Drosophila cyclin D/Cdk4 regulates mitochondrial biogenesis and aging and sensitizes animals to hypoxic stress

Cell Cycle

Volumn 11, Issue 3, 2012, Pages 554-568

  Icreverzi, Amalia ^a   Flor De La Cruz, Aida ^a   Van Voorhies, Wayne A ^b   Edgar, Bruce A ^a,c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b NEW MEXICO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Aging; CycD; Drosophila; Hypoxia; Mitobiogenesis; Superoxide

Indexed keywords

CYCLIN D; CYCLIN DEPENDENT KINASE 4; SUPEROXIDE; TRANSCRIPTION FACTOR NRF1;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CELL AGING; CELL CYCLE; CELL HYPOXIA; CONTROLLED STUDY; DROSOPHILA; HYPOXIA; LIFESPAN; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; PROTEIN FUNCTION; REGULATORY MECHANISM; SENSITIZATION;

EID: 84857198083     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.11.3.19062     Document Type: Article

References (54)

1. Diehl JA. Cycling to cancer with cyclin D1. Cancer Biol Ther 2002; 1:226-31; PMID:12432268.
2. Filmus JRA, Robles AI, Shi W, Wong MJ, Colombo LL, Conti CJ. Induction of cyclin D1 overexpression by activated ras. Oncogene 1994; 9:3627-33; PMID:7970723.
3. 1 phase of the cell cycle. Cell 1991; 65:701- 13; PMID:1827757; http://dx.doi.org/10.1016/0092- 8674(91)90101-4.
4. Sewing ABC, Bürger C, Brüsselbach S, Schalk C, Lucibello FC, Müller R. Human cyclin D1 encodes a labile nuclear protein whose synthesis is directly induced by growth factors and suppressed by cyclic AMP. J Cell Sci 1993; 104:545-55; PMID:8389378.
5. Surmacz ERK, Reiss K, Sell C, Baserga R. Cyclin D1 messenger RNA is inducible by platelet-derived growth factor in cultured fibroblasts. Cancer Res 1992; 52:4522-5; PMID:1379514.
6. Won KAXY, Xiong Y, Beach D, Gilman MZ. Growth-regulated expression of D-type cyclin genes in human diploid fibroblasts. Proc Natl Acad Sci USA 1992; 89:9910-4; PMID:1409718; http://dx.doi. org/10.1073/pnas.89.20.9910.
7. Miliani de Marval PLME, Macias E, Conti CJ, Rodriguez-Puebla ML. Enhanced malignant tumorigenesis in Cdk4 transgenic mice. Oncogene 2004; 23:1863-73; PMID:14647432; http://dx.doi. org/10.1038/sj.onc.1207309.
8. Mullany LKWP, White P, Hanse EA, Nelsen CJ, Goggin MM, Mullany JE, et al. Distinct proliferative and transcriptional effects of the D-type cyclins in vivo. Cell Cycle 2008; 7:2215-24; PMID:18635970; http:// dx.doi.org/10.4161/cc. 7.14.6274.
9. Yu QCM, Ciemerych MA, Sicinski P. Ras and Myc can drive oncogenic cell proliferation through individual D-cyclins. Oncogene 2005; 24:7114- 9; PMID:16103884; http://dx.doi.org/10.1038/ sj.onc.1208853.
10. Sicinski PDJ, Donaher JL, Parker SB, Li T, Fazeli A, Gardner H, et al. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 1995; 82:621-30; PMID:7664341; http://dx.doi. org/10.1016/0092- 8674(95)90034-9.
11. Meyer CAJH, Jacobs HW, Datar SA, Du W, Edgar BA, Lehner CF. Drosophila Cdk4 is required for normal growth and is dispensable for cell cycle progression. EMBO J 2000; 19:4533-42; PMID:10970847; http:// dx.doi.org/10.1093/emboj/19.17.4533.
