CDK1 Enhances Mitochondrial Bioenergetics for Radiation-Induced DNA Repair

Cell Reports

Volumn 13, Issue 10, 2015, Pages 2056-2063

  Qin, Lili ^a   Fan, Ming ^a   Candas, Demet ^a   Jiang, Guochun ^b   Papadopoulos, Stelios ^b   Tian, Lin ^b   Woloschak, Gayle ^c   Grdina, David J ^d   Li, Jian Jian ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

CDK1; DNA repair; mitochondrial bioenergetics; radiation

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL NUCLEUS DNA; CYCLIN B1; OXYGEN; RED FLUORESCENT PROTEIN; SMALL INTERFERING RNA; CDK1 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE;

ANIMAL CELL; ARTICLE; BIOENERGY; CELL COMMUNICATION; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL TARGETING SIGNAL; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION INJURY REPAIR; RESPIRATORY CHAIN; CELL LINE; COMET ASSAY; ENERGY METABOLISM; GENE SILENCING; GENETIC TRANSFECTION; METABOLISM; MITOCHONDRION; PHYSIOLOGY; PROTEIN TRANSPORT; RADIATION RESPONSE; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; BLOTTING, WESTERN; CELL LINE; COMET ASSAY; CYCLIN-DEPENDENT KINASES; DNA DAMAGE; DNA REPAIR; ENERGY METABOLISM; GENE KNOCKDOWN TECHNIQUES; HUMANS; MITOCHONDRIA; PROTEIN TRANSPORT; RADIATION EFFECTS; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84971254439     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.11.015     Document Type: Article

References (34)

