HMGA2 exhibits dRP/AP site cleavage activity and protects cancer cells from DNA-damage-induced cytotoxicity during chemotherapy

Nucleic Acids Research

Volumn 37, Issue 13, 2009, Pages 4371-4384

  Summer, Heike ^a   Li, Ou ^a   Bao, Qiuye ^a   Zhan, Lihong ^a   Peter, Sabrina ^a   Sathiyanathan, Padmapriya ^a   Henderson, Dana ^b   Klonisch, Thomas ^b   Goodman, Steven D ^c   Dröge, Peter ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b UNIVERSITY OF MANITOBA   (Canada)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' DEOXYRIBOSYLPHOSPHATE LYASE; CISPLATIN; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; HIGH MOBILITY GROUP A1A PROTEIN; HIGH MOBILITY GROUP A1B PROTEIN; HIGH MOBILITY GROUP A2 PROTEIN; HYDROXYUREA; LYASE; MESYLIC ACID; UNCLASSIFIED DRUG;

ARTICLE; AT HOOK MOTIF; BINDING AFFINITY; CANCER CELL; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DNA BINDING; DNA CLEAVAGE; DNA DAMAGE; ENZYME ACTIVITY; ENZYME SUBSTRATE; EXCISION REPAIR; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; AT-HOOK MOTIFS; CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; DRUG RESISTANCE, NEOPLASM; GENOME, HUMAN; HMGA2 PROTEIN; HUMANS; HYDROXYUREA; METHYL METHANESULFONATE; MUTAGENS; NEOPLASMS; PHOSPHORUS-OXYGEN LYASES;

EID: 67949109572     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp375     Document Type: Article

References (52)