12. Datar SAJH, Jacobs HW, de la Cruz AF, Lehner CF, Edgar BA. The Drosophila cyclin D-Cdk4 complex promotes cellular growth. EMBO J 2000; 19:4543- 54; PMID:10970848; http://dx.doi.org/10.1093/ emboj/19.17.4543.
13. Buttitta LAKA, Katzaroff AJ, Perez CL, de la Cruz A, Edgar BA. A double-assurance mechanism controls cell cycle exit upon terminal differentiation in Drosophila. Dev Cell 2007; 12:631-43; PMID:17419999; http:// dx.doi.org/10.1016/j.devcel.2007.02.020.
14. Frei CGM, Galloni M, Hafen E, Edgar BA. The Drosophila mitochondrial ribosomal protein mRpL12 is required for Cyclin D/Cdk4-driven growth. EMBO J 2005; 24:623-34; PMID:15692573; http://dx.doi. org/10.1038/sj.emboj.7600523.
15. Frei CEB, Edgar BA. Drosophila cyclin D/Cdk4 requires Hif-1 prolyl hydroxylase to drive cell growth. Dev Cell 2004; 6:241-51; PMID:14960278; http:// dx.doi.org/10.1016/S1534-5807(03)00409-X.
16. Centanin LRP, Ratcliffe PJ, Wappner P. Reversion of lethality and growth defects in Fatiga oxygen-sensor mutant flies by loss of hypoxia-inducible factor-alpha/ Sima. EMBO Rep 2005; 6:1070-5; PMID:16179946; http://dx.doi.org/ 10.1038/sj.embor.7400528.
17. McBride HMNM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Curr Biol 2006; 16:551-60; PMID:16860735; http://dx.doi. org/10.1016/j.cub.2006.06.054.
18. Scarpulla RC. Nuclear control of respiratory gene expression in mammalian cells. J Cell Biochem 2006; 97:673-83; PMID:16329141; http://dx.doi. org/10.1002/jcb.20743.
19. Dang CVLA, Le A, Gao P. MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clin Cancer Res 2009; 15:6479-83; PMID:19861459; http://dx.doi.org/10.1158/1078-0432.CCR-09-0889.
20. Trinei MBI, Pelicci PG, Giorgio M. Mitochondrial DNA copy number is regulated by cellular proliferation: a role for Ras and p66(Shc). Biochim Biophys Acta 2006; 1757:624-30.
21. Echave P, Machado-da-Silva G, Arkell RS, Duchen MR, Jacobson J, Mitter R, et al. Extracellular growth factors and mitogens cooperate to drive mitochondrial biogenesis. J Cell Sci 2009; 122:4516-25; PMID:19920079; http://dx.doi.org/10.1242/jcs.049734.
22. Herzig RP, Scacco S, Scarpulla RC. Sequential serumdependent activation of CREB and NRF-1 leads to enhanced mitochondrial respiration through the induction of cytochrome c. J Biol Chem 2000; 275:13134- 41; PMID:10777619; http://dx.doi.org/10.1074/ jbc.275.17.13134.
23. Andersson U, Scarpulla RC. Pgc-1-related coactivator, a novel, serum-inducible coactivator of nuclear respiratory factor 1-dependent transcription in mammalian cells. Mol Cell Biol 2001; 21:3738- 49; PMID:11340167; http://dx.doi.org/10.1128/ MCB.21.11.3738-49.2001.
24. Wang CLZ, Li Z, Lu Y, Du R, Katiyar S, Yang J, et al. Cyclin D1 repression of nuclear respiratory factor 1 integrates nuclear DNA synthesis and mitochondrial function. Proc Natl Acad Sci USA 2006; 103:11567- 72; PMID:16864783; http://dx.doi.org/10.1073/ pnas.0603363103.
25. Gugneja S Sr, Scarpulla RC. Serine phosphorylation within a concise amino-terminal domain in nuclear respiratory factor 1 enhances DNA binding. J Biol Chem 1997; 272:18732-9; PMID:9228045; http:// dx.doi.org/10.1074/jbc.272. 30.18732.
