c-MYC apoptotic function is mediated by NRF-1 target genes

Genes and Development

Volumn 17, Issue 2, 2003, Pages 240-255

  Morrish, Fionnuala ^a   Giedt, Christopher ^a   Hockenbery, David ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Apoptosis; c MYC; Mitochondrial biogenesis; NRF 1

Indexed keywords

CYTOCHROME C; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF 1; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BIOGENESIS; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; MITOCHONDRION; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION;

3T3 CELLS; ANIMALS; APOPTOSIS; BASE SEQUENCE; BINDING SITES; CELL DIVISION; CELL LINE; CYTOCHROME C GROUP; DNA; DNA-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION; GENES, MYC; MICE; MICROSCOPY, ELECTRON; MITOCHONDRIA; MUTATION; NF-E2-RELATED FACTOR 1; NUCLEAR RESPIRATORY FACTOR 1; NUCLEAR RESPIRATORY FACTORS; PROMOTER REGIONS (GENETICS); RATS; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS;

ANIMALIA;

EID: 0037439054     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1032503     Document Type: Article

References (64)

1. Bauer, M., Schubert, A., Rocks, O., and Grimm, S. 1999. Adenine nucleotide translocase-1, a component of the permeability transition pore, can dominantly induce apoptosis. J. Cell. Biol. 147: 1493-1501.
2. Becjker, T., Burgess, S., Amsterdam, A., Allende, M., and Hopkins, N. 1998. not really finished is crucial for development of the zebrafish outer retina and encodes a transcription factor highly homologous to human nuclear respiratory factor-1 and avian initiation binding repressor. Development 125: 4369-4378.
3. Bejarano, M., Cornvik, A., Brijker, S., Asker, C., Osorio, L., and Henriksson, M. 2000. Inhibition of cell growth and apoptosis by inducible expression of the transcriptional repressor Madl. Exp. Cell Res. 260: 61-72.
4. Bissonnette, R., Echeverri, F., Mahboubi, A., and Green, D. 1992. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature 359: 552-556.
5. Bouchard, C., Thieke, K., Maier, A., Saffrich, R., Hanley-Hyde, J., Ansorge, W., Reed, S., Sicinski, P., Bartek, J., and Eilers, M. 1999. Direct induction of cyclin D2 by Myc contributes to cell cycle progression and sequestration of p27. EMBO J. 18: 5321-5333.
6. Boyd, K.E. and Farnham, P.J. 1997 Myc versus USF: Discrimination at the cad gene is determined by core promoter elements. Mol. Cell Biol. 17: 2529-2537.
7. Capaldi, R. 1990. Structure and function of cytochrome c oxidase. Ann. Rev. Biochem. 59: 569-596.
8. Chau, C., Evans, M., and Scarpula, R. 1992. Nuclear respiratory factor 1 activation sites in genes encoding the γ subunit of ATP synthase, eukaryotic initiation factor 2α, and tyrosine aminotransferase. J. Biol. Chem. 267: 6999-7006.
9. Cole, M. and McMahon, S. 1999. The Myc oncoprotein: A critical evaluation of transactivation and target gene regulation. Oncogene 18: 2916-2924.
10. Coller, H.A., Grandori, C., Tamayo, P. Colbert, T. Lander, E.S., Eisenman, R.N., and Golub, T.R. 2000. Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling and adhesion. Proc. Natl. Acad. Sci. 97: 3260-3265.
11. Dang, C. 1999. c-Myc target genes involved in cell growth, apoptosis and metabolism. Mol. Cell Biol. 19: 1-11.
12. Daugas, E., Susin, S., Zamzami, N., Ferri, K., Iriniopoulou, T., Larochette, N., Prevost, M.-C., Leber, B., Andrews, D., Penninger, J., et al. 2000. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J. 14: 729-739.
13. Dean, M., Levine, R.A., Ran, W., Kindy, M.S., Sonenshein, G.E., and Campisi, J. 1986. Regulation of c-myc transcription and mRNA abundance by serum growth factors and cell contact. J. Biol. Chem. 261: 9161-9166.
14. DeSimone, S. 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.
15. D'Herde, K., De Prest, B., Mussche, S., Schotte, P., Beyaert, P., Van Coster, R., and Roels, F. 2000. The ultrastructural localization of cytochrome c in apoptosis demonstrates mitochondrial heterogeneity. Cell Death Diff. 7: 331-337.
16. Evan, G. and Littlewood, T. 1993. The role of c-myc in cell growth. Curr. Opin. Gene. Dev. 3: 44-49.
