p53 Ser15 phosphorylation and histone modifications contribute to IR-induced miR-34a transcription in mammary epithelial cells

Cell Cycle

Volumn 12, Issue 13, 2013, Pages 2073-2083

  Wang, Bo ^a   Li, Dongping ^a   Kovalchuk, Olga ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Histone modification; Ionizing radiation; Mammary epithelial cells; miR 34a transcription; p53 phosphorylation

Indexed keywords

HISTONE H3; HISTONE H4; LUCIFERASE; MICRORNA 34A; MITOGEN ACTIVATED PROTEIN KINASE P38; MUTANT PROTEIN; PROTEIN P53; VORINOSTAT;

ANIMAL TISSUE; ARTICLE; BREAST EPITHELIUM; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENZYME ACTIVITY; FEMALE; GENE DOSAGE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; NONHUMAN; PROMOTER REGION; PROTEIN PHOSPHORYLATION; RAT; WILD TYPE;

RATTUS;

EID: 84879777406     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.25135     Document Type: Article

References (64)

1. Schairer C, Mink PJ, Carroll L, Devesa SS. Probabilities of death from breast cancer and other causes among female breast cancer patients. J Natl Cancer Inst 2004; 96:1311-21; PMID:15339969; http://dx.doi.org/10.1093/jnci/ djh253
2. Mattsson A, Rudén BI, Hall P, Wilking N, Rutqvist LE. Radiation-induced breast cancer: long-term followup of radiation therapy for benign breast disease. J Natl Cancer Inst 1993; 85:1679-85; PMID:8411245; http://dx.doi.org/10.1093/jnci/85.20.1679
3. Doody MM, Lonstein JE, Stovall M, Hacker DG, Luckyanov N, Land CE. Breast cancer mortality after diagnostic radiography: findings from the U.S. Scoliosis Cohort Study. Spine (Phila Pa 1976) 2000; 25:2052-63; PMID:10954636; http://dx.doi.org/10.1097/00007632-200008150-00009
4. Ronckers CM, Erdmann CA, Land CE. Radiation and breast cancer: a review of current evidence. Breast Cancer Res 2005; 7:21-32; PMID:15642178; http://dx.doi.org/10.1186/bcr970
5. Calaf G, Hei TK. Oncoprotein expression in human breast epithelial cells transformed by high-LET radiation. Int J Radiat Biol 2001; 77:31-40; PMID:11213348; http://dx.doi.org/10.1080/095530001453096
6. Calaf GM, Alvarado ME, Hei TK. Oncoprotein expression and morphological phenotypes of human breast epithelial cells transformed by the c-Ha-ras oncogene. Oncol Rep 2005; 14:885-93; PMID:16142347
7. Brenner DJ, Sawant SG, Hande MP, Miller RC, Elliston CD, Fu Z, et al. Routine screening mammography: how important is the radiation-risk side of the benefit-risk equation? Int J Radiat Biol 2002; 78:1065-7; PMID:12556334; http://dx.doi.org/10.1080/0955300021000016576
8. Kruger RL, Schueler BA. A survey of clinical factors and patient dose in mammography. Med Phys 2001; 28:1449-54; PMID:11488578; http://dx.doi.org/10. 1118/1.1382606
9. Frankenberg D, Kelnhofer K, Garg I, Bär K, Frankenberg-Schwager M. Enhanced mutation and neoplastic transformation in human cells by 29 kVp relative to 200 kVp X rays indicating a strong dependence of RBE on photon energy. Radiat Prot Dosimetry 2002; 99:261-4; PMID:12194301; http://dx.doi.org/10.1093/oxfordjournals.rpd.a006779
10. Frankenberg D, Kelnhofer K, Bär K, Frankenberg- Schwager M. Enhanced neoplastic transformation by mammography X rays relative to 200 kVp X rays: indication for a strong dependence on photon energy of the RBE(M) for various end points. Radiat Res 2002; 157:99-105; PMID:11754647; http://dx.doi.org/10. 1667/0033-7587(2002)157[0099:ENTBMX]2.0.CO;2