1. Bustin,M. and Reeves,R. (1996) High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function. Prog. Nucleic Acid Res. Mol. Biol., 54, 35-100.
2. Reeves,R. (2001) Molecular biology of HMGA proteins: Hubs of nuclear function. Gene, 277, 63-81.
3. Cleynen,I. and van de Ven,W.J. (2008) The HMGA proteins: A myriad of functions (Review). Int. J. Oncol., 32, 289-305.
4. Huth,J.R., Bewley,C.A., Nissen,M.S., Evans,J.N., Reeves,R., Gronenborn,A.M. and Clore,G.M. (1997) The solution structure of an HMG-I(Y)-DNA complex defines a new architectural minor groove binding motif. Nat. Struct. Biol., 4, 657-665.
5. Zhou,X., Benson,K.F., Ashar,H.R. and Chada,K. (1995) Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature, 376, 771-774.
6. Hirning-Folz,U., Wilda,M., Rippe,V., Bullerdiek,J. and Hameister,H. (1998) The expression pattern of the Hmgic gene during development. Genes Chromosomes Cancer, 23, 350-357.
7. Chieffi,P., Battista,S., Barchi,M., Di Agostino,S., Pierantoni,G.M., Fedele,M., Chiariotti,L., Tramontano,D. and Fusco,A. (2002) HMGA1 and HMGA2 protein expression in mouse spermatogenesis. Oncogene, 21 3644-3650.
8. Caron,L., Bost,F., Prot,M., Hofman,P. and Binetruy,B. (2005) A new role for the oncogenic high-mobility group A2 transcription factor in myogenesis of embryonic stem cells. Oncogene, 24, 6281-6291.
9. Battista,S., Fidanza,V., Fedele,M., Klein-Szanto,A.J., Outwater,E., Brunner,H., Santoro,M., Croce,C.M. and Fusco,A. (1999) The expression of a truncated HMGI-C gene induces gigantism associated with lipomatosis. Cancer Res., 59, 4793-4797.
10. Zaidi,M.R., Okada,Y. and Chada,K.K. (2006) Misexpression of full-length HMGA2 induces benign mesenchymal tumors in mice. Cancer Res., 66, 7453-7459.
11. Gattas,G.J., Quade,B.J., Nowak,R.A. and Morton,C.C. (1999) HMGIC expression in human adult and fetal tissues and in uterine leiomyomata. Genes Chromosomes Cancer, 25, 316-322.
12. Li,O., Vasudevan,D., Davey,C.A. and Droge,P. (2006) High-level expression of DNA architectural factor HMGA2 and its association with nucleosomes in human embryonic stem cells. Genesis, 44, 523-529.
13. Li,O., Li,J. and Droge,P. (2007) DNA architectural factor and proto-oncogene HMGA2 regulates key developmental genes in pluripotent human embryonic stem cells. FEBS Lett., 581, 3533-3537.
14. Rogalla,P., Drechsler,K., Kazmierczak,B., Rippe,V., Bonk,U. and Bullerdiek,J. (1997) Expression of HMGI-C, a member of the high mobility group protein family, in a subset of breast cancers: Relationship to histologic grade. Mol. Carcinog., 19, 153-156.
15. Berner,J.M., Meza-Zepeda,L.A., Kools,P.F., Forus,A., Schoenmakers,E.F., Van de Ven,W.J., Fodstad,O. and Myklebost,O. (1997) HMGIC, the gene for an architectural transcription factor, is amplified and rearranged in a subset of human sarcomas. Oncogene, 14, 2935-2941.
16. Abe,N., Watanabe,T., Suzuki,Y., Matsumoto,N., Masaki,T., Mori,T., Sugiyama,M., Chiappetta,G., Fusco,A. and Atomi,Y. (2003) An increased high-mobility group A2 expression level is associated with malignant phenotype in pancreatic exocrine tissue. Br. J. Cancer, 89, 2104-2109.
17. Miyazawa,J., Mitoro,A., Kawashiri,S., Chada,K.K. and Imai,K. (2004) Expression of mesenchyme-specific gene HMGA2 in squamous cell carcinomas of the oral cavity. Cancer Res., 64, 2024-2029.
18. Meyer,B., Loeschke,S., Schultze,A., Weigel,T., Sandkamp,M., Goldmann,T., Vollmer,E. and Bullerdiek,J. (2007) HMGA2 overexpression in non-small cell lung cancer. Mol. Carcinog., 46, 503-511.
19. Subramanian,D. and Griffith,J.D. (2002) Interactions between p53, hMSH2-hMSH6 and HMG I(Y) on Holliday junctions and bulged bases. Nucleic Acids Res., 30, 2427-2434.
20. Fedele,M., Visone,R., De Martino,I., Troncone,G., Palmieri,D., Battista,S., Ciarmiello,A., Pallante,P., Arra,C., Melillo,R.M. et al. (2006) HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell, 9, 459-471.
21. Fusco,A. and Fedele,M. (2007) Roles of HMGA proteins in cancer. Nat. Rev. Cancer, 7, 899-910.
22. Tallini,G. and Dal Cin,P. (1999) HMGI(Y) and HMGI-C dysregulation: A common occurrence in human tumors. Adv. Anat. Pathol., 6, 237-246.
23. Di Cello,F., Hillion,J., Hristov,A., Wood,L.J., Mukherjee,M., Schuldenfrei,A., Kowalski,J., Bhattacharya,R., Ashfaq,R. and Resar,L.M. (2008) HMGA2 participates in transformation in human lung cancer. Mol. Cancer Res., 6, 743-750.
24. McMurray,H.R., Sampson,E.R., Compitello,G., Kinsey,C., Newman,L., Smith,B., Chen,S.R., Klebanov,L., Salzman,P., Yakovlev,A. et al. (2008) Synergistic response to oncogenic mutations defines gene class critical to cancer phenotype. Nature, 453, 1112-1116.
25. Mayr,C., Hemann,M.T. and Bartel,D.P. (2007) Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315, 1576-1579.
26. Hebert,C., Norris,K., Scheper,M.A., Nikitakis,N. and Sauk,J.J. (2007) High mobility group A2 is a target for miRNA-98 in head and neck squamous cell carcinoma. Mol. Cancer, 6, 5.
27. Yu,F., Yao,H., Zhu,P., Zhang,X., Pan,Q., Gong,C., Huang,Y., Hu,X., Su,F., Lieberman,J. et al. (2007) let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell, 131, 1109-1123.