17. Evan, G., Wyllie, A.H., Gilbert, C., Littlewood, T., Land, H., Brooks, M., Waters, C., Penn, L., and Hancock, D. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69: 119-128.
18. Evans, M. and Scarpulla, R. 1989. Interaction of nuclear factors with multiple sites in the somatic cytochrome c promoter. J. Biol. Chem. 264: 14361-14368.
19. Frank, S.R., Schroeder, M. Fernandez, P. Taubert, S., and Amati, B. 2001. Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes & Dev. 15: 2069-2082.
20. Fulda, S., Lutz, W., Schwab, M., and Debatin, K. 1999. MycN sensitizes neuroblastoma cells for drug-induced apoptosis. Oncogene 18: 1479-1486.
21. Gehring, S., Rottmann, S., Menkel, A., Mertsching, J., Krippner- Heidenreich, A., and Luscher, B. 2000. Inhibition of proliferation and apoptosis by the transcriptional repressor Mad1. J. Biol. Chem. 275: 10413-10420.
22. Grandori, C. and Eisenman, R.N. 1997. Myc target genes. Trends Biochem. Sci. 22: 177-181.
23. Grandori, C., Mac, J., Siebelt, F., Ayer, D.E., and Eisenman, R.N. 1996. Myc-Max hetrodimers activate a DEAD box gene and interact with multiple E box-related sites in vivo. EMBO J. 15: 4344-4357.
24. Grandori, C. Cowley, S.M., James, L.P., and Eisenman, R.N. 2000 The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol. 16: 653-699.
25. Grossman, L. and Lomax, M. 1997. Nuclear genes for cytochrome c oxidase. Bioch. Biophy. Acta 1352: 174-192.
26. Guo, Q.M., Malek, R.L., Kim, C.C., He, H., Ruffy, M., Sanka, K., Lee, N.H., Dang, C.V., and Liu, E.T. 2000. Identification of c-Myc responsive genes using rat cDNA microarray. Cancer Res. 60: 5922-5928.
27. Gugneia, S. and Scarpulla, R. 1997. Serine phosphorylation within a concise amino-terminal domain in nuclear respiratory factor enhances DNA binding. J. Biol. Chem. 272: 18732-18739.
28. Haiek, P., Villani, G., and Attarde, G. 2001 Rate-limiting step preceding cytochrome c release in cells primed for Fas-mediated apoptosis revealed by analysis of cellular mosaicism of respiratory changes. J. Biol. Chem. 278: 606-615.
29. Herzig, R., Scacco, S., and Scarpulla, R. 2000. Sequential serum-dependent activation of CREB and NRF-1 leads to enhanced mitochondrial respiration through the induction of cytochrome c. J. Biol. Chem. 275: 13134-13141.
30. Hirst, S. and Grandori, C. 2000. Differential activity of conditional Myc and its variant Myc-S in human mortal fibroblasts. Oncogene 19: 5189-5197.
31. Hockenbery, D.M., Oltvai, Z.N., Yin, X.M., Milliman, C.L., and Korsmeyer, S.J. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241-251.
32. 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.
33. Jakovicic, S., Swift, H.H., Gross, N.J., and Rabonowitz, M. 1978. Biochemical and stereological analysis of rat liver mitochondrial in different thyroid states. J. Cell Biol. 77: 887-901.
34. Juin, P., Hueber, A., Littlewood, T., and Evan, G. 2000. c-Myc- induced sensitization to apoptosis is mediated through cytochrome c release. Genes & Dev. 13: 1367-1381.
35. Kadenbach, B., Huttemann, M., Arnold, S., Lee, I., and Bender, E. 2000. Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Rad. Biol. Med. 29: 211-221.
36. Kagaya, S., Kitanaka, D., Noguchi, K., Mochizuki, T., Sugiyama, A., Asai, A., Yasuhara, N., Eguchi, Y., Tsujimoto, Y., and Kuchino, Y. 1997. A functional role for death proteases in s-Myc and c-Myc mediated apoptosis. Mol. Cell. Biol. 17: 6736-6745,
37. Kallioniemi, O., Visakorpi, T., Holi, K., Isola, J., and Rabinovitch, P. 1994. Automated peak detection and cell cycle analysis of flow cytometric DNA histograms. Cytometry 16: 250-255.
38. Kluck, R., Bossy-Wetzel, E., Green, D., and Newmeyer, D. 1997. The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136.
39. Knappik, A. and Pluckthus, A. 1994. An improved affinity tag based on the Flag peptide for the detection and purification of recombinant antibody fragments. Biotechniques 17: 754-761.
40. Li, K., Li, Y., Shelton, J., Richardson, J., Spencer, E., Chen, Z., Wang, X., and Williams, R. 2000. Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis. Cell 101: 389-399.
