Epigenetic silencing mediated through activated PI3K/AKT signaling in breast cancer

Cancer Research

Volumn 71, Issue 5, 2011, Pages 1752-1762

  Zuo, Tao ^a   Liu, Ta Ming ^a   Lan, Xun ^a   Weng, Yu I ^a   Shen, Rulong ^a   Gu, Fei ^a   Huang, Yi Wen ^a   Liyanarachchi, Sandya ^a   Deatherage, Daniel E ^a   Hsu, Pei Yin ^a   Taslim, Cenny ^a   Ramaswamy, Bhuvaneswari ^a   Shapiro, Charles L ^a   Lin, Huey Jen L ^b   Cheng, Alfred S L ^c   Jin, Victor X ^a   Huang, Tim H M ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 5 AZA 2' DEOXYCYTIDINE; HISTONE; HISTONE 3 LYSINE 27; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRICHOSTATIN A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVATION; EPIGENETICS; FEMALE; GENE LOCUS; GENE REPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HISTONES; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, SCID; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79952241034     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3573     Document Type: Article

References (48)

1. Esteller M. Epigenetics in cancer. N Engl J Med 2008;358:1148-59.
2. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007;128:683-92. (Pubitemid 46273572)
3. Bracken AP, Helin K. Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat Rev Cancer 2009;9:773-84.
4. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 2009;10:295-304.
5. Lo PK, Sukumar S. Epigenomics and breast cancer. Pharmacogenomics 2008;9:1879-902.
6. Simon JA, Kingston RE. Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 2009;10:697-708.
7. Sparmann A, van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 2006;6:846-56. (Pubitemid 44629896)
8. Cao R, Zhang Y. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 2004;14:155-64. (Pubitemid 38520143)
9. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007;39:237-42. (Pubitemid 46184356)
10. Schlesinger Y, Straussman R, Keshet I, Keshet I, Farkash S, Hecht M, Zimmerman J, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007;39:232-36. (Pubitemid 46184355)
11. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, et al. Epigenetic stem cell signature in cancer. Nat Genet 2007;39:157-58. (Pubitemid 46184343)
12. Bloushtain-Qimron N, Yao J, Shipitsin M, Maruyama R, Polyak K. Epigenetic patterns of embryonic and adult stem cells. Cell Cycle 2009;8:809-17.
13. McCabe MT, Lee EK, Vertino PM. A multifactorial signature of DNA sequence and polycomb binding predicts aberrant CpG island methylation. Cancer Res 2009;69:282-91.
14. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelo C, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006;439:871-84.
15. Gal-Yam EN, Egger G, Iniguez L, Holster H, Einarsson S, Zhang X, et al. Frequent switching of Polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc Natl Acad Sci U S A 2008;105:12979-84.
16. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet 2008;40:741-50. (Pubitemid 351748874)
17. McGarvey KM, Greene E, Fahrner JA, Jenuwein T, Baylin SB. DNA methylation and complete transcriptional silencing of cancer genes persist after depletion of EZH2. Cancer Res 2007;67:5097-102. (Pubitemid 46997244)
18. Jones PA, Liang G. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 2009;10:805-11.
19. Lin HJ, Zuo T, Lin CH, Chieh Ti, Kuo CT, Liyanarachchi S, Sun S, et al. Breast cancer-associated fibroblasts confer AKT1-mediated epigenetic silencing of Cystatin M in epithelial cells. Cancer Res 2008;68:10257-66.
20. Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell 2007;129:1261-74. (Pubitemid 46962095)
21. Vivanco I, Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2002;2:489-501. (Pubitemid 37328931)
22. Frietze S, Lan X, Jin VX, Farnham PJ. Genomic targets of the KRAB and SCAN domain-containing zinc finger protein 263. J Biol Chem 2010;285:1393-403.
23. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner F, Fevr T, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006;10:515-27. (Pubitemid 44854747)
24. Mohn F, Weber M, Schubeler D, Roloff TC. Methylated DNA immunoprecipitation (MeDIP). Methods Mol Biol 2009;507:55-64.
