Mitochondrial reactive oxygen species perturb AKT/cyclin D1 cell cycle signaling via oxidative inactivation of PP2A in lowdose irradiated human fibroblasts

Oncotarget

Volumn 7, Issue 3, 2016, Pages 3559-3570

  Shimura, Tsutomu ^a   Sasatani, Megumi ^b   Kamiya, Kenji ^b   Kawai, Hidehiko ^b   Inaba, Yohei ^a   Kunugita, Naoki ^a  

^a NATIONAL INSTITUTE OF PUBLIC HEALTH   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

AKT; Cyclin D1; Low dose radiation; Mitochondria; ROS

Indexed keywords

CYCLIN D1; CYCLINE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE B; PROTEIN PHOSPHATASE PP2A; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; AKT1 PROTEIN, HUMAN; ANTIOXIDANT; CCND1 PROTEIN, HUMAN; PHOSPHOPROTEIN PHOSPHATASE 2;

ARTICLE; CELL AGING; CELL CYCLE S PHASE; CELL GROWTH; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INACTIVATION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LONG TERM EXPOSURE; LOW ENERGY RADIATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PROTEIN EXPRESSION; RADIATION DOSE; RADIATION EXPOSURE; APOPTOSIS; CELL CULTURE; CELL CYCLE; CELL PROLIFERATION; DNA DAMAGE; DRUG EFFECTS; FIBROBLAST; GAMMA RADIATION; LUNG; METABOLISM; MITOCHONDRION; PATHOLOGY; RADIATION RESPONSE; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANTIOXIDANTS; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN D1; DNA DAMAGE; FIBROBLASTS; GAMMA RAYS; HUMANS; LUNG; MITOCHONDRIA; OXIDATION-REDUCTION; PROTEIN PHOSPHATASE 2; PROTO-ONCOGENE PROTEINS C-AKT; RADIATION DOSAGE; REACTIVE OXYGEN SPECIES;

EID: 84962277827     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6518     Document Type: Article

References (34)