41. Littlewood, T., Hancock, D., Danielina, P., Parker, M., and Evan, G. 1995. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucl. Acid Res. 23: 1686-1690.
42. Mateyak, M., Obaya, A., Adachi, S., and Sedivy, J. 1997. Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Diff. 8: 1039-1048.
43. Mirabella, M., Di Giovanni, S., Silvestri, G., Tonali, P., and Servidei, S. 2000. Apoptosis in mitochondrial encephalomyopathies with mitochondrial DNA mutations: A potential pathogenic mechanism. Brain 123: 93-104.
44. Nasi, S., Ciarapica, R., Jucker, R., Rosati, J., and Soucek, L. 2001. Making decisions through Myc. FEBS Lett. 490: 153-162.
45. Nelson, B., Luciakova, K., Li, R., and Betina, S. 1995. The role of thyroid hormone and promoter diversity in the regulation of nuclear encoded mitochondrial proteins. Bioch. Biophys. Acta 1271: 85-91.
46. Nesbit, C., Tersakk, J., and Prochownik, E. 1999. Myc oncogenes and human neoplastic disease. Oncogene 18: 3004-3016.
47. Okazaki, M., Ishibashi, Y., Asoh, S., and Ohta, S. 1998. Overexpressed mitochondrial hinge protein: A cytochrome c-binding protein accelerates apoptosis by enhancing the release of cytochrome c from mitochondria. Bioch. Biophys. Res Comm. 243: 131-135.
48. Oltvai, Z.N., Milliman, C.L., and Korsmeyer, S.J. 1993. Bcl-2 hetrodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 7: 609-619.
49. Orlando, V., Strutt, H., and Paro, R. 1997. Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11: 205-214.
50. Osthus, R.C., Shim, H., Kim, S., Li, Q., Reddy, R., Mukherjee, M., Xu, Y., Wonsey, D., Lee, L., and Dang, C. 2000. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J. Biol. Chem. 275: 21797-21800.
51. Pear, W., Nolan, G., Scott, M., and Baltimore, D. 1993. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. 90: 8392-8396.
52. Poyton, R. 1998. Assembly of a time bomb-cytochrome c oxidase and disease. Nat. Genet. 20: 316-317.
53. Poyton, R. and McEwen, J. 1996. Crosstalk between nuclear and mitochondrial genomes. Ann. Rev. Biochem. 65: 563-607.
54. Prendergast, G. 1999. Mechanisms of apoptosis by c-Myc. Oncogene 18: 2967-2987.
55. Scarpulla, R. 2002. Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286: 81-89.
56. Schapira, A. and Cock, H. 1999. Mitochondrial myopathies and encephalomyopathies. Eur. J. Clin. Invest. 29: 886-898.
57. Seligman, A., Karnovsky, M., Wasserkrug, H., and Hanker, J. 1968. Non-droplet ultrastructural demonstration of cytochrome oxidase activity with a polymerizing osmiophilic reagent, diaminobenzidine (DAB). J. Cell Biol. 38: 1-13.
58. Virabsius, J. and Scarpulla, R. 1994. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: A potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc. Natl. Acad. Sci. 91: 1309-1313.
59. Virbasius, C.M.A., Virbasius, J., and Scarpulla, R. 1993. NRF-1, an activator involved in nuclear-mitochondrial interactions, utilizes a new DNA-binding domain conserved in a family of developmental regulators. Genes & Dev. 7: 2431-2445.
60. Wong-Riley, M., Guo, A., Bachman, N.J., and Lomax, M.I. 2000. Human COX6A1 gene: Promoter analysis, cDNA isolation and expression in the monkey brain. Gene 247: 63-75.
61. Wu, K., Grandori, C., Amacker, M., Simon-Vermot, N., Polack, A., Lingner, J., and Dalla-Favera, R. 1999. Direct activation of TERT transcription by c-Myc. Nature Genet. 21: 220-224.
62. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R., et al. 2000. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
63. Xia, Y., Buja, L., Scarpulla, R., and McMillin, J. 1997. Electrical stimulation of neonatal cardiomycetes results in the sequential activation of nuclear genes governing mitochondrial proliferation and differentiation. Proc. Natl. Acad. Sci. 94: 11399-11404.
64. Zeller, K.I., Haggerty, T.J., Barrett, J.F., Guo, Q., Wonsey, D.R., and Dang, C.V. 2001. characterization of nucleophosmin (B23) as a Myc target by scanning chromatin immunoprecipitation. J. Biol. Chem. 276: 48285-48291.