11. Frankenberg D, Frankenberg-Schwager M, Garg I, Pralle E, Uthe D, Greve B, et al. Mutation induction and neoplastic transformation in human and human-hamster hybrid cells: dependence on photon energy and modulation in the low-dose range. J Radiol Prot 2002; 22(3A):A17-20; PMID:12400941; http://dx.doi.org/10.1088/0952-4746/22/3A/303
12. Brenner DJ, Amols HI. Enhanced risk from low-energy screen - film mammography X rays. Br J Radiol 1989; 62:910-4; PMID:2819359; http://dx.doi.org/10.1259/0007-1285-62-742-910
13. Eccles LJ, O'Neill P, Lomax ME. Delayed repair of radiation induced clustered DNA damage: friend or foe? Mutat Res 2011; 711:134-41; PMID:21130102; http://dx.doi.org/10.1016/j.mrfmmm.2010.11.003
14. Georgakilas AG. Processing of DNA damage clusters in human cells: current status of knowledge. Mol Biosyst 2008; 4:30-5; PMID:18075671; http://dx.doi.org/10.1039/b713178j
15. van Bekkum DW, Broerse JJ. Induction of mammary tumors by ionising radiation. Radiat Environ Biophys 1991; 30:217-20; PMID:1924709; http://dx.doi.org/10.1007/BF01226623
16. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33(Suppl):245-54; PMID:12610534; http://dx.doi.org/10.1038/ng1089
17. Rountree MR, Bachman KE, Herman JG, Baylin SB. DNA methylation, chromatin inheritance, and cancer. Oncogene 2001; 20:3156-65; PMID:11420732; http://dx.doi.org/10.1038/sj.onc.1204339
18. Shames DS, Minna JD, Gazdar AF. DNA methylation in health, disease, and cancer. Curr Mol Med 2007; 7:85-102; PMID:17311535; http://dx.doi.org/10.2174/ 156652407779940413
19. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 2006; 31:89-97; PMID:16403636; http://dx.doi.org/10.1016/j. tibs.2005.12.008
20. Weber M, Schübeler D. Genomic patterns of DNA methylation: targets and function of an epigenetic mark. Curr Opin Cell Biol 2007; 19:273-80; PMID:17466503; http://dx.doi.org/10.1016/j.ceb.2007.04.011
21. Weidman JR, Dolinoy DC, Murphy SK, Jirtle RL. Cancer susceptibility: epigenetic manifestation of environmental exposures. Cancer J 2007; 13:9-16; PMID:17464241; http://dx.doi.org/10.1097/PPO.0b013e31803c71f2
22. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293:1074-80; PMID:11498575; http://dx.doi.org/10.1126/science.1063127
23. Munshi A, Shafi G, Aliya N, Jyothy A. Histone modifications dictate specific biological readouts. J Genet Genomics 2009; 36:75-88; PMID:19232306; http://dx.doi.org/10.1016/S1673-8527(08)60094-6
24. Cheung P, Lau P. Epigenetic regulation by histone methylation and histone variants. Mol Endocrinol 2005; 19:563-73; PMID:15677708; http://dx.doi.org/10. 1210/me.2004-0496
25. Hwang HW, Mendell JT. MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br J Cancer 2006; 94:776-80; PMID:16495913; http://dx.doi.org/10. 1038/sj.bjc.6603023
26. Sevignani C, Calin GA, Siracusa LD, Croce CM. Mammalian microRNAs: a small world for fine-tuning gene expression. Mamm Genome 2006; 17:189-202; PMID:16518686; http://dx.doi.org/10.1007/s00335-005-0066-3
27. Hutvágner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002; 297:2056-60; PMID:12154197; http://dx.doi.org/10. 1126/science.1073827
28. Hutvágner G, Zamore PD. RNAi: nature abhors a double-strand. Curr Opin Genet Dev 2002; 12:225-32; PMID:11893497; http://dx.doi.org/10.1016/S0959- 437X(02)00290-3
29. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007; 26:745-52; PMID:17540599; http://dx.doi.org/10.1016/j.molcel.2007.05.010
