CDK4-mediated MnSOD activation and mitochondrial homeostasis in radioadaptive protection

Free Radical Biology and Medicine

Volumn 81, Issue , 2015, Pages 77-87

  Jin, Cuihong ^a,f   Qin, Lili ^a   Shi, Yan ^a   Candas, Demet ^a   Fan, Ming ^a   Lu, Chung Ling ^a   Vaughan, Andrew T M ^a   Shen, Rulong ^b   Wu, Larry S ^a   Liu, Rui ^a   Li, Robert F ^a   Murley, Jeffrey S ^c   Woloschak, Gayle ^d   Grdina, David J ^c   Li, Jian Jian ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Cyclin D1 CDK4; Free radicals; Mitochondrial homeostasis; MnSOD; Phosphorylation; Radioadaptive response

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE 4; MANGANESE SUPEROXIDE DISMUTASE; CCND1 PROTEIN, MOUSE; CDK4 PROTEIN, MOUSE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CYTOSOLIC FRACTION; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; IONIZING RADIATION; KERATINOCYTE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RADIATION PROTECTION; WHOLE BODY RADIATION; ADAPTATION; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; RADIATION DOSE; RADIATION RESPONSE; SIGNAL TRANSDUCTION;

MAMMALIA; MUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL LINE; CYCLIN D1; CYCLIN-DEPENDENT KINASE 4; DOSE-RESPONSE RELATIONSHIP, RADIATION; GENE EXPRESSION REGULATION; HUMANS; KERATINOCYTES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED BALB C; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; PHOSPHORYLATION; RADIATION TOLERANCE; RADIATION, IONIZING; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; WHOLE-BODY IRRADIATION;

EID: 84923616310     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.12.026     Document Type: Article

References (51)