26. Galloni M. Bonsaï, a ribosomal protein S15 homolog, involved in gut mitochondrial activity and systemic growth. Dev Biol 2003; 264:482-94; PMID:14651932; http://dx.doi.org/10.1016/j.ydbio.2003.08.021.
27. Fernández-Ayala DJCS, Chen S, Kemppainen E, O'Dell KM, Jacobs HT. Gene expression in a Drosophila model of mitochondrial disease. PLoS One 2010; 5:8549; PMID:20066047; http://dx.doi. org/10.1371/journal.pone.0008549.
28. Zhang HGP, Gao P, Fukuda R, Kumar G, Krishnamachary B, Zeller KI, et al. HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 2007; 11:407- 20; PMID:17482131; http://dx.doi.org/10.1016/j. ccr.2007.04.001.
29. Kim JWTI, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006; 3:177- 85; PMID:16517405; http://dx.doi.org/10.1016/j. cmet.2006.02.002.
30. Liu GRJ, Roy J, Johnson EA. Identification and function of hypoxia-response genes in Drosophila melanogaster. Physiol Genomics 2006; 25:134-41; PMID:16403841; http://dx.doi.org/10.1152/physiolgenomics. 00262.2005.
31. Azad P, Zhou D, Russo E, Haddad GG. Distinct mechanisms underlying tolerance to intermittent and constant hypoxia in Drosophila melanogaster. PLoS One 2009; 4:5371; PMID:19401761; http://dx.doi. org/10.1371/journal.pone. 0005371.
32. Hoppeler HVM, Vogt M, Weibel ER, Flück M. Response of skeletal muscle mitochondria to hypoxia. Exp Physiol 2003; 88:109-19; PMID:12525860; http://dx.doi.org/10.1113/eph8802513.
33. Hoppeler H, Vogt M, Weibel ER, Flück M. Response of skeletal muscle mitochondria to hypoxia. Exp Physiol 2003; 88:109-19; PMID:12525860; http:// dx.doi.org/10.1113/eph8802513.
34. Hales KGFM, Fuller MT. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 1997; 90:121-9; PMID:9230308; http://dx.doi.org/10.1016/S0092- 8674(00)80319-0.
35. Melvin RGVVW, Ballard JW. Working harder to stay alive: metabolic rate increases with age in Drosophila simulans but does not correlate with life span. Insect Physiol 2007; 53:1300-6; http://dx.doi.org/10.1016/j. jinsphys.2007.07.006.
36. Batandier CFE, Fontaine E, Kériel C, Leverve XM. Determination of mitochondrial reactive oxygen species: methodological aspects. J Cell Mol Med 2002; 6:175-87; PMID:12169203; http://dx.doi. org/10.1111/j.1582-4934.2002. tb00185.x.
37. Bahadorani S, Cho J, Lo T, Contreras H, Lawal HO, Krantz DE, et al. Neuronal expression of a single-subunit yeast NADH-ubiquinone oxidoreductase (Ndi1) extends Drosophila lifespan. Aging Cell 2010; 9:191-202; PMID:20089120; http://dx.doi. org/10.1111/j.1474-9726.2010.00546.x.
38. Muller FLLM, Lustgarten MS, Jang Y, Richardson A, Van Remmen H. Trends in oxidative aging theories. Free Radic Biol Med 2007; 43:477-503; PMID:17640558; http://dx.doi.org/10.1016/j.freeradbiomed. 2007.03.034.
39. Bannai HTY, Tamada Y, Maruyama O, Nakai K, Miyano S. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 2002; 18:298- 305; PMID:11847077; http://dx.doi.org/10.1093/ bioinformatics/18.2.298.
40. Eden ENR, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 2009; 10:48; PMID:19192299; http:// dx.doi.org/10.1186/1471-2105- 10-48.
41. Roy DTR. NRF1 (nuclear respiratory factor 1). Atlas Genet Cytogenet Oncol Haematol 2008.
