Functional activation of ATM by the prostate cancer suppressor NKX3.1

Cell Reports

Volumn 4, Issue 3, 2013, Pages 516-529

  Bowen, Cai ^a   Ju, Jeong Ho ^a   Lee, Ji Hoon ^b   Paull, TanyaT ^b   Gelmann, EdwardP ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; HISTONE H2AX; PROTEIN NKX3.1; PROTEIN P53; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CANCER CELL; CANCER STEM CELL; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL STRAIN LNCAP; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA INTEGRATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; IN VITRO STUDY; MISSENSE MUTATION; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

ATAXIA TELANGIECTASIA;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE, TUMOR; DNA DAMAGE; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; HUMANS; MALE; PHOSPHORYLATION; PROSTATIC NEOPLASMS; TRANSCRIPTION FACTORS;

EID: 84881614943     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.06.039     Document Type: Article

References (51)

1. Asatiani E., Huang W.X., Wang A., Rodriguez Ortner E., Cavalli L.R., Haddad B.R., Gelmann E.P. Deletion, methylation, and expression of the NKX3.1 suppressor gene in primary human prostate cancer. Cancer Res. 2005, 65:1164-1173.
2. Bakkenist C.J., Kastan M.B. DNA damage activates ATM throughintermolecular autophosphorylation and dimer dissociation. Nature 2003, 421:499-506.
3. Bartek J., Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 2003, 3:421-429.
4. Bekker-Jensen S., Lukas C., Kitagawa R., Melander F., Kastan M.B., Bartek J., Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J.Cell Biol. 2006, 173:195-206.
5. Bethel C.R., Faith D., Li X., Guan B., Hicks J.L., Lan F., Jenkins R.B., Bieberich C.J., De Marzo A.M. Decreased NKX3.1 protein expression in focal prostatic atrophy, prostatic intraepithelial neoplasia, and adenocarcinoma: association with gleason score and chromosome 8p deletion. Cancer Res. 2006, 66:10683-10690.
6. Bhaskara V., Dupré A., Lengsfeld B., Hopkins B.B., Chan A., Lee J.H., Zhang X., Gautier J., Zakian V., Paull T.T. Rad50 adenylate kinase activity regulates DNA tethering by Mre11/Rad50 complexes. Mol. Cell 2007, 25:647-661.
7. Bowen C., Gelmann E.P. NKX3.1 activates cellular response to DNA damage. Cancer Res. 2010, 70:3089-3097.
8. Bowen C., Bubendorf L., Voeller H.J., Slack R., Willi N., Sauter G., Gasser T.C., Koivisto P., Lack E.E., Kononen J., et al. Loss of NKX3.1 expression in human prostate cancers correlates with tumor progression. Cancer Res. 2000, 60:6111-6115.
9. Bowen C., Stuart A., Ju J.H., Tuan J., Blonder J., Conrads T.P., Veenstra T.D., Gelmann E.P. NKX3.1 homeodomain protein binds to topoisomerase I and enhances its activity. Cancer Res. 2007, 67:455-464.
10. Chou W.C., Wang H.C., Wong F.H., Ding S.L., Wu P.E., Shieh S.Y., Shen C.Y. Chk2-dependent phosphorylation of XRCC1 in the DNA damage response promotes base excision repair. EMBO J. 2008, 27:3140-3150.
11. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
12. Daniel J.A., Pellegrini M., Lee J.H., Paull T.T., Feigenbaum L., Nussenzweig A. Multiple autophosphorylation sites are dispensable for murine ATM activation invivo. J.Cell Biol. 2008, 183:777-783.
13. Ditch S., Paull T.T. The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem. Sci. 2011, 37:15-22.
14. Fernandez-Capetillo O., Lee A., Nussenzweig M., Nussenzweig A. H2AX: the histone guardian of the genome. DNA Repair (Amst.) 2004, 3:959-967.
