Rapid inactivation and proteasome-mediated degradation of OGG1 contribute to the synergistic effect of hyperthermia on genotoxic treatments

DNA Repair

Volumn 12, Issue 3, 2013, Pages 227-237

  Fantini, Damiano ^a   Moritz, Eva ^b   Auvré, Frédéric ^a   Amouroux, Rachel ^a,c   Campalans, Anna ^a   Epe, Bernd ^b   Bravard, Anne ^a   Radicella, J Pablo ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Base excision repair; Chemosensitisation; CHIP E3 ligase; DNA glycosylases; Hyperthermia; OGG1; Ubiquitin

Indexed keywords

8 OXOGUANINE DNA GLYCOSYLASE; BINDING PROTEIN; CARBOXY TERMINUS OF HSC70 INTERACTING PROTEIN; DETERGENT; DNA GLYCOSYLTRANSFERASE; PROTEASOME; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL NUCLEUS; CHEMOSENSITIZATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INACTIVATION; ENZYME STABILITY; EXCISION REPAIR; GENOTOXICITY; HEAT SHOCK; HELA CELL; HYPERTHERMIA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; THERMAL EXPOSURE; UBIQUITINATION;

CELL NUCLEUS; CELL PROLIFERATION; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; ENZYME STABILITY; HEAT-SHOCK RESPONSE; HELA CELLS; HUMANS; PHOTOSENSITIZING AGENTS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN TRANSPORT; PROTEOLYSIS; PYRROLIDINES; QUINOLIZINES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84875366629     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2012.12.006     Document Type: Article

References (67)

