT3 GENE; SRC42A GENE; TRANSCRIPTION REGULATION; TRANSGENE; TRANSLATION REGULATION; VIMAR GENE;

ANIMALS; CHROMOSOME MAPPING; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENOME, INSECT; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; PROTEIN BIOSYNTHESIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

DROSOPHILA MELANOGASTER; EUKARYOTA;

EID: 38049029093     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.6940108     Document Type: Article

References (86)

1. Affaitati, A., Cardone, L., De, C.T., Carlucci, A., Ginsberg, M.D., Varrone, S., Gottesman, M.E., Avvedimento, E.V., and Feliciello, A. 2003. Essential role of A-kinase anchor protein 121 for cAMP signaling to mitochondria. J. Biol. Chem. 278: 4286-4294.
2. Appaix, F., Kuznetsov, A.V., Usson, Y., Kay, L., Andrienko, T., Olivares, J., Kaambre, T., Sikk, P., Margreiter, R., and Saks, V. 2003. Possible role of cytoskeleton in intracellular arrangement and regulation of mitochondria. Exp. Physiol. 88: 175-190.
3. Bakin, R.E. and Jung, M.O. 2004. Cytoplasmic sequestration of HDAC7 from mitochondrial and nuclear compartments upon initiation of apoptosis. J. Biol. Chem. 279: 51218-51225.
4. Barlow, A.L., van Drunen, C.M., Johnson, C.A., Tweedie, S., Bird, A., and Turner, B.M. 2001. dSIR2 and dHDAC6: Two novel, inhibitor-resistant deacetylases in Drosophila melanogaster. Exp. Cell Res. 265: 90-103.
5. Bhat, M.A., Philp, A.V., Glover, D.M., and Bellen, H.J. 1996. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II. Cell 87: 1103-1114.
6. Bos, J.L. 2005. Linking Rap to cell adhesion. Curr. Opin. Cell Biol. 17: 123-128.
7. Bruce, C.R., Kriketos, A.D., Cooney, G.J., and Hawley, J.A. 2004. Disassociation of muscle triglyceride content and insulin sensitivity after exercise training in patients with Type 2 diabetes. Diabetologia 47: 23-30.
8. Cardone, L., Carlucci, A., Affaitati, A., Livigni, A., DeCristofaro, T., Garbi, C., Varrone, S., Ullrich, A., Gottesman, M.E., Avvedimento, E.V., et al. 2004. Mitochondrial AKAP121 binds and targets protein tyrosine phosphatase D1, a novel positive regulator of src signaling. Mol. Cell. Biol. 24: 4613-4626.
9. Catalano, D., Licciulli, F., Turi, A., Grillo, G., Saccone, C., and D'Elia, D. 2006. MitoRes: A resource of nuclear-encoded mitochondrial genes and their products in Metazoa. BMC Bioinformatics 7: 36. doi: 10.1186/1471-2105-7-36.
10. Celotto, A.M., Frank, A.C., McGrath, S.W., Fergestad, T., Van Voorhies, W.A., Buttle, K.F., Mannella, C.A., and Palladino, M.J. 2006. Mitochondrial encephalomyopathy in Drosophila. J. Neurosci. 26: 810-820.
11. Chen, H. and Chan, D.C. 2005. Emerging functions of mammalian mitochondrial fusion and fission. Hum. Mol. Genet. 14: R283-R289.
12. Czubryt, M.P., McAnally, J., Fishman, G.I., and Olson, E.N. 2003. Regulation of peroxisome proliferator-activated receptor γ coactivator 1α (PGC-1α) and mitochondrial function by MEF2 and HDAC5. Proc. Natl. Acad. Sci. 100: 1711-1716.
13. DeSimone, S.M. and White, K. 1993. The Drosophila erect wing gene, which is important for both neuronal and muscle development, encodes a protein which is similar to the sea urchin P3A2 DNA binding protein. Mol. Cell. Biol. 13: 3641-3649.
14. DeSimone, S., Coelho, C., Roy, S., Vijay Raghavan, K., and White, K. 1996. ERECT WING, the Drosophila member of a family of DNA binding proteins is required in imaginal myoblasts for flight muscle development. Development 122: 31-39.
