Local depletion of DNA methylation identifies a repressive p53 regulatory region in the NEK2 promoter

Journal of Biological Chemistry

Volumn 288, Issue 50, 2013, Pages 35940-35951

  Nabilsi, Nancy H ^a   Ryder, Daniel J ^b   Peraza Penton, Ashley C ^a   Poudyal, Rosha ^a   Loose, David S ^c   Kladde, Michael P ^a  

^a UNIVERSITY OF FLORIDA HEALTH   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE-SEQUENCING; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; ECTOPIC EXPRESSIONS; EPIGENETIC REGULATION; METHYLTRANSFERASES; PROMOTER ACTIVITIES; TRANSCRIPTIONAL REPRESSION;

ALKYLATION;

GENES;

5 AZA 2' DEOXYCYTIDINE; BISULFITE; DOXORUBICIN; METHYLTRANSFERASE; MICROCOCCAL NUCLEASE; MUTANT PROTEIN; PHOSPHOTRANSFERASE; PROTEIN NEK2; PROTEIN P53; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL STRAIN HCT116; CHROMATIN STRUCTURE; COLON CANCER; CONTROLLED STUDY; DEMETHYLATION; DNA DAMAGE; DNA FOOTPRINTING; DNA METHYLATION; DNA SEQUENCE; DNA TEMPLATE; DRUG MECHANISM; GENE; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NEK2 GENE; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN STABILITY; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

CHROMATIN REGULATION; CHROMATIN STRUCTURE; DNA METHYLATION; EPIGENETICS; MAPIT; NEK2; NUCLEOSOME; P53;

AZACITIDINE; BASE SEQUENCE; BINDING SITES; CELL CYCLE; CELL PROLIFERATION; DNA; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; HCT116 CELLS; HUMANS; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84890318401     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.523837     Document Type: Article

References (58)