1. Lindner L.H., Issels R.D. Hyperthermia in soft tissue sarcoma. Curr. Treat. Options Oncol. 2011, 12:12-20.
2. van der Zee J. Heating the patient: a promising approach?. Ann. Oncol. 2002, 13:1173-1184.
3. Wust P., Hildebrandt B., Sreenivasa G., Rau B., Gellermann J., Riess H., Felix R., Schlag P.M. Hyperthermia in combined treatment of cancer. Lancet Oncol. 2002, 3:487-497.
4. Gerashchenko B.I., Gooding G., Dynlacht J.R. Hyperthermia alters the interaction of proteins of the Mre11 complex in irradiated cells. Cytometry A 2010, 77A:940-952.
5. Krawczyk P.M., Eppink B., Essers J., Stap J., Rodermond H., Odijk H., Zelensky A., van Bree C., Stalpers L.J., Buist M.R., Soullie T., Rens J., Verhagen H.J.M., O'Connor M.J., Franken N.A.P., Hagen T.L.M., Kanaar R., Aten J.A. Mild hyperthermia inhibits homologous recombination, induces BRCA2 degradation, and sensitizes cancer cells to poly (ADP-ribose) polymerase-1 inhibition. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9851-9856.
6. Laszlo A., Fleischer I. Heat-induced perturbations of DNA damage signaling pathways are modulated by molecular chaperones. Cancer Res. 2009, 69:2042-2049.
7. Roti J.L.R. Cellular responses to hyperthermia (40-46°C): cell killing and molecular events. Int. J. Hyperthermia 2008, 24:3-15.
8. Cadet J., Douki T., Gasparutto D., Gromova M., Pouget J.P., Ravanat J.L., Romieu A., Sauvaigo S. Radiation-induced damage to DNA: mechanistic aspects and measurement of base lesions. Nucl. Instrum. Methods Phys. Res. B: Beam Interact. Mater. Atoms 1999, 151:1-7.
9. Fu D., Calvo J.A., Samson L.D. Balancing repair and tolerance of DNA damage caused by alkylating agents. Nat. Rev. Cancer 2012, 12:104-120.
10. Kampinga H.H., Dynlacht J.R., Dikomey E. Mechanism of radiosensitization by hyperthermia (≥43°C) as derived from studies with DNA repair defective mutant cell lines. Int. J. Hyperthermia 2004, 20:131-139.
11. Wallace S.S. Biological consequences of free radical-damaged DNA bases. Free Radic. Biol. Med. 2002, 33:1-14.
12. Tudek B. Imidazole ring-opened DNA purines and their biological significance. J. Biochem. Mol. Biol. 2003, 36:12-19.
13. Barnes D.E., Lindahl T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 2004, 38:445-476.
14. Batra V.K., Shock D.D., Beard W.A., McKenna C.E., Wilson S.H. Binary complex crystal structure of DNA polymerase beta reveals multiple conformations of the templating 8-oxoguanine lesion. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:113-118.
15. Hyun J.W., Jung Y.C., Kim H.S., Choi E.Y., Kim J.E., Yoon B.H., Yoon S.H., Lee Y.S., Choi J.H., You H.J., Chung H.M. 8-Hydroxydeoxyguanosine causes death of human leukemia cells deficient in 8-oxoguanine glyosylase 1 activity by inducing apoptosis. Mol. Cancer Res. 2003, 1:290-299.
16. Kitsera N., Stathis D., Luehnsdorf B., Mueller H., Carell T., Epe B., Khobta A. 8-Oxo-7,8-dihydroguanine in DNA does not constitute a barrier to transcription, but is converted into transcription-blocking damage by OGG1. Nucleic Acids Res. 2011, 39:5926-5934.
17. Choi S., Choi H.H., Choi J.-H., Yoon B.-H., You H.J., Hyun J.-W., Kim J.-E., Ye S.-K., Chung M.-H. Inhibitory effect of 8-oxo-7,8-dihydro-2'-deoxyguanosine on the growth of KG-1 myelosarcoma in Balb/c nude mice. Leuk. Res. 2006, 30:1425-1436.
18. Jacobs A.L., Schaer P. DNA glycosylases: in DNA repair and beyond. Chromosoma 2012, 121:1-20.
19. Lindahl T., Karran P., Wood R.D. DNA excision repair pathways. Curr. Opin. Genet. Dev. 1997, 7:158-169.
20. Adhikari S., Choudhury S., Mitra P.S., Dubash J.J., Sajankila S.P., Roy R. Targeting base excision repair for chemosensitization. Anti-Canc. Agents Med. Chem. 2008, 8:351-357.
21. Helleday T., Petermann E., Lundin C., Hodgson B., Sharma R.A. DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer 2008, 8:193-204.
22. Sharma R.A., Dianov G.L. Targeting base excision repair to improve cancer therapies. Mol. Aspects Med. 2007, 28:345-374.
23. Tell G., Wilson D.M. Targeting DNA repair proteins for cancer treatment. Cell. Mol. Life Sci. 2010, 67:3569-3572.
24. Abbotts R., Madhusudan S. Human AP endonuclease 1 (APE1): from mechanistic insights to druggable target in cancer. Cancer Treat. Rev. 2010, 36:425-435.