15. Dohmen, R.J. 2004. SUMO protein modification. Biochim. Biophys. Acta 1695: 113-131.
16. Dokmanovic, M. and Marks, P.A. 2005. Prospects: Histone deacetylase inhibitors. J. Cell. Biochem. 96: 293-304.
17. Fazio, I.K., Bolger, T.A., and Gill, G. 2001. Conserved regions of the Drosophila erect wing protein contribute both positively and negatively to transcriptional activity. J. Biol. Chem. 276: 18710-18716.
18. Feliciello, A., Gottesman, M.E., and Avvedimento, E.V. 2005. cAMP-PKA signaling to the mitochondria: Protein scaffolds, mRNA and phosphatases. Cell. Signal. 17: 279-287.
19. Fergestad, T., Bostwick, B., and Ganetzky, B. 2006. Metabolic disruption in Drosophila bang-sensitive seizure mutants. Genetics 173: 1357-1364.
20. Gallinari, P., Di, M.S., Jones, P., Pallaoro, M., and Steinkuhler, C. 2007. HDACs, histone deacetylation and gene transcription: From molecular biology to cancer therapeutics. Cell Res. 17: 195-211.
21. Gao, L., Cueto, M.A., Asselbergs, F., and Atadja, P. 2002. Cloning and functional characterization of HDAC11, a novel member of the human histone deacetylase family. J. Biol. Chem. 277: 25748-25755.
22. Graham, B.H., Waymire, K.G., Cottrell, B., Trounce, I.A., MacGregor, G.R., and Wallace, D.C. 1997. A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nat. Genet. 16: 226-234.
23. Haggarty, S.J., Koeller, K.M., Wong, J.C., Grozinger, C.M., and Schreiber, S.L. 2003. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl. Acad. Sci. 100: 4389-4394.
24. Harada, H., Becknell, B., Wilm, M., Mann, M., Huang, L.J., Taylor, S.S., Scott, J.D., and Korsmeyer, S.J. 1999. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol. Cell 3: 413-422.
25. Harder, Z., Zunino, R., and McBride, H. 2004. Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr. Biol. 14: 340-345.
26. Hild, M., Beckmann, B., Haas, S.A., Koch, B., Solovyev, V., Busold, C., Fellenberg, K., Boutros, M., Vingron, M., Sauer, F., et al. 2003. An integrated gene annotation and transcriptional profiling approach towards the full gene content of the Drosophila genome. Genome Biol. 5: R3. doi: 10.1186/gb-2003-5-1-r3.
27. Hirano, T., Kobayashi, R., and Hirano, M. 1997. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 89: 511-521.
28. Horbinski, C. and Chu, C.T. 2005. Kinase signaling cascades in the mitochondrion: A matter of life or death. Free Radic. Biol. Med. 38: 2-11.
29. Hubbert, C., Guardiola, A., Shao, R., Kawaguchi, Y., Ito, A., Nixon, A., Yoshida, M., Wang, X.F., and Yao, T.P. 2002. HDAC6 is a microtubule-associated deacetylase. Nature 417: 455-458.
30. Huo, L. and Scarpulla, R.C. 2001. Mitochondrial DNA instability and peri-implantation lethality associated with targeted disruption of nuclear respiratory factor 1 in mice. Mol. Cell. Biol. 21: 644-654.
31. Iwata, A., Riley, B.E., Johnston, J.A., and Kopito, R.R. 2005. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J. Biol. Chem. 280: 40282-40292.
32. Iyengar, B., Roote, J., and Campos, A.R. 1999. The tamas gene, identified as a mutation that disrupts larval behavior in Drosophila melanogaster, codes for the mitochondrial DNA polymerase catalytic subunit (DNApol-gamma125). Genetics 153: 1809-1824.
33. Jacobs, H.T., Fernández-Ayala, D.J., Manjiry, S., Kemppainen, E., Toivonen, J.M., and O'Dell, K.M. 2004. Mitochondrial disease in flies. Biochim. Biophys. Acta 1659: 190-196.
