Regulator of G protein signaling 6 mediates doxorubicin-induced ATM and p53 activation by a reactive oxygen species-dependent mechanism

Cancer Research

Volumn 71, Issue 20, 2011, Pages 6310-6319

  Huang, Jie ^a   Yang, Jianqi ^a   Maity, Biswanath ^a   Mayuzumi, Daisuke ^a   Fisher, Rory A ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; PROTEIN P53; REACTIVE OXYGEN METABOLITE; RGS PROTEIN; RGS6 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATAXIA TELANGIECTASIA; CANCER CELL; CELL DEATH; CONTROLLED STUDY; DNA DAMAGE; DRUG MECHANISM; DRUG TARGETING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE PROTEINS; DNA-BINDING PROTEINS; DOXORUBICIN; FIBROBLASTS; MICE; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; RGS PROTEINS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 80054030854     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3397     Document Type: Article

References (36)

1. Carter SK. Adriamycin-a review. J Natl Cancer Inst 1975;55:1265-74.
2. Capranico G, Zunino F. DNA topoisomerase-trapping antitumour drugs. Eur J Cancer 1992;28A:2055-60.
3. Tewey KM, Rowe TC, Yang L, Halligan BD, Liu LF. Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II. Science 1984;226:466-8. (Pubitemid 14012819)
4. Lown JW, Sim SK, Majumdar KC, Chang RY. Strand scission of DNA by bound adriamycin and daunorubicin in the presence of reducing agents. Biochem Biophys Res Commun 1977;76:705-10. (Pubitemid 8130857)
5. Evan G, Littlewood T. A matter of life and cell death. Science 1998;281:1317-22. (Pubitemid 28406818)
6. Iliakis G, Wang Y, Guan J, Wang H. DNA damage checkpoint control in cells exposed to ionizing radiation. Oncogene 2003;22:5834-47. (Pubitemid 37176704)
7. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 1998;281:1677-9. (Pubitemid 28435584)
8. Khanna KK, Keating KE, Kozlov S, Scott S, Gatei M, Hobson K, et al. ATM associates with and phosphorylates p53: mapping the region of interaction. Nat Genet 1998;20:398-400. (Pubitemid 28541643)
9. Maya R, Balass M, Kim ST, Shkedy D, Leal JF, Shifman O, et al. ATM-dependent phosphorylation of Mdm2 on serine 395: role in p53 activation by DNA damage. Genes Dev 2001;15:1067-77. (Pubitemid 32417300)
10. Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 1993;362:847-9. (Pubitemid 23132161)
11. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Molecular cell 2010;40:179-204.
12. Dohlman HG, Thorner J. RGS proteins and signaling by heterotrimeric G proteins. J Biol Chem 1997;272:3871-4. (Pubitemid 27078439)
13. Berman DM, Gilman AG. Mammalian RGS proteins: barbarians at the gate. J Biol Chem 1998;273:1269-72. (Pubitemid 28133638)
14. Ross EM, Wilkie TM. GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu Rev Biochem 2000;69:795-827.
15. Berman DM, Wang Y, Liu Z, Dong Q, Burke LA, Liotta LA, et al. A functional polymorphism in RGS6 modulates the risk of bladder cancer. Cancer Res 2004;64:6820-6. (Pubitemid 39297947)
16. Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature 2009;461:1071-8.
17. Maity B, Yang J, Huang J, Askeland RW, Bera S, Fisher RA. Regulator of G protein signaling 6 (RGS6) induces apoptosis via a mitochondrial-dependent pathway not involving its GTPase-activating protein activity. J Biol Chem 2010;286:1409-19.
18. Guo Z, Kozlov S, Lavin MF, Person MD, Paull TT. ATM activation by oxidative stress. Science 2010;330:517-21.