42. Wen W, Ding J, Sun W, Wu K, Ning B, Gong W, et al. Suppression of cyclin D1 by hypoxia-inducible factor-1 via direct mechanism inhibits the proliferation and 5-fluorouracil-induced apoptosis of A549 cells. Cancer Res 2010; 70:2010-9; PMID:20179204; http://dx.doi. org/10.1158/0008-5472.CAN-08-4910.
43. López-Lázaro MLL. HIF-1: hypoxia-inducible factor or dysoxia-inducible factor? FASEB J 2006; 20:828- 32; PMID:16675839; http://dx.doi.org/10.1096/fj.05- 5168 hyp.
44. Bienvenu FJS, Jirawatnotai S, Elias JE, Meyer CA, Mizeracka K, Marson A, et al. Transcriptional role of cyclin D1 in development revealed by a genetic-proteomic screen. Nature 2010; 463:374- 8; PMID:20090754; http://dx.doi.org/10.1038/ nature08684.
45. Ciemerych MAK, Kenney AM, Sicinska E, Kalaszczynska I, Bronson RT, Rowitch DH, et al. Development of mice expressing a single D-type cyclin. Genes Dev 2002; 16:3277-89; PMID:12502747; http://dx.doi.org/10.1101/gad.1023602.
46. Wang C, Li Z, Lu Y, Du R, Katiyar S, Yang J, et al. Cyclin D1 repression of nuclear respiratory factor 1 integrates nuclear DNA synthesis and mitochondrial function. Proc Natl Acad Sci USA 2006; 103:11567- 72; PMID:16864783; http://dx.doi.org/10.1073/ pnas.0603363103.
47. Yu Q, Ciemerych MA, Sicinski P. Ras and Myc can drive oncogenic cell proliferation through individual D-cyclins. Oncogene 2005; 24:7114- 9; PMID:16103884; http://dx.doi.org/10.1038/ sj.onc.1208853.
48. Köhl RZJ, Zhou J, Brüne B. Reactive oxygen species attenuate nitric-oxide-mediated hypoxia-inducible factor-1alpha stabilization. Free Radic Biol Med 2006; 40:1430-42; PMID:16631533; http://dx.doi. org/10.1016/j. freeradbiomed.2005.12.012.
49. Wen WDJ, Ding J, Sun W, Wu K, Ning B, Gong W, et al. Suppression of cyclin D1 by hypoxia-inducible factor-1 via direct mechanism inhibits the proliferation and 5-fluorouracil-induced apoptosis of A549 cells. Cancer Res 2010; 70:2010-9; PMID:20179204; http://dx.doi.org/10.1158/0008-5472.CAN-08-4910.
50. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006; 3:177- 85; PMID:16517405; http://dx.doi.org/10.1016/j. cmet.2006.02.002.
51. He YWJ, Wu J, Dressman DC, Iacobuzio-Donahue C, Markowitz SD, Velculescu VE, et al. Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature 2010; 464:610-4; PMID:20200521; http://dx.doi.org/10.1038/nature08802.
52. Van Voorhies WA, Khazaeli AA, Curtsinger JW. Testing the "rate of living" model: further evidence that longevity and metabolic rate are not inversely correlated in Drosophila melanogaster. J Appl Physiol 2004; 97:1915- 22; PMID:15234957; http://dx.doi.org/10.1152/japplphysiol. 00505.2004.
53. Zid BM, Rogers AN, Katewa SD, Vargas MA, Kolipinski MC, Lu TA, et al. 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 2009; 139:149- 60; PMID:19804760; http://dx.doi.org/10.1016/j. cell.2009.07.034.
54. Bahadorani S, Bahadorani P, Marcon E, Walker DW, Hilliker AJ. A Drosophila model of Menkes disease reveals a role for DmATP7 in copper absorption and neurodevelopment. Dis Model Mech 2010; 3:84- 91; PMID:20038716; http://dx.doi.org/10.1242/ dmm.002642.