1. Artesi, M., Kroonen, J., Bredel, M., Nguyen-Khac, M., Deprez, M., Schoysman, L., Poulet, C., Chakravarti, A., Kim, H., Scholtens, D., et al. Connexin 30 expression inhibits growth of human malignant gliomas but protects them against radiation therapy. Neuro-oncol. 17 (2015), 392–406.
2. Bakkenist, C.J., Kastan, M.B., Initiating cellular stress responses. Cell 118 (2004), 9–17.
3. Bernstein, C., Bernstein, H., Payne, C.M., Garewal, H., DNA repair/pro-apoptotic dual-role proteins in five major DNA repair pathways: fail-safe protection against carcinogenesis. Mutat. Res. 511 (2002), 145–178.
4. Candas, D., Fan, M., Nantajit, D., Vaughan, A.T., Murley, J.S., Woloschak, G.E., Grdina, D.J., Li, J.J., CyclinB1/Cdk1 phosphorylates mitochondrial antioxidant MnSOD in cell adaptive response to radiation stress. J. Mol. Cell Biol. 5 (2013), 166–175.
5. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S.A., Bakalarski, C.E., Elledge, S.J., Gygi, S.P., A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105 (2008), 10762–10767.
6. Eguchi, Y., Shimizu, S., Tsujimoto, Y., Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57 (1997), 1835–1840.
7. Frezza, C., Cipolat, S., Scorrano, L., Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat. Protoc. 2 (2007), 287–295.
8. Gafter-Gvili, A., Herman, M., Ori, Y., Korzets, A., Chagnac, A., Zingerman, B., Rozen-Zvi, B., Gafter, U., Malachi, T., Inhibition of mitochondrial function reduces DNA repair in human mononuclear cells. Leuk. Res. 35 (2011), 219–225.
9. Gautier, J., Minshull, J., Lohka, M., Glotzer, M., Hunt, T., Maller, J.L., Cyclin is a component of maturation-promoting factor from Xenopus. Cell 60 (1990), 487–494.
10. Gavet, O., Pines, J., Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis. J. Cell Biol. 189 (2010), 247–259.
11. Gong, B., Chen, Q., Almasan, A., Ionizing radiation stimulates mitochondrial gene expression and activity. Radiat. Res. 150 (1998), 505–512.
12. Harbauer, A.B., Opalińska, M., Gerbeth, C., Herman, J.S., Rao, S., Schönfisch, B., Guiard, B., Schmidt, O., Pfanner, N., Meisinger, C., Mitochondria. Cell cycle-dependent regulation of mitochondrial preprotein translocase. Science 346 (2014), 1109–1113.
13. Hochegger, H., Takeda, S., Hunt, T., Cyclin-dependent kinases and cell-cycle transitions: does one fit all?. Nat. Rev. Mol. Cell Biol. 9 (2008), 910–916.
14. Hoeijmakers, J.H., DNA damage, aging, and cancer. N. Engl. J. Med. 361 (2009), 1475–1485.
15. Hopfner, K.P., Karcher, A., Shin, D.S., Craig, L., Arthur, L.M., Carney, J.P., Tainer, J.A., Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101 (2000), 789–800.
16. Horbinski, C., Chu, C.T., Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radic. Biol. Med. 38 (2005), 2–11.
17. Jin, C., Qin, L., Shi, Y., Candas, D., Fan, M., Lu, C.L., Vaughan, A.T., Shen, R., Wu, L.S., Liu, R., et al. CDK4-mediated MnSOD activation and mitochondrial homeostasis in radioadaptive protection. Free Radic. Biol. Med. 81 (2015), 77–87.
18. Kastan, M.B., Bartek, J., Cell-cycle checkpoints and cancer. Nature 432 (2004), 316–323.
19. Kulkarni, R., Reither, A., Thomas, R.A., Tucker, J.D., Mitochondrial mutant cells are hypersensitive to ionizing radiation, phleomycin and mitomycin C. Mutat. Res. 663 (2009), 46–51.
20. Kulkarni, R., Thomas, R.A., Tucker, J.D., Expression of DNA repair and apoptosis genes in mitochondrial mutant and normal cells following exposure to ionizing radiation. Environ. Mol. Mutagen. 52 (2011), 229–237.
21. Lu, C.L., Qin, L., Liu, H.C., Candas, D., Fan, M., Li, J.J., Tumor cells switch to mitochondrial oxidative phosphorylation under radiation via mTOR-mediated hexokinase II inhibition–a Warburg-reversing effect. PLoS ONE, 10, 2015, e0121046.
22. Meike, S., Yamamori, T., Yasui, H., Eitaki, M., Matsuda, A., Inanami, O., 8-Aminoadenosine enhances radiation-induced cell death in human lung carcinoma A549 cells. J. Radiat. Res. (Tokyo) 52 (2011), 456–463.
23. Nantajit, D., Fan, M., Duru, N., Wen, Y., Reed, J.C., Li, J.J., Cyclin B1/Cdk1 phosphorylation of mitochondrial p53 induces anti-apoptotic response. PLoS ONE, 5, 2010, e12341.
24. Pagliarini, D.J., Dixon, J.E., Mitochondrial modulation: reversible phosphorylation takes center stage?. Trends Biochem. Sci. 31 (2006), 26–34.
25. Paull, T.T., Gellert, M., Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13 (1999), 1276–1288.
26. Scheibye-Knudsen, M., Fang, E.F., Croteau, D.L., Wilson, D.M. 3rd, Bohr, V.A., Protecting the mitochondrial powerhouse. Trends Cell Biol. 25 (2015), 158–170.
27. Shao, L., Luo, Y., Zhou, D., Hematopoietic stem cell injury induced by ionizing radiation. Antioxid. Redox Signal. 20 (2014), 1447–1462.
28. Soule, H.D., Maloney, T.M., Wolman, S.R., Peterson, W.D. Jr., Brenz, R., McGrath, C.M., Russo, J., Pauley, R.J., Jones, R.F., Brooks, S.C., Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50 (1990), 6075–6086.
29. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T., Mihara, K., Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282 (2007), 11521–11529.
30. Vives-Bauza, C., Yang, L., Manfredi, G., Assay of mitochondrial ATP synthesis in animal cells and tissues. Methods Cell Biol. 80 (2007), 155–171.
31. Wang, Z., Fan, M., Candas, D., Zhang, T.Q., Qin, L., Eldridge, A., Wachsmann-Hogiu, S., Ahmed, K.M., Chromy, B.A., Nantajit, D., et al. Cyclin B1/Cdk1 coordinates mitochondrial respiration for cell-cycle G2/M progression. Dev. Cell 29 (2014), 217–232.
32. Ward, I., Chen, J., Early events in the DNA damage response. Curr. Top. Dev. Biol. 63 (2004), 1–35.
33. Yamamori, T., Yasui, H., Yamazumi, M., Wada, Y., Nakamura, Y., Nakamura, H., Inanami, O., Ionizing radiation induces mitochondrial reactive oxygen species production accompanied by upregulation of mitochondrial electron transport chain function and mitochondrial content under control of the cell cycle checkpoint. Free Radic. Biol. Med. 53 (2012), 260–270.
34. Yamano, K., Youle, R.J., Coupling mitochondrial and cell division. Nat. Cell Biol. 13 (2011), 1026–1027.