34. Kania, A., Salzberg, A., Bhat, M., D'Evelyn, D., He, Y., Kiss, I., and Bellen, H.J. 1995. P-element mutations affecting embryonic peripheral nervous system development in Drosophila melanogaster. Genetics 139: 1663-1678.
35. Kelley, D.E., He, J., Menshikova, E.V., and Ritov, V.B. 2002. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950.
36. Klingenberg, M. 1992. Structure-function of the ADP/ATP carrier. Biochem. Soc. Trans. 20: 547-550.
37. Knutti, D. and Kralli, A. 2001. PGC-1, a versatile coactivator. Trends Endocrinol. Metab. 12: 360-365.
38. Kovacs, J.J., Murphy, P.J., Gaillard, S., Zhao, X., Wu, J.T., Nicchitta, C.V., Yoshida, M., Toft, D.O., Pratt, W.B., and Yao, T.P. 2005. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 18: 601-607.
39. Kraft, C.S., LeMoine, C.M., Lyons, C.N., Michaud, D., Mueller, C.R., and Moyes, C.D. 2006. Control of mitochondrial biogenesis during myogenesis. Am. J. Physiol. Cell Physiol. 290: C1119-C1127.
40. Kuhajda, F.P. 2006. Fatty acid synthase and cancer: New application of an old pathway. Cancer Res. 66: 5977-5980.
41. Le Bras, B.M., Rouy, I., and Brenner, C. 2006. The modulation of inter-organelle cross-talk to control apoptosis. Med. Chem. 2: 1-12.
42. Lee, Y.S. and Carthew, R.W. 2003. Making a better RNAi vector for Drosophila: Use of intron spacers. Methods 30: 322-329.
43. Legagneux, V., Cubizolles, F., and Watrin, E. 2004. Multiple roles of Condensins: A complex story. Biol. Cell. 96: 201-213.
44. Lehman, J.J., Barger, P.M., Kovacs, A., Saffitz, J.E., Medeiros, D.M., and Kelly, D.P. 2000. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106: 847-856.
45. Leon, J., Cuna-Castroviejo, D., Sainz, R.M., Mayo, J.C., Tan, D.X., and Reiter, R.J. 2004. Melatonin and mitochondrial function. Life Sci. 75: 765-790.
46. Lin, J., Puigserver, P., Donovan, J., Tarr, P., and Spiegelman, B.M. 2002. Peroxisome proliferator-activated receptor γ coactivator 1β (PGC-1β), a novel PGC-1-related transcription coactivator associated with host cell factor. J. Biol. Chem. 277: 1645-1648.
47. Livigni, A., Scorziello, A., Agnese, S., Adornetto, A., Carlucci, A., Garbi, C., Castaldo, I., Annunziato, L., Avvedimento, E.V., and Feliciello, A. 2006. Mitochondrial AKAP121 links cAMP and src signaling to oxidative metabolism. Mol. Biol. Cell 17: 263-271.
48. Lu, X. and Li, Y. 1999. Drosophila Src42A is a negative regulator of RTK signaling. Dev. Biol. 208: 233-243.
49. Maier, D., Farr, C.L., Poeck, B., Alahari, A., Vogel, M., Fischer, S., Kaguni, L.S., and Schneuwly, S. 2001. Mitochondrial single-stranded DNA-binding protein is required for mitochondrial DNA replication and development in Drosophila melanogaster. Mol. Biol. Cell 12: 821-830.
50. Martin, M., Macías, M., León, J., Escames, G., Khaldy, H., and Acuña-Castroviejo, D. 2002. Melatonin increases the activity of the oxidative phosphorylation enzymes and the production of ATP in rat brain and liver mitochondria. Int. J. Biochem. Cell Biol. 34: 348-357.
51. Matsuyama, A., Shimazu, T., Sumida, Y., Saito, A., Yoshimatsu, Y., Seigneurin-Berny, D., Osada, H., Komatsu, Y., Nishino, N., Khochbin, S., et al. 2002. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21: 6820-6831.
52. McBride, H.M., Neuspiel, M., and Wasiak, S. 2006. Mitochondria: More than just a powerhouse. Curr. Biol. 16: R551-R560.