1. Finkel T. From sulfenylation to sulfhydration: what a thiolate needs to tolerate. Science signaling. 2012; 5:pe10.
2. Liu X, Kim CN, Yang J, Jemmerson R and Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 1996; 86:147-157.
3. Sena LA and Chandel NS. Physiological roles of mitochondrial reactive oxygen species. Molecular cell. 2012; 48:158-167.
4. Chandel NS. Mitochondria as signaling organelles. BMC biology. 2014; 12:34.
5. Mandal S, Lindgren AG, Srivastava AS, Clark AT and Banerjee U. Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem cells. 2011; 29:486-495.
6. Kim GJ, Chandrasekaran K and Morgan WF. Mitochondrial dysfunction, persistently elevated levels of reactive oxygen species and radiation-induced genomic instability: a review. Mutagenesis. 2006; 21:361-367.
7. Kim GJ, Fiskum GM and Morgan WF. A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer research. 2006; 66:10377-10383.
8. Fridovich I. Superoxide radical and superoxide dismutases. Annual review of biochemistry. 1995; 64:97-112.
9. Meister A. Glutathione, ascorbate, and cellular protection. Cancer research. 1994; 54:1969s-1975s.
10. Nicholson KM and Anderson NG. The protein kinase B/Akt signalling pathway in human malignancy. Cellular signalling. 2002; 14:381-395.
11. Vivanco I and Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nature reviews Cancer. 2002; 2:489-501.
12. Manning BD and Cantley LC. AKT/PKB signaling: navigating downstream. Cell. 2007; 129:1261-1274.
13. Zhou BB and Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature. 2000; 408:433-439.
14. Shimura T, Kakuda S, Ochiai Y, Nakagawa H, Kuwahara Y, Takai Y, Kobayashi J, Komatsu K and Fukumoto M. Acquired radioresistance of human tumor cells by DNA-PK/AKT/GSK3beta-mediated cyclin D1 overexpression. Oncogene. 2010; 29:4826-4837.
15. Gao T, Brognard J and Newton AC. The phosphatase PHLPP controls the cellular levels of protein kinase C. The Journal of biological chemistry. 2008; 283:6300-6311.
16. Gao T, Furnari F and Newton AC. PHLPP: a phosphatase that directly dephosphorylates Akt, promotes apoptosis, and suppresses tumor growth. Molecular cell. 2005; 18:13-24.
17. Georgescu MM. PTEN Tumor Suppressor Network in PI3K-Akt Pathway Control. Genes & cancer. 2010; 1:1170-1177.
18. Liu W, Akhand AA, Takeda K, Kawamoto Y, Itoigawa M, Kato M, Suzuki H, Ishikawa N and Nakashima I. Protein phosphatase 2A-linked and-unlinked caspase-dependent pathways for downregulation of Akt kinase triggered by 4-hydroxynonenal. Cell death and differentiation. 2003; 10:772-781.
19. Clerkin JS, Naughton R, Quiney C and Cotter TG. Mechanisms of ROS modulated cell survival during carcinogenesis. Cancer letters. 2008; 266:30-36.
20. Foley TD, Petro LA, Stredny CM and Coppa TM. Oxidative inhibition of protein phosphatase 2A activity: role of catalytic subunit disulfides. Neurochemical research. 2007; 32:1957-1964.
21. Finkel T. Signal transduction by reactive oxygen species. The Journal of cell biology. 2011; 194:7-15.
22. Shimura T, Hamada N, Sasatani M, Kamiya K and Kunugita N. Nuclear accumulation of cyclin D1 following long-term fractionated exposures to low-dose ionizing radiation in normal human diploid cells. Cell cycle. 2014; 13:1248-1255.
23. Wu G, Fang YZ, Yang S, Lupton JR and Turner ND. Glutathione metabolism and its implications for health. The Journal of nutrition. 2004; 134:489-492.
24. Staal FJ, Roederer M, Herzenberg LA and Herzenberg LA. Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. Proceedings of the National Academy of Sciences of the United States of America. 1990; 87:9943-9947.
25. Lee DH and Jacobs DR, Jr. Hormesis and public health: can glutathione depletion and mitochondrial dysfunction due to very low-dose chronic exposure to persistent organic pollutants be mitigated? Journal of epidemiology and community health. 2014.
26. Slezak BP, Hatch GE, DeVito MJ, Diliberto JJ, Slade R, Crissman K, Hassoun E and Birnbaum LS. Oxidative stress in female B6C3F1 mice following acute and subchronic exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicological sciences: an official journal of the Society of Toxicology. 2000; 54:390-398.
27. Gillett C, Fantl V, Smith R, Fisher C, Bartek J, Dickson C, Barnes D and Peters G. Amplification and overexpression of cyclin D1 in breast cancer detected by immunohistochemical staining. Cancer research. 1994; 54:1812-1817.
28. Russell A, Thompson MA, Hendley J, Trute L, Armes J and Germain D. Cyclin D1 and D3 associate with the SCF complex and are coordinately elevated in breast cancer. Oncogene. 1999; 18:1983-1991.
29. Shimura T, Ochiai Y, Noma N, Oikawa T, Sano Y and Fukumoto M. Cyclin D1 overexpression perturbs DNA replication and induces replication-associated DNA double-strand breaks in acquired radioresistant cells. Cell cycle. 2013; 12:773-782.
30. Dulic V, Drullinger LF, Lees E, Reed SI and Stein GH. Altered regulation of G1 cyclins in senescent human diploid fibroblasts: accumulation of inactive cyclin E-Cdk2 and cyclin D1-Cdk2 complexes. Proceedings of the National Academy of Sciences of the United States of America. 1993; 90:11034-11038.
31. Leontieva OV, Lenzo F, Demidenko ZN and Blagosklonny MV. Hyper-mitogenic drive coexists with mitotic incompetence in senescent cells. Cell cycle. 2012; 11:4642-4649.
32. Shimura T, Toyoshima M, Adiga SK, Kunoh T, Nagai H, Shimizu N, Inoue M and Niwa O. Suppression of replication fork progression in low-dose-specific p53-dependent S-phase DNA damage checkpoint. Oncogene. 2006; 25:5921-5932.
33. Inaba Y, Koide S, Yokoyama K and Karube I. Development of urinary 8-hydroxy-2'-deoxyguanosine (8-OHdG) measurement method combined with SPE. Journal of chromatographic science. 2011; 49:303-309.
34. Moreno ML, Escobar J, Izquierdo-Alvarez A, Gil A, Perez S, Pereda J, Zapico I, Vento M, Sabater L, Marina A, Martinez-Ruiz A and Sastre J. Disulfide stress: a novel type of oxidative stress in acute pancreatitis. Free radical biology & medicine. 2014; 70:265-277.