30. Fabbri M, Ivan M, Cimmino A, Negrini M, Calin GA. Regulatory mechanisms of microRNAs involvement in cancer. Expert Opin Biol Ther 2007; 7:1009-19; PMID:17665990; http://dx.doi.org/10.1517/14712598.7.7.1009
31. Piao HL, Ma L. Non-coding RNAs as regulators of mammary development and breast cancer. J Mammary Gland Biol Neoplasia 2012; 17:33-42; PMID:22350981; http://dx.doi.org/10.1007/s10911-012-9245-5
32. Deng D, Liu Z, Du Y. Epigenetic alterations as cancer diagnostic, prognostic, and predictive biomarkers. Adv Genet 2010; 71:125-76; PMID:20933128; http://dx.doi.org/10.1016/B978-0-12-380864-6.00005-5
33. Esteller M. Cancer Epigenetics for the 21st Century: What's Next? Genes Cancer 2011; 2:604-6; PMID:21941616; http://dx.doi.org/10.1177/1947601911423096
34. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004; 4:143-53; PMID:14732866; http://dx.doi.org/10.1038/nrc1279
35. Herceg Z, Ushijima T. Introduction: epigenetics and cancer. Adv Genet 2010; 70:1-23; PMID:20920743; http://dx.doi.org/10.1016/B978-0-12-380866-0. 60001-0
36. Koturbash I, Zemp FJ, Pogribny I, Kovalchuk O. Small molecules with big effects: the role of the microRNAome in cancer and carcinogenesis. Mutat Res 2011; 722:94-105; PMID:20472093; http://dx.doi.org/10.1016/j.mrgentox.2010.05. 006
37. Pogribny IP, Beland FA. DNA hypomethylation in the origin and pathogenesis of human diseases. Cell Mol Life Sci 2009; 66:2249-61; PMID:19326048; http://dx.doi.org/10.1007/s00018-009-0015-5
38. Kovalchuk O, Baulch JE. Epigenetic changes and non-targeted radiation effects--is there a link? Environ Mol Mutagen 2008; 49:16-25; PMID:18172877; http://dx.doi.org/10.1002/em.20361
39. Ilnytskyy Y, Kovalchuk O. Non-targeted radiation effects-an epigenetic connection. Mutat Res 2011; 714:113-25; PMID:21784089; http://dx.doi.org/10. 1016/j.mrfmmm.2011.06.014
40. Loree J, Koturbash I, Kutanzi K, Baker M, Pogribny I, Kovalchuk O. Radiation-induced molecular changes in rat mammary tissue: possible implications for radiation-induced carcinogenesis. Int J Radiat Biol 2006; 82:805-15; PMID:17148264; http://dx.doi.org/10.1080/09553000600960027
41. Koturbash I, Zemp FJ, Kutanzi K, Luzhna L, Loree J, Kolb B, et al. Sex-specific microRNAome deregulation in the shielded bystander spleen of cranially exposed mice. Cell Cycle 2008; 7:1658-67; PMID:18560276; http://dx.doi.org/10.4161/cc.7.11.5981
42. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, et al. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 2007; 6:1586-93; PMID:17554199; http://dx.doi.org/10.4161/cc.6.13.4436
43. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007; 447:1130-4; PMID:17554337; http://dx.doi.org/10.1038/nature05939
44. Macleod KF, Sherry N, Hannon G, Beach D, Tokino T, Kinzler K, et al. p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev 1995; 9:935-44; PMID:7774811; http://dx.doi.org/10.1101/gad.9.8.935
45. Valerie K, Yacoub A, Hagan MP, Curiel DT, Fisher PB, Grant S, et al. Radiation-induced cell signaling: insideout and outside-in. Mol Cancer Ther 2007; 6:789-801; PMID:17363476; http://dx.doi.org/10.1158/1535-7163.MCT-06-0596
46. Cho HN, Lee SJ, Park SH, Lee YJ, Cho CK, Lee YS. Overexpression of heat-shock protein 25 augments radiation-induced cell-cycle arrest in murine L929 cells. Int J Radiat Biol 2001; 77:225-33; PMID:11236929; http://dx.doi.org/10.1080/09553000010001024
47. Hagan M, Wang L, Hanley JR, Park JS, Dent P. Ionizing radiation-induced mitogen-activated protein (MAP) kinase activation in DU145 prostate carcinoma cells: MAP kinase inhibition enhances radiation-induced cell killing and G2/M-phase arrest. Radiat Res 2000; 153:371-83; PMID:10760996; http://dx.doi.org/10.1667/0033-7587(2000)153[0371:IRIMAP]2.0.CO;2
48. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001; 294:853-8; PMID:11679670; http://dx.doi.org/10.1126/science.1064921
49. Lau NC, Lim LP, Weinstein EG, Bartel DP. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001; 294:858-62; PMID:11679671; http://dx.doi.org/10.1126/science.1065062
50. Lee RC, Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001; 294:862-4; PMID:11679672; http://dx.doi.org/10.1126/ science.1065329
51. Welch C, Chen Y, Stallings RL. MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 2007; 26:5017-22; PMID:17297439; http://dx.doi.org/10.1038/sj.onc.1210293
52. Raver-Shapira N, Oren M. Tiny actors, great roles: microRNAs in p53's service. Cell Cycle 2007; 6:2656-61; PMID:17957137; http://dx.doi.org/10.4161/ cc.6.21.4915
53. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 2007; 26:731-43; PMID:17540598; http://dx.doi.org/10.1016/j. molcel.2007.05.017
54. Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, Johnson E, et al. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 2009; 69:7569-76; PMID:19773441; http://dx.doi.org/10.1158/0008-5472. CAN-09-0529
55. Tazawa H, Tsuchiya N, Izumiya M, Nakagama H. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci USA 2007; 104:15472-7; PMID:17875987; http://dx.doi.org/10.1073/pnas.0707351104
56. Christoffersen NR, Shalgi R, Frankel LB, Leucci E, Lees M, Klausen M, et al. p53-independent upregulation of miR-34a during oncogene-induced senescence represses MYC. Cell Death Differ 2010; 17:236-45; PMID:19696787; http://dx.doi.org/10.1038/cdd.2009.109
57. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Körner H, et al. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008; 7:2591-600; PMID:18719384; http://dx.doi.org/10. 4161/cc.7.16.6533
58. Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG, et al. Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 2010; 31:745-50; PMID:20118199; http://dx.doi.org/10.1093/carcin/bgq033
59. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ 2010; 17:193-9; PMID:19461653; http://dx.doi.org/10.1038/cdd.2009.56
60. Vogt M, Munding J, Grüner M, Liffers ST, Verdoodt B, Hauk J, et al. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch 2011; 458:313-22; PMID:21225432; http://dx.doi.org/10.1007/s00428-010-1030-5
61. Saito S, Yamaguchi H, Higashimoto Y, Chao C, Xu Y, Fornace AJ Jr., et al. Phosphorylation site interdependence of human p53 post-translational modifications in response to stress. J Biol Chem 2003; 278:37536-44; PMID:12860987; http://dx.doi.org/10.1074/jbc.M305135200
62. Healy S, Khan P, He S, Davie JR. Histone H3 phosphorylation, immediate-early gene expression, and the nucleosomal response: a historical perspective. Biochem Cell Biol 2012; 90:39-54; PMID:22250664
63. Livengood JA, Scoggin KE, Van Orden K, McBryant SJ, Edayathumangalam RS, Laybourn PJ, et al. p53 Transcriptional activity is mediated through the SRC1-interacting domain of CBP/p300. J Biol Chem 2002; 277:9054-61; PMID:11782467; http://dx.doi.org/10.1074/jbc.M108870200
64. Gentile M, Latonen L, Laiho M. Cell cycle arrest and apoptosis provoked by UV radiation-induced DNA damage are transcriptionally highly divergent responses. Nucleic Acids Res 2003; 31:4779-90; PMID:12907719; http://dx.doi.org/10.1093/nar/gkg675