15. Gelmann E.P., Steadman D.J., Ma J., Ahronovitz N., Voeller H.J., Swope S., Abbaszadegan M., Brown K.M., Strand K., Hayes R.B., Stampfer M.J. Occurrence of NKX3.1 C154T polymorphism in men with and without prostate cancer and studies of its effect on protein function. Cancer Res. 2002, 62:2654-2659.
16. Germann M., Wetterwald A., Guzmán-Ramirez N., van der Pluijm G., Culig Z., Cecchini M.G., Williams E.D., Thalmann G.N. Stem-like cells with luminal progenitor phenotype survive castration in human prostate cancer. Stem Cells 2012, 30:1076-1086.
17. Grollman A.P., Moriya M. Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet. 1993, 9:246-249.
18. Guo Z., Deshpande R., Paull T.T. ATM activation in the presence of oxidative stress. Cell Cycle 2010, 9:4805-4811.
19. Guo Z., Kozlov S., Lavin M.F., Person M.D., Paull T.T. ATM activation by oxidative stress. Science 2010, 330:517-521.
20. He H.H., Meyer C.A., Shin H., Bailey S.T., Wei G., Wang Q., Zhang Y., Xu K., Ni M., Lupien M., et al. Nucleosome dynamics define transcriptional enhancers. Nat. Genet. 2010, 42:343-347.
21. Huang X., King M.A., Halicka H.D., Traganos F., Okafuji M., Darzynkiewicz Z. Histone H2AX phosphorylation induced by selective photolysis of BrdU-labeled DNA with UV light: relation to cell cycle phase. Cytometry A 2004, 62:1-7.
22. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
23. Khalil A., Morgan R.N., Adams B.R., Golding S.E., Dever S.M., Rosenberg E., Povirk L.F., Valerie K. ATM-dependent ERK signaling via AKT in response to DNA double-strand breaks. Cell Cycle 2011, 10:481-491.
24. Khalili M., Mutton L.N., Gurel B., Hicks J.L., De Marzo A.M., Bieberich C.J. Loss of Nkx3.1 expression in bacterial prostatitis: a potential link between inflammation and neoplasia. Am. J. Pathol. 2010, 176:2259-2268.
25. Khanna K.K., Keating K.E., Kozlov S., Scott S., Gatei M., Hobson K., Taya Y., Gabrielli B., Chan D., Lees-Miller S.P., Lavin M.F. ATM associates with and phosphorylates p53: mapping the region of interaction. Nat. Genet. 1998, 20:398-400.
26. Kurz E.U., Lees-Miller S.P. DNA damage-induced activation ofATM and ATM-dependent signaling pathways. DNA Repair (Amst.) 2004, 3:889-900.
27. Lee J.H., Paull T.T. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 2004, 304:93-96.
28. Lee J.H., Paull T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 2005, 308:551-554.
29. Lee J.H., Paull T.T. Purification and biochemical characterization of ataxia-telangiectasia mutated and Mre11/Rad50/Nbs1. Methods Enzymol. 2006, 408:529-539.
30. Li X., Guan B., Maghami S., Bieberich C.J. NKX3.1 is regulated by protein kinase CK2 in prostate tumor cells. Mol. Cell. Biol. 2006, 26:3008-3017.
31. Limoli C.L., Ward J.F. A new method for introducing double-strand breaks into cellular DNA. Radiat. Res. 1993, 134:160-169.
32. Lin X., Tascilar M., Lee W.H., Vles W.J., Lee B.H., Veeraswamy R., Asgari K., Freije D., van Rees B., Gage W.R., et al. GSTP1 CpG island hypermethylation is responsible for the absence of GSTP1 expression in human prostate cancer cells. Am. J. Pathol. 2001, 159:1815-1826.
33. Lin C., Yang L., Tanasa B., Hutt K., Ju B.G., Ohgi K., Zhang J., Rose D.W., Fu X.D., Glass C.K., Rosenfeld M.G. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 2009, 139:1069-1083.