28. Park,S.M., Shell,S., Radjabi,A.R., Schickel,R., Feig,C., Boyerinas,B., Dinulescu,D.M., Lengyel,E. and Peter,M.E. (2007) Let-7 prevents early cancer progression by suppressing expression of the embryonic gene HMGA2. Cell Cycle, 6, 2585-2590.
29. Droge,P. and Davey,C.A. (2008) Do cells let-7 determine stemness? Cell Stem Cell, 2, 8-9.
30. Liau,S.S. and Whang,E. (2008) HMGA1 is a molecular determinant of chemoresistance to gemcitabine in pancreatic adenocarcinoma. Clin. Cancer Res., 14, 1470-1477.
31. Prasad,R., Liu,Y., Deterding,L.J., Poltoratsky,V.P., Kedar,P.S., Horton,J.K., Kanno,S., Asagoshi,K., Hou,E.W., Khodyreva,S.N. et al. (2007) HMGB1 is a cofactor in mammalian base excision repair. Mol. Cell, 27, 829-841.
32. Singh,N.P., McCoy,M.T., Tice,R.R. and Schneider,E.L. (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res., 175, 184-191.
33. Olive,P.L., Banath,J.P. and Durand,R.E. (1990) Detection of etoposide resistance by measuring DNA damage in individual Chinese hamster cells. J. Natl Cancer Inst., 82, 779-783.
34. Verdine,G.L. and Norman,D.P. (2003) Covalent trapping of protein-DNA complexes. Annu. Rev. Biochem., 72, 337-366.
35. Liu,L. and Gerson,S.L. (2004) Therapeutic impact of methoxyamine: blocking repair of abasic sites in the base excision repair pathway. Curr. Opin. Investig. Drugs, 5, 623-627.
36. Sakano,K., Oikawa,S., Hasegawa,K. and Kawanishi,S. (2001) Hydroxyurea induces site-specific DNA damage via formation of hydrogen peroxide and nitric oxide. Jpn J. Cancer Res., 92, 1166-1174.
37. Wang,T.H., Popp,D.M., Wang,H.S., Saitoh,M., Mural,J.G., Henley,D.C., Ichijo,H. and Wimalasena,J. (1999) Microtubule dysfunction induced by paclitaxel initiates apoptosis through both c-Jun N-terminal kinase (JNK)-dependent and -independent pathways in ovarian cancer cells. J. Biol. Chem., 274, 8208-8216.
38. Boo,L.M., Lin,H.H., Chung,V., Zhou,B., Louie,S.G., O'Reilly,M.A., Yen,Y. and Ann,D.K. (2005) High mobility group A2 potentiates genotoxic stress in part through the modulation of basal and DNA damage-dependent phosphatidylinositol 3-kinase-related protein kinase activation. Cancer Res., 65, 6622-6630.
39. Sgarra,R., Furlan,C., Zammitti,S., Lo Sardo,A., Maurizio,E., Di Bernardo,J., Giancotti,V. and Manfioletti,G. (2008) Interaction proteomics of the HMGA chromatin architectural factors. Proteomics 8, 4721-4732.
40. Cattaruzzi,G., Altamura,S., Tessari,M.A., Rustighi,A., Giancotti,V., Pucillo,C. and Manfioletti,G. (2007) The second AT-hook of the architectural transcription factor HMGA2 is determinant for nuclear localization and function. Nucleic Acids Res., 35, 1751-1760.
41. Nakamura,J. and Swenberg,J.A. (1999) Endogenous apurinic/apyrimidinic sites in genomic DNA of mammalian tissue s. Cancer Res., 59, 2522-2526.
42. Sobol,R.W., Prasad,R., Evenski,A., Baker,A., Yang,X.P., Horton,J.K. and Wilson,S.H. (2000) The lyase activity of the DNA repair protein beta-polymerase protects from DNA-damage-induced cytotoxicity. Nature 405, 807-810.
43. Srivastava,D.K., Husain,I., Arteaga,C.L. and Wilson,S.H. (1999) DNA polymerase beta expression differences in selected human tumors and cell lines. Carcinogenesis, 20, 1049-1054.
44. Almeida,K.H. and Sobol,R.W. (2007) A unified view of base excision repair: Lesion-dependent protein complexes regulated by post-translational modification. DNA Rep., 6, 695-711.
45. Parsons,J.L., Tait,P.S., Finch,D., Dianova,II, Allinson,S.L. and Dianov,G.L. (2008) CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol. Cell, 29, 477-487.
46. Weinberger,M., Trabold,P.A., Lu,M., Sharma,K., Huberman,J.A. and Burhans,W.C. (1999) Induction by adozelesin and hydroxyurea of origin recognition complex-dependent DNA damage and DNA replication checkpoints in Saccharomyces cerevisiae. J. Biol. Chem., 274, 35975-35984.
47. Borrmann,L., Schwanbeck,R., Heyduk,T., Seebeck,B., Rogalla,P., Bullerdiek,J. and Wisniewski,J.R. (2003) High mobility group A2 protein and its derivatives bind a specific region of the promoter of DNA repair gene ERCC1 and modulate its activity. Nucleic Acids Res., 31 6841-6851.
48. Reeves,R. and Adair,J.E. (2005) Role of high mobility group (HMG) chromatin proteins in DNA repair. DNA Rep., 4, 926-938.
49. Loeb,L.A. and Preston,B.D. (1986) Mutagenesis by apurinic/apyrimidinic sites. Annu. Rev. Genet., 20, 201-230.
50. Saretzki,G., Walter,T., Atkinson,S., Passos,J.F., Bareth,B., Keith,W.N., Stewart,R., Hoare,S., Stojkovic,M., Armstrong,L. et al. (2008) Downregulation of multiple stress defense mechanisms during differentiation of human embryonic stem cells. Stem Cells, 26 455-464.
51. Ding,J., Miao,Z.H., Meng,L.H. and Geng,M.Y. (2006) Emerging cancer therapeutic opportunities target DNA-repair systems. Trends Pharmacol. Sci., 27, 338-344.
52. Matsuoka,S., Ballif,B.A., Smogorzewska,A., McDonald,E.R. 3rd, Hurov,K.E., Luo,J., Bakalarski,C.E., Zhao,Z., Solimini,N., Lerenthal,Y. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316, 1160-1166.