53. Meirhaeghe, A., Crowley, V., Lenaghan, C., Lelliott, C., Green, K., Stewart, A., Hart, K., Schinner, S., Sethi, J.K., Yeo, G., et al. 2003. Characterization of the human, mouse and rat PGC1β (peroxisome- proliferator-activated receptor-γ co-activator 1β) gene in vitro and in vivo. Biochem. J. 373: 155-165.
54. Miceli, M.V. and Jazwinski, S.M. 2005. Nuclear gene expression changes due to mitochondrial dysfunction in ARPE-19 cells: Implications for age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 46: 1765-1773.
55. Mootha, V.K., Handschin, C., Arlow, D., Xie, X., St, P.J., Sihag, S., Yang, W., Altshuler, D., Puigserver, P., Patterson, N., et al. 2004. Errα and Gabpa/b specify PGC-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. 101: 6570-6575.
56. Mortensen, O.H., Frandsen, L., Schjerling, P., Nishimura, E., and Grunnet, N. 2006. PGC-1α and PGC-1β have both similar and distinct effects on myofiber switching toward an oxidative phenotype. Am. J. Physiol. Endocrinol. Metab. 291: E807-E816.
57. Moyes, C.D., Mathieu-Costello, O.A., Tsuchiya, N., Filburn, C., and Hansford, R.G. 1997. Mitochondrial biogenesis during cellular differentiation. Am. J. Phys. 272: C1345-C1351.
58. Murphy, P.J., Morishima, Y., Kovacs, J.J., Yao, T.P., and Pratt, W.B. 2005. Regulation of the dynamics of hsp90 action on the glucocorticoid receptor by acetylation/deacetylation of the chaperone. J. Biol. Chem. 280: 33792-33799.
59. Nisoli, E., Clementi, E., Moncada, S., and Carruba, M.O. 2004. Mitochondrial biogenesis as a cellular signaling framework. Biochem. Pharmacol. 67: 1-15.
60. Nisoli, E., Tonello, C., Cardile, A., Cozzi, V., Bracale, R., Tedesco, L., Falcone, S., Valerio, A., Cantoni, O., Clementi, E., et al. 2005. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310: 314-317.
61. Pile, L.A., Spellman, P.T., Katzenberger, R.J., and Wassarman, D.A. 2003. The SIN3 deacetylase complex represses genes encoding mitochondrial proteins: Implications for the regulation of energy metabolism. J. Biol. Chem. 278: 37840-37848.
62. Psarra, A.M., Solakidi, S., Trougakos, I.P., Margaritis, L.H., Spyrou, G., and Sekeris, C.E. 2005. Glucocorticoid receptor isoforms in human hepatocarcinoma HepG2 and SaOS-2 osteosarcoma cells: Presence of glucocorticoid receptor alpha in mitochondria and of glucocorticoid receptor beta in nucleoli. Int. J. Biochem. Cell Biol. 37: 2544-2558.
63. Puigserver, P. and Spiegelman, B.M. 2003. Peroxisome proliferator- activated receptor γ coactivator 1α (PGC-1α): Transcriptional coactivator and metabolic regulator. Endocr. Rev. 24: 78-90.
64. Qiao, J., Mei, F.C., Popov, V.L., Vergara, L.A., and Cheng, X. 2002. Cell cycle-dependent subcellular localization of exchange factor directly activated by cAMP. J. Biol. Chem. 277: 26581-26586.
65. Reznick, R.M. and Shulman, G.I. 2006. The role of AMP-activated protein kinase in mitochondrial biogenesis. J. Physiol. 574: 33-39.
66. Rikhy, R., Ramaswami, M., and Krishnan, K.S. 2003. A temperature- sensitive allele of Drosophila sesB reveals acute functions for the mitochondrial adenine nucleotide translocase in synaptic transmission and dynamin regulation. Genetics 165: 1243-1253.
67. Rusconi, J.C., Fink, J.L., and Cagan, R. 2004. klumpfuss regulates cell death in the Drosophila retina. Mech. Dev. 121: 537-546.
68. Ryan, M.T. and Hoogenraad, N.J. 2007. Mitochondrial-nuclear communications. Annu. Rev. Biochem. 76: 701-722.
69. Salvi, M., Brunati, A.M., Bordin, L., La, R.N., Clari, G., and Toninello, A. 2002. Characterization and location of Src-dependent tyrosine phosphorylation in rat brain mitochondria. Biochim. Biophys. Acta 1589: 181-195.