1. L.E. Feinendegen, V.P. Bond, C.A. Sondhaus, and H. Muehlensiepen Radiation effects induced by low doses in complex tissue and their relation to cellular adaptive responses Mutat. Res. 358 1996 199 205
2. S. Are Wolff radiation-induced effects hormetic? Science 245 575 1989 621
3. L.E. Feinendegen, V.P. Bond, C.A. Sondhaus, and K.I. Altman Cellular signal adaptation with damage control at low doses versus the predominance of DNA damage at high doses C. R. Acad. Sci. III 322 1999 245 251
4. S.Z. Liu Biological effects of low level exposures to ionizing radiation: theory and practice Hum. Exp. Toxicol. 29 2010 275 281
5. L.W. Oberley, and G.R. Buettner Role of superoxide dismutase in cancer: a review Cancer Res. 39 1979 1141 1149
6. J.M. McCord, B.B. Keele Jr., and I. Fridovich An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase Proc. Natl. Acad. Sci. USA 68 1971 1024 1027
7. M. Fan, K.M. Ahmed, M.C. Coleman, D.R. Spitz, and J.J. Li Nuclear factor-kappaB and manganese superoxide dismutase mediate adaptive radioresistance in low-dose irradiated mouse skin epithelial cells Cancer Res. 67 2007 3220 3228
8. D. Candas, M. Fan, D. Nantajit, A.T. Vaughan, J.S. Murley, G.E. Woloschak, D.J. Grdina, and J.J. Li CyclinB1/Cdk1 phosphorylates mitochondrial antioxidant MnSOD in cell adaptive response to radiation stress J. Mol. Cell Biol. 5 2013 166 175
9. D.J. Grdina, J.S. Murley, R.C. Miller, H.J. Mauceri, H.G. Sutton, M.J. Thirman, J.J. Li, G.E. Woloschak, and R.R. Weichselbaum A manganese superoxide dismutase (SOD2)-mediated adaptive response Radiat. Res. 179 2013 115 124
10. J.S. Murley, K.L. Baker, R.C. Miller, T.E. Darga, R.R. Weichselbaum, and D.J. Grdina SOD2-mediated adaptive responses induced by low-dose ionizing radiation via TNF signaling and amifostine Free Radic. Biol. Med. 51 2011 1918 1925
11. J. Veeraraghavan, M. Natarajan, T.S. Herman, and N. Aravindan Low-dose gamma-radiation-induced oxidative stress response in mouse brain and gut: regulation by NFkappaB-MnSOD cross-signaling Mutat. Res. 718 2011 44 55
12. H.C. Yen, T.D. Oberley, S. Vichitbandha, Y.S. Ho St, and D.K. Clair The protective role of manganese superoxide dismutase against adriamycin-induced acute cardiac toxicity in transgenic mice J. Clin. Invest. 98 1996 1253 1260
13. M.W. Epperly, C. Sikora, S. Defilippi, J. Bray, G. Koe, D. Liggitt, J.D. Luketich, and J.S. Greenberger Plasmid/liposome transfer of the human manganese superoxide dismutase transgene prevents ionizing irradiation-induced apoptosis in human esophagus organ explant culture Int. J. Cancer 90 2000 128 137
14. Y. Niu, H. Wang, D. Wiktor-Brown, R. Rugo, H. Shen, M.S. Huq, B. Engelward, M. Epperly, and J.S. Greenberger Irradiated esophageal cells are protected from radiation-induced recombination by MnSOD gene therapy Radiat. Res. 173 2010 453 461
15. J.S. Murley, Y. Kataoka, C.J. Weydert, L.W. Oberley, and D.J. Grdina Delayed radioprotection by nuclear transcription factor kappaB-mediated induction of manganese superoxide dismutase in human microvascular endothelial cells after exposure to the free radical scavenger WR1065 Free Radic. Biol. Med. 40 2006 1004 1016
16. G.E. Borgstahl, H.E. Parge, M.J. Hickey, W.F. Beyer Jr., R.A. Hallewell, and J.A. Tainer The structure of human mitochondrial manganese superoxide dismutase reveals a novel tetrameric interface of two 4-helix bundles Cell 71 1992 107 118
17. Y. Chen, J. Zhang, Y. Lin, Q. Lei, K.L. Guan, S. Zhao, and Y. Xiong Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS EMBO Rep. 12 2011 534 541
18. R. Tao, M.C. Coleman, J.D. Pennington, O. Ozden, S.H. Park, H. Jiang, H.S. Kim, C.R. Flynn, S. Hill, W. Hayes McDonald, A.K. Olivier, D.R. Spitz, and D. Gius Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress Mol. Cell 40 2010 893 904
19. C. Quijano, D. Hernandez-Saavedra, L. Castro, J.M. McCord, B.A. Freeman, and R. Radi Reaction of peroxynitrite with Mn-superoxide dismutase: role of the metal center in decomposition kinetics and nitration J. Biol. Chem. 276 2001 11631 11638
20. G. Roue, V. Pichereau, H. Lincet, D. Colomer, and B. Sola Cyclin D1 mediates resistance to apoptosis through upregulation of molecular chaperones and consequent redistribution of cell death regulators Oncogene 27 2008 4909 4920
21. K.M. Ahmed, M. Fan, D. Nantajit, N. Cao, and J.J. Li Cyclin D1 in low-dose radiation-induced adaptive resistance Oncogene 27 2008 6738 6748
22. R. Agami, and R. Bernards Distinct initiation and maintenance mechanisms cooperate to induce G1 cell cycle arrest in response to DNA damage Cell 102 2000 55 66
23. T. Sakamaki, M.C. Casimiro, X. Ju, A.A. Quong, S. Katiyar, M. Liu, X. Jiao, A. Li, X. Zhang, Y. Lu, C. Wang, S. Byers, R. Nicholson, T. Link, M. Shemluck, J. Yang, S.T. Fricke, P.M. Novikoff, A. Papanikolaou, A. Arnold, C. Albanese, and R. Pestell Cyclin D1 determines mitochondrial function in vivo Mol. Cell. Biol. 26 2006 5449 5469
24. C. Wang, Z. Li, Y. Lu, R. Du, S. Katiyar, J. Yang, M. Fu, J.E. Leader, A. Quong, P.M. Novikoff, and R.G. Pestell Cyclin D1 repression of nuclear respiratory factor 1 integrates nuclear DNA synthesis and mitochondrial function Proc. Natl. Acad. Sci. USA 103 2006 11567 11572