25. Robinson MD, Stirzaker C, Statham AL, Coolen MW, Song JZ, Nair SS, et al. Evaluation of affinity-based genome-wide DNA methylation data: Effects of CpG density, amplification bias, and copy number variation. Genome Res 2010;20:1719-29.
26. Xu JS, Huang J, Qin R, Hinkle GH, Povosky SP, Martin EW, et al. Synthesizing and binding dual-mode poly (lactic-co-glycolic acid) (PLGA) nanobubbles for cancer targeting and imaging. Biomaterials 2009;31:1716-22.
27. Brugge J, Hung MC, Mills GB. A new mutational AKTivation in the PI3K pathway. Cancer Cell 2007;12:104-07. (Pubitemid 47199129)
28. Maroulakou IG, Oemler W, Naber SP, Tsichlis PN. Akt1 ablation inhibits, whereas Akt2 ablation accelerates, the development of mammary adenocarcinomas in mouse mammary tumor virus (MMTV)-ErbB2/neu and MMTV-polyoma middle T transgenic mice. Cancer Res 2007;67:167-77. (Pubitemid 46142772)
29. Pauler FM, Sloane MA, Huang R, Regha K, Koemer MV, Tamir I, et al. H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res 2009;19:221-33.
30. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006;441:349-53. (Pubitemid 44050199)
31. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006;125:301-13. (Pubitemid 44313811)
32. Engelman JA. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 2009;9:550-62.
33. Oki Y, Issa JP. Review: recent clinical trials in epigenetic therapy. Rev Recent Clin Trials 2006;1:169-82.
34. Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran- 4-one (LY294002). J Biol Chem 1994;269:5241-48,.
35. Chan MW, Huang YW, Hartman-Frey C, Kuo CT, Deatherage D, Qin H, et al. Aberrant transforming growth factor beta1 signaling and SMAD4 nuclear translocation confer epigenetic repression of ADAM19 in ovarian cancer. Neoplasia 2008;10:908-19.
36. Hinshelwood RA, Huschtscha LI, Melki J, Stirzaker C, Abdipranoto A, Vissel B, et al. Concordant epigenetic silencing of transforming growth factor-beta signaling pathway genes occurs early in breast carcinogenesis. Cancer Res 2007;67:11517-27.
37. Leu YW, Yan PS, Fan M, Jin VX, Liu JC, Curran EM, et al. Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res 2004;64:8184-92. (Pubitemid 39491754)
38. Cheng AS, Culhane AC, Chan MW, Venkataramu CR, Ehrich M, Nasir A, et al. Epithelial progeny of estrogen-exposed breast progenitor cells display a cancer-like methylome. Cancer Res 2008;68:1786-96. (Pubitemid 351416564)
39. Hsu PY, Deatherage DE, Rodriguez BA, Liyanarachchi S, Yu-I Weng YI, Zuo T, et al. Xenoestrogen-induced epigenetic repression of micro- RNA-9-3 in breast epithelial cells. Cancer Res 2009;69:5936-45.
40. Cha TL, Zhou BP, Xia W, Wu Y, Yang C-C, Chen C-T, et al. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 2005;310:306-10. (Pubitemid 41457195)
41. Sun L, Zhao H, Xu Z, Liub Q, Liangb Y, Wanga L, et al. Phosphatidylinositol 3-kinase/protein kinase B pathway stabilizes DNA methyltransferase I protein and maintains DNA methylation. Cell Signal 2007;19:2255-63. (Pubitemid 47361683)
42. Bredfeldt TG, Greathouse KL, Safe SH, Hung M-C, Bedford MT, Walker CL. Xenoestrogen-induced regulation of EZH2 and histone methylation via estrogen receptor signaling to PI3K/AKT. Mol Endocrinol 2010;24:993-1006.
43. Hennessy BT, Smith DL, Ram PT, Lu Y, Mills GB. Exploiting the PI3K/ AKT pathway for cancer drug discovery. Nat Rev Drug Discov 2005;4:988-1004.
44. Liu P, Cheng H, Roberts TM, Zhao JJ. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat Rev Drug Discov 2009;8:627-44.
45. Issa JP, Kantarjian HM. Targeting DNA methylation. Clin Cancer Res 2009;15:3938-46.
46. Silverman LR, Demakos EP, Peterson BL, Kornblith AB, Holland JC, Odchimar-Reissig R, et al. Randomized controlled trial of azacitidine in patients with the myelodysplastic syndrome: a study of the cancer and leukemia group B. J Clin Oncol 2002;20:2429-40. (Pubitemid 34525728)
47. Kagey JD, Kapoor-Vazirani P, McCabe MT, Powell DR, Vertino PM. Long-term stability of demethylation after transient exposure to 5-aza- 20-deoxycytidine correlates with sustained RNA polymerase II occupancy. Mol Cancer Res 2010;8:1048-59.
48. Oki Y, Jelinek J, Shen L, Kantarjian HM, Issa JP. Induction of hypomethylation and molecular response after decitabine therapy in patients with chronic myelomonocytic leukemia. Blood 2008;111: 2382-84. (Pubitemid 351451448)