1. Bird, A. (2002) DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21
2. Hon, G. C., Hawkins, R. D., Caballero, O. L., Lo, C., Lister, R., Pelizzola, M., Valsesia, A., Ye, Z., Kuan, S., Edsall, L. E., Camargo, A. A, Stevenson, B. J., Ecker, J. R., Bafna, V., Strausberg, R. L., Simpson, A. J., and Ren, B. (2012) Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer. Genome Res. 22, 246-258
3. Hellman, A., and Chess, A. (2007) Gene body-specific methylation on the active X chromosome. Science 315, 1141-1143
4. Ball, M. P., Li, J. B., Gao, Y., Lee, J. H., LeProust, E. M., Park, I. H., Xie, B., Daley, G. Q., and Church, G. M. (2009) Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat. Biotechnol. 27, 361-368
5. Wu, H., Coskun, V., Tao, J., Xie, W., Ge, W., Yoshikawa, K., Li, E., Zhang, Y., and Sun, Y. E. (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329, 444-448
6. Barletta, J. M., Rainier, S., and Feinberg, A. P. (1997) Reversal of loss of imprinting in tumor cells by 5-aza-2′-deoxycytidine. Cancer Res. 57, 48-50
7. Renaud, S., Loukinov, D., Abdullaev, Z., Guilleret, I., Bosman, F. T., Lobanenkov, V., and Benhattar, J. (2007) Dual role of DNA methylation inside and outside of CTCF-binding regions in the transcriptional regulation of the telomerase hTERT gene. Nucleic Acids Res. 35, 1245-1256
8. Nabilsi, N. H., Broaddus, R. R., and Loose, D. S. (2009) DNA methylation inhibits p53-mediated survivin repression. Oncogene 28, 2046-2050
9. Lai, A. Y., Fatemi, M., Dhasarathy, A., Malone, C., Sobol, S. E., Geigerman, C., Jaye, D. L., Mav, D., Shah, R., Li, L., and Wade, P. A. (2010) DNA methylation prevents CTCF-mediated silencing of the oncogene BCL6 in B cell lymphomas. J. Exp. Med. 207, 1939-1950
10. Hayward, D. G., and Fry, A. M. (2006) NEK2 kinase in chromosome instability and cancer. Cancer Lett. 237, 155-166
11. Kokuryo, T., Senga, T., Yokoyama, Y., Nagino, M., Nimura, Y., and Hamaguchi, M. (2007) NEK2 as an effective target for inhibition of tumorigenic growth and peritoneal dissemination of cholangiocarcinoma. Cancer Res. 67, 9637-9642
12. Barbagallo, F., Paronetto, M. P., Franco, R., Chieffi, P., Dolci, S., Fry, A. M., Geremia, R., and Sette, C. (2009) Increased expression and nuclear localization of the centrosomal kinase NEK2 in human testicular seminomas. J. Pathol. 217, 431-441
13. Brendle, A., Brandt, A., Johansson, R., Enquist, K., Hallmans, G., Hemminki, K., Lenner, P., and Försti, A. (2009) Single nucleotide polymorphisms in chromosomal instability genes and risk and clinical outcome of breast cancer: a Swedish prospective case-control study. Eur. J. Cancer 45, 435-442
14. Wu, G., Qiu, X. L., Zhou, L., Zhu, J., Chamberlin, R., Lau, J., Chen, P. L., and Lee, W. H. (2008) Small molecule targeting the Hec1/NEK2 mitotic pathway suppresses tumor cell growth in culture and in animal. Cancer Res. 68, 8393-8399
15. Qiu, X. L., Li, G., Wu, G., Zhu, J., Zhou, L., Chen, P. L., Chamberlin, A. R., and Lee, W. H. (2009) Synthesis and biological evaluation of a series of novel inhibitor of NEK2/Hec1 analogues. J. Med. Chem. 52, 1757-1767
16. Schultz, S. J., Fry, A. M., Sütterlin, C., Ried, T., and Nigg, E. A. (1994) Cell cycle-dependent expression of NEK2, a novel human protein kinase related to the NIMA mitotic regulator of Aspergillus nidulans. Cell Growth Differ. 5, 625-635
17. Iyer, V. R., Eisen, M. B., Ross, D. T., Schuler, G., Moore, T., Lee, J. C., Trent, J. M., Staudt, L. M., Hudson, J., Jr., Boguski, M. S., Lashkari, D., Shalon, D., Botstein, D., and Brown, P. O. (1999) The transcriptional program in the response of human fibroblasts to serum. Science 283, 83-87
18. Fry, A. M. (2002) The NEK2 protein kinase: a novel regulator of centrosome structure. Oncogene 21, 6184-6194
19. 2/M checkpoints. Genes Dev. 16, 245-256
20. Whitfield, M. L., Sherlock, G., Saldanha, A. J., Murray, J. I., Ball, C. A., Alexander, K. E., Matese, J. C., Perou, C. M., Hurt, M. M., Brown, P. O., and Botstein, D. (2002) Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol. Biol. Cell 13, 1977-2000