25. Wilson D.M., Simeonov A. Small molecule inhibitors of DNA repair nuclease activities of APE1. Cell. Mol. Life Sci. 2010, 67:3621-3631.
26. Sultana R., McNeill D.R., Abbotts R., Mohammed M.Z., Zdzienicka M.Z., Qutob H., Seedhouse C., Laughton C.A., Fischer P.M., Patel P.M., Wilson D.M., Madhusudan S. Synthetic lethal targeting of DNA double-strand break repair deficient cells by human apurinic/apyrimidinic endonuclease inhibitors. Int. J. Cancer 2012, 131:2433-2444.
27. Bryant H.E., Schultz N., Thomas H.D., Parker K.M., Flower D., Lopez E., Kyle S., Meuth M., Curtin N.J., Helleday T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
28. Barakat K., Gajewski M., Tuszynski J.A. DNA repair inhibitors: the next major step to improve cancer therapy. Curr. Top. Med. Chem. 2012, 12:1376-1390.
29. Jaiswal A.S., Banerjee S., Aneja R., Sarkar F.H., Ostrov D.A., Narayan S.C.e DNA polymerase beta as a novel target for chemotherapeutic intervention of colorectal cancer. PLoS ONE 2011, 6:e16691.
30. Wilson S.H., Beard W.A., Shock D.D., Batra V.K., Cavanaugh N.A., Prasad R., Hou E.W., Liu Y., Asagoshi K., Horton J.K., Stefanick D.F., Kedar P.S., Carrozza M.J., Masaoka A., Heacock M.L. Base excision repair and design of small molecule inhibitors of human DNA polymerase beta. Cell. Mol. Life Sci. 2010, 67:3633-3647.
31. Aburatani H., Hippo Y., Ishida T., Takashima R., Matsuba C., Kodama T., Takao M., Yasui A., Yamamoto K., Asano M. Cloning and characterization of mammalian 8-hydroxyguanine-specific DNA glycosylase/apurinic, apyrimidinic lyase, a functional mutM homologue. Cancer Res. 1997, 57:2151-2156.
32. Bjoras M., Luna L., Johnsen B., Hoff E., Haug T., Rognes T., Seeberg E. Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites. EMBO J. 1997, 16:6314-6322.
33. Radicella J.P., Dherin C., Desmaze C., Fox M.S., Boiteux S. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:8010-8015.
34. Roldan-Arjona T., Wei Y.F., Carter K.C., Klungland A., Anselmino C., Wang R.P., Augustus M., Lindahl T. Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:8016-8020.
35. Rosenquist T.A., Zharkov D.O., Grollman A.P. Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:7429-7434.
36. van der Kemp P.A., Thomas D., Barbey R., de Oliveira R., Boiteux S. Cloning and expression in Escherichia coli of the OGG1 gene of Saccharomyces cerevisiae, which codes for a DNA glycosylase that excises 7,8-dihydro-8-oxoguanine and 2,6-diamino-4-hydroxy-5-N-methylformamidopyrimidine. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:5197-5202.
37. Cussac C., Laval F. Reduction of the toxicity and mutagenicity of aziridine in mammalian cells harboring the Escherichia coli fpg gene. Nucleic Acids Res. 1996, 24:1742-1746.
38. Kobune M., Xu Y., Baum C., Kelley M.R., Williams D.A. Retrovirus-mediated expression of the base excision repair proteins, formamidopyrimidine DNA glycosylase or human oxoguanine DNA glycosylase, protects hematopoietic cells from N,N',N'-triethylenethiophosphoramide (thioTEPA)-induced toxicity in vitro and in vivo. Cancer Res. 2001, 61:5116-5125.
39. He Y.H., Xu Y., Kobune M., Wu M., Kelley M.R., Martin W.J. Escherichia coli FPG and human OGG1 reduce DNA damage and cytotoxicity by BCNU in human lung cells. Am. J. Physiol.: Lung Cell. Mol. Physiol. 2002, 282:L50-L55.
40. Preston T.J., Henderson J.T., McCallum G.P., Wells P.G. Base excision repair of reactive oxygen species-initiated 7,8-dihydro-8-oxo-2'-deoxyguanosine inhibits the cytotoxicity of platinum anticancer drugs. Mol. Cancer Ther. 2009, 8:2015-2026.
41. Obtulowicz T., Swoboda M., Speina E., Gackowski D., Rozalski R., Siomek A., Janik J., Janowska B., Ciesla J.M., Jawien A., Banaszkiewicz Z., Guz J., Dziaman T., Szpila A., Olinski R., Tudek B. Oxidative stress and 8-oxoguanine repair are enhanced in colon adenoma and carcinoma patients. Mutagenesis 2010, 25:463-471.
42. Saebo M., Skjelbred C.F., Nexo B.A., Wallin H., Hansteen I.-L., Vogel U., Kure E.H.C. Increased mRNA expression levels of ERCC1, OGG1 and RAI in colorectal adenomas and carcinomas. BMC Cancer 2006, 6.
43. Liddiard K., Hills R., Burnett A.K., Darley R.L., Tonks A. OGG1 is a novel prognostic indicator in acute myeloid leukaemia. Oncogene 2010, 29:2005-2012.