70. Sanchez-Martinez, A., Luo, N., Clemente, P., Adan, C., Hernandez-Sierra, R., Ochoa, P., Fernandez-Moreno, M.A., Kaguni, L.S., and Garesse, R. 2006. Modeling human mitochondrial diseases in flies. Biochim. Biophys. Acta 1757: 1190-1198.
71. Sardiello, M., Licciulli, F., Catalano, D., Attimonelli, M., and Caggese, C. 2003. MitoDrome: A database of Drosophila melanogaster nuclear genes encoding proteins targeted to the mitochondrion. Nucleic Acids Res. 31: 322-324. doi: 10.1093/nar/gkg123.
72. Scarpulla, R.C. 2002. Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim. Biophys. Acta 1576: 1-14.
73. Scarpulla, R.C. 2006. Nuclear control of respiratory gene expression in mammalian cells. J. Cell. Biochem. 97: 673-683.
74. Schapira, A.H. 2006. Mitochondrial disease. Lancet 368: 70-82.
75. Scheller, K. and Sekeris, C.E. 2003. The effects of steroid hormones on the transcription of genes encoding enzymes of oxidative phosphorylation. Exp. Physiol. 88: 129-140.
76. Schreiber, S.N., Emter, R., Hock, M.B., Knutti, D., Cardenas, J., Podvinec, M., Oakeley, E.J., and Kralli, A. 2004. The estrogen-related receptor α (ERRα) functions in PPARγ coactivator 1α (PGC-1α)-induced mitochondrial biogenesis. Proc. Natl. Acad. Sci. 101: 6472-6477.
77. Tateno, M., Nishida, Y., and Chi-Yamada, T. 2000. Regulation of JNK by Src during Drosophila development. Science 287: 324-327.
78. Toivonen, J.M., Odell, K.M., Petit, N., Irvine, S.C., Knight, G.K., Lehtonen, M., Longmuir, M., Luoto, K., Touraille, S., Wang, Z., et al. 2001. Technical knockout, a Drosophila model of mitochondrial deafness. Genetics 159: 241-254.
79. Traven, A., Wong, J.M., Xu, D., Sopta, M., and Ingles, C.J. 2001. Interorganellar communication. Altered nuclear gene expression profiles in a yeast mitochondrial dna mutant. J. Biol. Chem. 276: 4020-4027.
80. Wang, H., Hiatt, W.R., Barstow, T.J., and Brass, E.P. 1999. Relationships between muscle mitochondrial DNA content, mitochondrial enzyme activity and oxidative capacity in man: Alterations with disease. Eur. J. Appl. Physiol. Occup. Physiol. 80: 22-27.
81. Wang, Z., Dillon, T.J., Pokala, V., Mishra, S., Labudda, K., Hunter, B., and Stork, P.J. 2006. Rap1-mediated activation of extracellular signal-regulated kinases by cyclic AMP is dependent on the mode of Rap1 activation. Mol. Cell. Biol. 26: 2130-2145.
82. Weber, K., Bruck, P., Mikes, Z., Kupper, J.H., Klingenspor, M., and Wiesner, R.J. 2002. Glucocorticoid hormone stimulates mitochondrial biogenesis specifically in skeletal muscle. Endocrinology 143: 177-184.
83. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R.C., et al. 1999. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
84. Zhang, Y.Q., Roote, J., Brogna, S., Davis, A.W., Barbash, D.A., Nash, D., and Ashburner, M. 1999. stress sensitive B encodes an adenine nucleotide translocase in Drosophila melanogaster. Genetics 153: 891-903.
85. Zhang, Y., Li, N., Caron, C., Matthias, G., Hess, D., Khochbin, S., and Matthias, P. 2003. HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J. 22: 1168-1179.
86. Zunino, R., Schauss, A., Rippstein, P., Ndrade-Navarro, M., and McBride, H.M. 2007. The SUMO protease SENP5 is required to maintain mitochondrial morphology and function. J. Cell Sci. 120: 1178-1188.