21. Laoukili, J., Kooistra, M. R., Brás, A., Kauw, J., Kerkhoven, R. M., Morrison, A., Clevers, H., and Medema, R. H. (2005) FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat. Cell Biol. 7, 126-136
22. Xie, R., Loose, D. S., Shipley, G. L., Xie, S., Bassett, R. L., Jr., and Broaddus, R. R. (2007) Hypomethylation-induced expression of S100A4 in endometrial carcinoma. Mod. Pathol. 20, 1045-1054
23. Jain, A. K., Allton, K., Iacovino, M., Mahen, E., Milczarek, R. J., Zwaka, T. P., Kyba, M., and Barton, M. C. (2012) p53 regulates cell cycle and microRNAs to promote differentiation of human embryonic stem cells. PLoS Biol. 10, e1001268
24. Pardo, C. E., Darst, R. P., Nabilsi, N. H., Delmas, A. L., and Kladde, M. P. (2011) Simultaneous single-molecule mapping of protein-DNA interactions and DNA methylation by MAPit. Curr. Protoc. Mol. Biol. Chapter 21, Unit 21.22
25. Pardo, C. E., Carr, I. M., Hoffman, C. J., Darst, R. P., Markham, A. F., Bonthron, D. T., and Kladde, M. P. (2011) MethylViewer: computational analysis and editing for bisulfite sequencing and methyltransferase accessibility protocol for individual templates (MAPit) projects. Nucleic Acids Res. 39, e5
26. Darst, R. P., Nabilsi, N. H., Pardo, C. E., Riva, A., and Kladde, M. P. (2012) DNA methyltransferase accessibility protocol for individual templates by deep sequencing. Methods Enzymol. 513, 185-204
27. Demircan, B., Dyer, L. M., Gerace, M., Lobenhofer, E. K., Robertson, K. D., and Brown, K. D. (2009) Comparative epigenomics of human and mouse mammary tumors. Genes Chromosomes Cancer 48, 83-97
28. Cui, K., and Zhao, K. (2012) Genome-wide approaches to determining nucleosome occupancy in metazoans using MNase-Seq. Methods Mol. Biol. 833, 413-419
29. Nabilsi, N. H., Broaddus, R. R., McCampbell, A. S., Lu, K. H., Lynch, H. T., Chen, L. M., and Loose, D. S. (2010) Sex hormone regulation of survivin gene expression. J. Endocrinol. 207, 237-243
30. Frommer, M., McDonald, L. E., Millar, D. S., Collis, C. M., Watt, F., Grigg, G. W., Molloy, P. L., and Paul, C. L. (1992)Agenomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sci. U.S.A. 89, 1827-1831
31. Stadler, M. B., Murr, R., Burger, L., Ivanek, R., Lienert, F., Schöler, A., van Nimwegen, E., Wirbelauer, C., Oakeley, E. J., Gaidatzis, D., Tiwari, V. K, and Schübeler, D. (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480, 490-495
32. Lienert, F., Wirbelauer, C., Som, I., Dean, A., Mohn, F., and Schübeler, D. (2011) Identification of genetic elements that autonomously determine DNA methylation states. Nat. Genet. 43, 1091-1097
33. Riley, T., Sontag, E., Chen, P., and Levine, A. (2008) Transcriptional control of human p53-regulated genes. Nat. Rev. Mol. Cell Biol. 9, 402-412
34. Feng, Z., Jin, S., Zupnick, A., Hoh, J., de Stanchina, E., Lowe, S., Prives, C., and Levine, A. J. (2006) p53 tumor suppressor protein regulates the levels of huntingtin gene expression. Oncogene 25, 1-7
35. Lin, J. C., Jeong, S., Liang, G., Takai, D., Fatemi, M., Tsai, Y. C., Egger, G., Gal-Yam, E. N., and Jones, P. A. (2007) Role of nucleosomal occupancy in the epigenetic silencing of the MLH1 CpG island. Cancer Cell 12, 432-444
36. Kilgore, J. A., Hoose, S. A., Gustafson, T. L., Porter, W., and Kladde, M. P. (2007) Single-molecule and population probing of chromatin structure using DNA methyltransferases. Methods 41, 320-332
37. Xu, M., Kladde, M. P., Van Etten, J. L., and Simpson, R. T. (1998) Cloning, characterization and expression of the gene coding for a cytosine-5-DNA methyltransferase recognizing GpC. Nucleic Acids Res. 26, 3961-3966
38. Yang, F., Kemp, C. J., and Henikoff, S. (2013) Doxorubicin enhances nucleosome turnover around promoters. Curr. Biol. 23, 782-787
39. WAF1 is component of a positive feedback loop that maintains the p53 transcriptional program. Cell Cycle 10, 932-950
40. Broude, E. V., Demidenko, Z. N., Vivo, C., Swift, M. E., Davis, B. M., Blagosklonny, M. V., and Roninson, I. B. (2007) p21 (CDKN1A) is a negative regulator of p53 stability. Cell Cycle 6, 1468-1471