44. Batuello C.N., Kelley M.R., Dynlacht J.R. Role of Ape1 and base excision repair in the radioresponse and heat-radiosensitization of HeLa cells. Anticancer Res. 2009, 29:1319-1325.
45. Spiro I.J., Denman D.L., Dewey W.C. Effect of hyperthermia on CHO DNA-polymerases alpha and beta. Radiat. Res. 1982, 89:134-149.
46. Campalans A., Amouroux R., Bravard A., Epe B., Radicella J.P. UVA irradiation induces relocalisation of the DNA repair protein hOGG1 to nuclear speckles. J. Cell Sci. 2007, 120:23-32.
47. Bravard A., Vacher M., Moritz E., Vaslin L., Hall J., Epe B., Radicella J.P. Oxidation status of human OGG1-S326C polymorphic variant determines cellular DNA repair capacity. Cancer Res. 2009, 69:3642-3649.
48. Parsons J.L., Tait P.S., Finch D., Dianova I.I., Allinson S.L., Dianov G.L. CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol. Cell 2008, 29:477-487.
49. Choo Y.S., Zhang Z. Detection of protein ubiquitination. J. Vis. Exp. 2009.
50. Kohn K.W., Erickson L.C., Ewig R.A., Friedman C.A. Fractionation of DNA from mammalian cells by alkaline elution. Biochemistry 1976, 15:4629-4637.
51. Amouroux R., Campalans A., Epe B., Radicella J.P. Oxidative stress triggers the preferential assembly of base excision repair complexes on open chromatin regions. Nucleic Acids Res. 2010, 38:2878-2890.
52. Pflaum M., Will O., Epe B. Determination of steady-state levels of oxidative DNA base modifications in mammalian cells by means of repair endonucleases. Carcinogenesis 1997, 18:2225-2231.
53. Myerson R.J., Roti J.L.R., Moros E.G., Straube W.L., Xu M. Modelling heat-induced radiosensitization: clinical implications. Int. J. Hyperthermia 2004, 20:201-212.
54. Dai Q., Zhang C., Wu Y., McDonough H., Whaley R.A., Godfrey V., Li H.H., Madamanchi N., Xu W., Neckers L., Cyr D., Patterson C. CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J. 2003, 22:5446-5458.
55. Tripathi V., Ali A., Bhat R., Pati U. CHIP chaperones wild type p53 tumor suppressor protein. J. Biol. Chem. 2007, 282:28441-28454.
56. Anderson L.G., Meeker R.B., Poulton W.E., Huang D.Y. Brain distribution of carboxy terminus of Hsc70-interacting protein (CHIP) and its nuclear translocation in cultured cortical neurons following heat stress or oxygen-glucose deprivation. Cell Stress Chaperones 2010, 15:487-495.
57. Hirsch C., Gauss R., Sommer T. Coping with stress: cellular relaxation techniques. Trends Cell Biol. 2006, 16.
58. McDonough H., Patterson C. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones 2003, 8.
59. Bravard A., Vacher M., Gouget B., Coutant A., de Boisferon F.H., Marsin S., Chevillard S., Radicella J.P. Redox regulation of human OGG1 activity in response to cellular oxidative stress. Mol. Cell. Biol. 2006, 26:7430-7436.
60. Bravard A., Campalans A., Vacher M., Gouget B., Levalois C., Chevillard S., Radicella J.P. Inactivation by oxidation and recruitment into stress granules of hOGG1 but not APE1 in human cells exposed to sub-lethal concentrations of cadmium. Mutat. Res.: Fundam. Mol. Mech. Mutagen. 2010, 685:61-69.
61. Arslan M.A., Chikina M., Csermely P., Soti C. Misfolded proteins inhibit proliferation and promote stress-induced death in SV40-transformed mammalian cells. FASEB J. 2012, 26:766-777.
62. Zhang X., Qian S.-B. Chaperone-mediated hierarchical control in targeting misfolded proteins to aggresomes. Mol. Biol. Cell 2011, 22:3277-3288.
63. Schulz I., Mahler H.C., Boiteux S., Epe B. Oxidative DNA base damage induced by singlet oxygen and photosensitization: recognition by repair endonucleases and mutagenicity. Mutat. Res.: DNA Repair 2000, 461:145-156.
64. Will O., Gocke E., Eckert I., Schulz I., Pflaum M., Mahler H.C., Epe B. Oxidative DNA damage and mutations induced by a polar photosensitizer, Ro19-8022. Mutat. Res. 1999, 435:89-101.
65. Boiteux S., Radicella J.P. The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis. Arch. Biochem. Biophys. 2000, 377:1-8.
66. Powell S.N., Kachnic L.A. Homologous recombination research is heating up and ready for therapy. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9731-9732.
67. Hooten N.N., Kompaniez K., Barnes J., Lohani A., Evans M.K. Poly(ADP-ribose) polymerase 1 (PARP-1) binds to 8-oxoguanine-DNA glycosylase (OGG1). J. Biol. Chem. 2011, 286:44679-44690.