34. Mani R.S., Tomlins S.A., Callahan K., Ghosh A., Nyati M.K., Varambally S., Palanisamy N., Chinnaiyan A.M. Induced chromosomal proximity and gene fusions in prostate cancer. Science 2009, 326:1230.
35. Markowski M.C., Bowen C., Gelmann E.P. Inflammatory cytokines induce phosphorylation and ubiquitination of prostate suppressor protein NKX3.1. Cancer Res. 2008, 68:6896-6901.
36. Miao Z.H., Player A., Shankavaram U., Wang Y.H., Zimonjic D.B., Lorenzi P.L., Liao Z.Y., Liu H., Shimura T., Zhang H.L., et al. Nonclassic functions of human topoisomerase I: genome-wide and pharmacologic analyses. Cancer Res. 2007, 67:8752-8761.
37. Murata M., Thanan R., Ma N., Kawanishi S. Role of nitrative and oxidative DNA damage in inflammation-related carcinogenesis. J.Biomed. Biotechnol. 2012, 2012:623019.
38. Nelson W.G., De Marzo A.M., Isaacs W.B. Prostate cancer. N.Engl. J. Med. 2003, 349:366-381.
39. Nupponen N.N., Wallén M.J., Ponciano D., Robbins C.M., Tammela T.L., Vessella R.L., Carpten J.D., Visakorpi T. Mutational analysis of susceptibility genes RNASEL/HPC1, ELAC2/HPC2, and MSR1 in sporadic prostate cancer. Genes Chromosomes Cancer 2004, 39:119-125.
40. Ouyang X., DeWeese T.L., Nelson W.G., Abate-Shen C. Loss-of-function of Nkx3.1 promotes increased oxidative damage in prostate carcinogenesis. Cancer Res. 2005, 65:6773-6779.
41. Parlanti E., Fortini P., Macpherson P., Laval J., Dogliotti E. Base excision repair of adenine/8-oxoguanine mispairs by an aphidicolin-sensitive DNA polymerase in human cell extracts. Oncogene 2002, 21:5204-5212.
42. Pascucci B., Maga G., Hübscher U., Bjoras M., Seeberg E., Hickson I.D., Villani G., Giordano C., Cellai L., Dogliotti E. Reconstitution of the base excision repair pathway for 7,8-dihydro-8-oxoguanine with purified human proteins. Nucleic Acids Res. 2002, 30:2124-2130.
43. Paull T.T., Lee J.H. The Mre11/Rad50/Nbs1 complex and its role as a DNA double-strand break sensor for ATM. Cell Cycle 2005, 4:737-740.
44. Pollack A., Zagars G.K. External beam radiotherapy dose response of prostate cancer. Int. J. Radiat. Oncol. Biol. Phys. 1997, 39:1011-1018.
45. Pollack A., Zagars G.K., Smith L.G., Lee J.J., von Eschenbach A.C., Antolak J.A., Starkschall G., Rosen I. Preliminary results of a randomized radiotherapy dose-escalation study comparing 70Gy with 78Gy for prostate cancer. J.Clin. Oncol. 2000, 18:3904-3911.
46. Rouet P., Smih F., Jasin M. Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell. Biol. 1994, 14:8096-8106.
47. Seppälä E.H., Ikonen T., Autio V., Rökman A., Mononen N., Matikainen M.P., Tammela T.L., Schleutker J. Germ-line alterations in MSR1 gene and prostate cancer risk. Clin. Cancer Res. 2003, 9:5252-5256.
48. Shen M.M., Abate-Shen C. Molecular genetics of prostate cancer: new prospects for old challenges. Genes Dev. 2010, 24:1967-2000.
49. Tan P.Y., Chang C.W., Chng K.R., Wansa K.D., Sung W.K., Cheung E. Integration of regulatory networks by NKX3-1 promotes androgen-dependent prostate cancer survival. Mol. Cell. Biol. 2012, 32:399-414.
50. Tomlins S.A., Rhodes D.R., Perner S., Dhanasekaran S.M., Mehra R., Sun X.W., Varambally S., Cao X., Tchinda J., Kuefer R., et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005, 310:644-648.
51. Wang L., McDonnell S.K., Cunningham J.M., Hebbring S., Jacobsen S.J., Cerhan J.R., Slager S.L., Blute M.L., Schaid D.J., Thibodeau S.N. No association of germline alteration of MSR1 with prostate cancer risk. Nat. Genet. 2003, 35:128-129.