41. Troester, M. A., Herschkowitz, J. I., Oh, D. S., He, X., Hoadley, K. A., Barbier, C. S., and Perou, C. M. (2006) Gene expression patterns associated with p53 status in breast cancer. BMC Cancer 6, 276
42. Tsunoda, N., Kokuryo, T., Oda, K., Senga, T., Yokoyama, Y., Nagino, M., Nimura, Y., and Hamaguchi, M. (2009) NEK2 as a novel molecular target for the treatment of breast carcinoma. Cancer Sci. 100, 111-116
43. Suzuki, K., Kokuryo, T., Senga, T., Yokoyama, Y., Nagino, M., and Hamaguchi, M. (2010) Novel combination treatment for colorectal cancer using NEK2 siRNA and cisplatin. Cancer Sci. 101, 1163-1169
44. Löffler, H., Lukas, J., Bartek, J., and Krämer, A. (2006) Structure meets function-centrosomes, genome maintenance and the DNA damage response. Exp. Cell Res. 312, 2633-2640
45. Fletcher, L., Cerniglia, G. J., Nigg, E. A., Yend, T. J., and Muschel, R. J. (2004) Inhibition of centrosome separation after DNA damage: a role for NEK2. Radiat. Res. 162, 128-135
46. Li, M., He, Y., Dubois, W., Wu, X., Shi, J., and Huang, J. (2012) Distinct regulatory mechanisms and functions for p53-activated and p53-repressed DNA damage response genes in embryonic stem cells. Mol. Cell 46, 30-42
47. Petrovich, M., and Veprintsev, D. B. (2009) Effects of CpG methylation on recognition of DNA by the tumour suppressor p53. J. Mol. Biol. 386, 72-80
48. Botcheva, K., McCorkle, S. R., McCombie, W. R., Dunn, J. J., and Anderson, C. W. (2011) Distinct p53 genomic binding patterns in normal and cancer-derived human cells. Cell Cycle 10, 4237-4249
49. a binding sites that activate some tissue-specific genes. Proc. Natl. Acad. Sci. U.S.A. 107, 20311-20316
50. Budhram-Mahadeo, V., Morris, P. J., Smith, M. D., Midgley, C. A., Boxer, L. M., and Latchman, D. S. (1999) p53 suppresses the activation of the Bcl-2 promoter by the Brn-3a POU family transcription factor. J. Biol. Chem. 274, 15237-15244
51. Hoffman, W. H., Biade, S., Zilfou, J. T., Chen, J., and Murphy, M. (2002) Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J. Biol. Chem. 277, 3247-3257
52. Hsieh, C. L. (1999) Evidence that protein binding specifies sites of DNA demethylation. Mol. Cell. Biol. 19, 46-56
53. Lin, I. G., Tomzynski, T. J., Ou, Q., and Hsieh, C. L. (2000) Modulation of DNA binding protein affinity directly affects target site demethylation. Mol. Cell. Biol. 20, 2343-2349
54. Peltonen, K., Colis, L., Liu, H., Jäämaa, S., Moore, H. M., Enbäck, J., Laakkonen, P., Vaahtokari, A., Jones, R. J., af Hällström, T. M., and Laiho, M. (2010) Identification of novel p53 pathway activating small-molecule compounds reveals unexpected similarities with known therapeutic agents. PLoS One 5, e12996
55. Miller, L. D., Smeds, J., George, J., Vega, V. B., Vergara, L., Ploner, A., Pawitan, Y., Hall, P., Klaar, S., Liu, E. T., and Bergh, J. (2005) An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc. Natl. Acad. Sci. U.S.A. 102, 13550-13555
56. Bertheau, P., Turpin, E., Rickman, D. S., Espié, M., de Reyniès, A., Feugeas, J. P., Plassa, L. F., Soliman, H., Varna, M., de Roquancourt, A., Lehmann-Che, J., Beuzard, Y., Marty, M., Misset, J. L., Janin, A., and de Thé, H. (2007) Exquisite sensitivity of TP53 mutant and basal breast cancers to a dosedense epirubicin-cyclophosphamide regimen. PLoS Med. 4, e90
57. Guedj, M., Marisa, L., de Reynies, A., Orsetti, B., Schiappa, R., Bibeau, F., MacGrogan, G., Lerebours, F., Finetti, P., Longy, M., Bertheau, P., Bertrand, F., Bonnet, F., Martin, A. L., Feugeas, J. P., Bièche, I., Lehmann-Che, J., Lidereau, R., Birnbaum, D., Bertucci, F., de Thé, H., and Theillet, C. (2012) A refined molecular taxonomy of breast cancer. Oncogene 31, 1196-1206
58. Herbert, B. S., Chanoux, R. A., Liu, Y., Baenziger, P. H., Goswami, C. P., McClintick, J. N., Edenberg, H. J., Pennington, R. E., Lipkin, S. M., and Kopelovich, L. (2010) A molecular signature of normal breast epithelial and stromal cells from Li-Fraumeni syndrome mutation carriers. Oncotarget 1, 405-422