25. P. Sumrejkanchanakij, M. Tamamori-Adachi, Y. Matsunaga, K. Eto, and M.A. Ikeda Role of cyclin D1 cytoplasmic sequestration in the survival of postmitotic neurons Oncogene 22 2003 8723 8730
26. K.R. Hagen, X. Zeng, M.Y. Lee, S. Tucker Kahn, M.K. Harrison Pitner, S.S. Zaky, Y. Liu, R.M. O'Regan, X. Deng, and H.I. Saavedra Silencing CDK4 radiosensitizes breast cancer cells by promoting apoptosis Cell Div 8 2013 10
27. D.R. Spitz, and L.W. Oberley An assay for superoxide dismutase activity in mammalian tissue homogenates Anal. Biochem. 179 1989 8 18
28. C. Frezza, S. Cipolat, and L. Scorrano Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts Nat. Protoc. 2 2007 287 295
29. G. Lu, S. Ren, P. Korge, J. Choi, Y. Dong, J. Weiss, C. Koehler, J.N. Chen, and Y. Wang A novel mitochondrial matrix serine/threonine protein phosphatase regulates the mitochondria permeability transition pore and is essential for cellular survival and development Genes Dev. 21 2007 784 796
30. P. Mukhopadhyay, M. Rajesh, G. Hasko, B.J. Hawkins, M. Madesh, and P. Pacher Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy Nat. Protoc. 2 2007 2295 2301
31. C. Vives-Bauza, L. Yang, and G. Manfredi Assay of mitochondrial ATP synthesis in animal cells and tissues Methods Cell Biol. 80 2007 155 171
32. J.A. Marchal, M.C. Nunez, I. Suarez, M. Diaz-Gavilan, J.A. Gomez-Vidal, H. Boulaiz, F. Rodriguez-Serrano, M.A. Gallo, A. Espinosa, A. Aranega, and J.M. Campos A synthetic uracil derivative with antitumor activity through decreasing cyclin D1 and Cdk1, and increasing p21 and p27 in MCF-7 cells Breast Cancer Res. Treat. 105 2007 237 246
33. M. Malumbres, and M. Barbacid To cycle or not to cycle: a critical decision in cancer Nat. Rev. Cancer 1 2001 222 231
34. E. Blanchet, J.S. Annicotte, and L. Fajas Cell cycle regulators in the control of metabolism Cell Cycle 8 2009 4029 4031
35. M. Tamamori-Adachi, H. Ito, P. Sumrejkanchanakij, S. Adachi, M. Hiroe, M. Shimizu, J. Kawauchi, M. Sunamori, F. Marumo, S. Kitajima, and M.A. Ikeda Critical role of cyclin D1 nuclear import in cardiomyocyte proliferation Circ. Res. 92 2003 e12 e19
36. Z. Wang, M. Fan, D. Candas, T.Q. Zhang, L. Qin, A. Eldridge, S. Wachsmann-Hogiu, K.M. Ahmed, B.A. Chromy, D. Nantajit, N. Duru, F. He, M. Chen, T. Finkel, L.S. Weinstein, and J.J. Li Cyclin B1/Cdk1 coordinates mitochondrial respiration for cell-cycle G2/M progression Dev. Cell 29 2014 217 232
37. J.R. Henderson, H. Swalwell, S. Boulton, P. Manning, C.J. McNeil, and M.A. Birch-Machin Direct, real-time monitoring of superoxide generation in isolated mitochondria Free Radic. Res. 43 2009 796 802
38. 2 signaling Antioxid. Redox Signaling 14 2011 459 468
39. T.R. Figueira, M.H. Barros, A.A. Camargo, R.F. Castilho, J.C. Ferreira, A.J. Kowaltowski, F.E. Sluse, N.C. Souza-Pinto, and A.E. Vercesi Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health Antioxid. Redox Signaling 18 2013 2029 2074
40. R.S. Balaban, S. Nemoto, and T. Finkel Mitochondria, oxidants, and aging Cell 120 2005 483 495
41. S.K. Dhar St, and D.K. Clair Manganese superoxide dismutase regulation and cancer Free Radic. Biol. Med. 52 2012 2209 2222
42. S.J. Stohs, and D. Bagchi Oxidative mechanisms in the toxicity of metal ions Free Radic. Biol. Med. 18 1995 321 336
43. S.S. Leonard, G.K. Harris, and X. Shi Metal-induced oxidative stress and signal transduction Free Radic. Biol. Med. 37 2004 1921 1942
44. M. Valko, C.J. Rhodes, J. Moncol, M. Izakovic, and M. Mazur Free radicals, metals and antioxidants in oxidative stress-induced cancer Chem. Biol. Interact. 160 2006 1 40
45. J.C. Lee, Y.O. Son, P. Pratheeshkumar, and X. Shi Oxidative stress and metal carcinogenesis Free Radic. Biol. Med. 53 2012 742 757
46. C. Hureaua Coordination of redox active metal ions to the amyloid precursor protein and to amyloid-β peptides involved in Alzheimer disease Coord. Chem. Rev. 256 2012 2164 2174
47. M. Pollycove Radiobiological basis of low-dose irradiation in prevention and therapy of cancer Dose Response 5 2007 26 38
48. N. Phan, M. De Lisio, G. Parise, and D.R. Boreham Biological effects and adaptive response from single and repeated computed tomography scans in reticulocytes and bone marrow of C57BL/6 mice Radiat. Res. 177 2012 164 175
49. E. Blanchet, J.S. Annicotte, S. Lagarrigue, V. Aguilar, C. Clape, C. Chavey, V. Fritz, F. Casas, F. Apparailly, J. Auwerx, and L. Fajas E2F transcription factor-1 regulates oxidative metabolism Nat. Cell Biol. 13 2011 1146 1152
50. Y. Lee, J.E. Dominy, Y.J. Choi, M. Jurczak, N. Tolliday, J.P. Camporez, H. Chim, J.H. Lim, H.B. Ruan, X. Yang, F. Vazquez, P. Sicinski, G.I. Shulman, and P. Puigserver Cyclin D1-Cdk4 controls glucose metabolism independently of cell cycle progression Nature 510 2014 547 551
51. D. Nantajit, M. Fan, N. Duru, Y. Wen, J.C. Reed, and J.J. Li Cyclin B1/Cdk1 phosphorylation of mitochondrial p53 induces anti-apoptotic response PLoS One 5 2010 e12341