19. Chatterjee TK, Liu Z, Fisher RA. Human RGS6 gene structure, complex alternative splicing, and role of N terminus and G protein gammasubunit-like (GGL) domain in subcellular localization of RGS6 splice variants. J Biol Chem 2003;278:30261-71. (Pubitemid 36962420)
20. Yang J, Huang J, Maity B, Gao Z, Lorca RA, Gudmundsson H, et al. RGS6, a modulator of parasympathetic activation in heart. Circ Res 2010;107:1345-9.
21. Gopinath S, Vanamala SK, Gujrati M, Klopfenstein JD, Dinh DH, Rao JS. Doxorubicin-mediated apoptosis in glioma cells requires NFAT3. Cell Mol Life Sci 2009;66:3967-78.
22. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003;421:499-506. (Pubitemid 36168436)
23. Martemyanov KA, Yoo PJ, Skiba NP, Arshavsky VY. R7BP, a novel neuronal protein interacting with RGS proteins of the R7 family. J Biol Chem 2005;280:5133-6. (Pubitemid 40279981)
24. Cabrera JL, de Freitas F, Satpaev DK, Slepak VZ. Identification of the Gbeta5-RGS7 protein complex in the retina. Biochem Biophys Res Commun 1998;249:898-902. (Pubitemid 28441935)
25. Liu Z, Chatterjee TK, Fisher RA. RGS6 interacts with SCG10 and promotes neuronal differentiation. Role of the G gamma subunit-like (GGL) domain of RGS6. J Biol Chem 2002;277:37832-9.
26. Shieh SY, Ikeda M, Taya Y, Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 1997;91:325-34. (Pubitemid 27467963)
27. Siliciano JD, Canman CE, Taya Y, Sakaguchi K, Appella E, Kastan MB. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev 1997;11:3471-81. (Pubitemid 28023968)
28. Khosravi R, Maya R, Gottlieb T, Oren M, Shiloh Y, Shkedy D. Rapid ATM-dependent phosphorylation of MDM2 precedes p53 accumulation in response to DNA damage. Proc Natl Acad Sci U S A 1999;96:14973-7. (Pubitemid 30019749)
29. Rojas E, Lopez MC, Valverde M. Single cell gel electrophoresis assay: methodology and applications. J Chromatogr B Biomed Sci Appl 1999;722:225-54. (Pubitemid 29142512)
30. Kurz EU, Douglas P, Lees-Miller SP. Doxorubicin activates ATM-dependent phosphorylation of multiple downstream targets in part through the generation of reactive oxygen species. J Biol Chem 2004;279:53272-81. (Pubitemid 40051831)
31. Yoshida M, Shiojima I, Ikeda H, Komuro I. Chronic doxorubicin cardiotoxicity is mediated by oxidative DNA damage-ATM-p53-apoptosis pathway and attenuated by pitavastatin through the inhibition of Rac1 activity. J Mol Cell Cardiol 2009;47:698-705.
32. Zhu W, Soonpaa MH, Chen H, Shen W, Payne RM, Liechty EA, et al. Acute doxorubicin cardiotoxicity is associated with p53-induced inhibition of the mammalian target of rapamycin pathway. Circulation 2009;119:99-106.
33. Shizukuda Y, Matoba S, Mian OY, Nguyen T, Hwang PM. Targeted disruption of p53 attenuates doxorubicin-induced cardiac toxicity in mice. Mol Cell Biochem 2005;273:25-32. (Pubitemid 40774760)
34. Liu X, Chua CC, Gao J, Chen Z, Landy CL, Hamdy R, et al. Pifithrinalpha protects against doxorubicin-induced apoptosis and acute cardiotoxicity in mice. Am J Physiol Heart Circ Physiol 2004;286:H933-9. (Pubitemid 38248606)
35. Zheng B, De Vries L, Gist Farquhar M. Divergence of RGS proteins: evidence for the existence of six mammalian RGS subfamilies. Trends Biochem Sci 1999;24:411-4. (Pubitemid 29528196)
36. Cheever ML, Snyder JT, Gershburg S, Siderovski DP, Harden TK, Sondek J. Crystal structure of the multifunctional Gbeta5-RGS9 complex. Nat Struct Mol Biol 2008;15:155-62. (Pubitemid 351227317)