Elevated level of lysine 9-acetylated histone H3 at the MDR1 promoter in multidrug-resistant cells

Cancer Science

Volumn 103, Issue 4, 2012, Pages 659-669

  Toth, Monika ^a,b   Boros, Imre M ^b   Balint, Eva ^a,b,c  

^a BAY ZOLTÁN NONPROFIT LTD FOR APPLIED RESEARCH   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE ACETYLTRANSFERASE GCN5; HISTONE ACETYLTRANSFERASE PCAF; HISTONE H3; MULTIDRUG RESISTANCE PROTEIN 1;

ARTICLE; BREAST CANCER; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER RESISTANCE; CARCINOMA CELL; CONTROLLED STUDY; DRUG EXPOSURE; EXON; GENE LOCUS; GENE OVEREXPRESSION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR DOWN REGULATION;

ACETYLATION; BREAST NEOPLASMS; CELL LINE, TUMOR; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE ACETYLTRANSFERASES; HISTONE DEACETYLASE INHIBITORS; HISTONES; HUMANS; LYSINE; P-GLYCOPROTEIN; P300-CBP TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE;

EID: 84859004082     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2012.02215.x     Document Type: Article

References (47)

1. Fojo AT, Whang-Peng J, Gottesman MM, Pastan I. Amplification of DNA sequences in human multidrug-resistant KB carcinoma cells. Proc Natl Acad Sci USA 1985; 82: 7661-5.
2. Scotto KW, Biedler JL, Melera PW. Amplification and expression of genes associated with multidrug resistance in mammalian cells. Science 1986; 232: 751-5.
3. Mickley LA, Spengler BA, Knutsen TA, Biedler JL, Fojo T. Gene rearrangement: a novel mechanism for MDR-1 gene activation. J Clin Invest 1997; 99: 1947-57.
4. Shen DW, Fojo A, Chin JE et al. Human multidrug-resistant cell lines: increased mdr1 expression can precede gene amplification. Science 1986; 232: 643-5.
5. Nakayama M, Wada M, Harada T et al. Hypomethylation status of CpG sites at the promoter region and overexpression of the human MDR1 gene in acute myeloid leukemias. Blood 1998; 92: 4296-307.
6. Chaudhary PM, Roninson IB. Induction of multidrug resistance in human cells by transient exposure to different chemotherapeutic drugs. J Natl Cancer Inst 1993; 85: 632-9.
7. Leonessa F, Clarke R. ATP binding cassette transporters and drug resistance in breast cancer. Endocr Relat Cancer 2003; 10: 43-73.
8. Abolhoda A, Wilson AE, Ross H, Danenberg PV, Burt M, Scotto KW. Rapid activation of MDR1 gene expression in human metastatic sarcoma after in vivo exposure to doxorubicin. Clin Cancer Res 1999; 5: 3352-6.
9. Ueda K, Clark DP, Chen CJ, Roninson IB, Gottesman MM, Pastan I. The human multidrug resistance (mdr1) gene. cDNA cloning and transcription initiation. J Biol Chem 1987; 262: 505-8.
10. Chin JE, Soffir R, Noonan KE, Choi K, Roninson IB. Structure and expression of the human MDR (P-glycoprotein) gene family. Mol Cell Biol 1989; 9: 3808-20.
11. Chen KG, Wang YC, Schaner ME et al. Genetic and epigenetic modeling of the origins of multidrug-resistant cells in a human sarcoma cell line. Cancer Res 2005; 65: 9388-97.
12. Raguz S, Randle RA, Sharpe ER et al. Production of P-glycoprotein from the MDR1 upstream promoter is insufficient to affect the response to first-line chemotherapy in advanced breast cancer. Int J Cancer 2008; 122: 1058-67.
13. Raguz S, Tamburo De Bella M, Tripuraneni G et al. Activation of the MDR1 upstream promoter in breast carcinoma as a surrogate for metastatic invasion. Clin Cancer Res 2004; 10: 2776-83.
14. Labialle S, Gayet L, Marthinet E, Rigal D, Baggetto LG. Transcriptional regulators of the human multidrug resistance 1 gene: recent views. Biochem Pharmacol 2002; 64: 943-8.
15. Scotto KW. Transcriptional regulation of ABC drug transporters. Oncogene 2003; 22: 7496-511.
16. Jin S, Scotto KW. Transcriptional regulation of the MDR1 gene by histone acetyltransferase and deacetylase is mediated by NF-Y. Mol Cell Biol 1998; 18: 4377-84.
17. Jin W, Liu Y, Xu SG et al. UHRF1 inhibits MDR1 gene transcription and sensitizes breast cancer cells to anticancer drugs. Breast Cancer Res Treat 2010; 124: 39-48.
18. El-Khoury V, Breuzard G, Fourre N, Dufer J. The histone deacetylase inhibitor trichostatin A downregulates human MDR1 (ABCB1) gene expression by a transcription-dependent mechanism in a drug-resistant small cell lung carcinoma cell line model. Br J Cancer 2007; 97: 562-73.
19. Kim SN, Kim NH, Lee W, Seo DW, Kim YK. Histone deacetylase inhibitor induction of P-glycoprotein transcription requires both histone deacetylase 1 dissociation and recruitment of CAAT/enhancer binding protein beta and pCAF to the promoter region. Mol Cancer Res 2009; 7: 735-44.
20. Baker EK, Johnstone RW, Zalcberg JR, El-Osta A. Epigenetic changes to the MDR1 locus in response to chemotherapeutic drugs. Oncogene 2005; 24: 8061-75.
21. Yatouji S, El-Khoury V, Trentesaux C et al. Differential modulation of nuclear texture, histone acetylation, and MDR1 gene expression in human drug-sensitive and -resistant OV1 cell lines. Int J Oncol 2007; 30: 1003-9.
22. Kars MD, Iseri OD, Gunduz U, Ural AU, Arpaci F, Molnar J. Development of rational in vitro models for drug resistance in breast cancer and modulation of MDR by selected compounds. Anticancer Res 2006; 26: 4559-68.
23. Molnár J, Engi H, Gyémánt N et al. Multidrug resistance reversal on cancer cells by selected carotenoids, flavonoids and anthocyanins. In: Motohashi N, ed. Bioactive Heterocycles VI. Berlin/Heidelberg: Springer, 2008; 133-59.
24. Nagy Z, Riss A, Fujiyama S et al. The metazoan ATAC and SAGA coactivator HAT complexes regulate different sets of inducible target genes. Cell Mol Life Sci 2010; 67: 611-28.
25. Brand M, Moggs JG, Oulad-Abdelghani M et al. UV-damaged DNA-binding protein in the TFTC complex links DNA damage recognition to nucleosome acetylation. EMBO J 2001; 20: 3187-96.
26. Helmlinger D, Hardy S, Eberlin A, Devys D, Tora L. Both normal and polyglutamine- expanded ataxin-7 are components of TFTC-type GCN5 histone acetyltransferase- containing complexes. Biochem Soc Symp 2006; 73: 155-63.
27. Fairchild CR, Ivy SP, Kao-Shan CS et al. Isolation of amplified and overexpressed DNA sequences from adriamycin-resistant human breast cancer cells. Cancer Res 1987; 47: 5141-8.
28. Wang Z, Zang C, Cui K et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009; 138: 1019-31.
29. Costi R, Di Santo R, Artico M et al. Cinnamoyl compounds as simple molecules that inhibit p300 histone acetyltransferase. J Med Chem 2007; 50: 1973-7.
30. Jin Q, Yu LR, Wang L et al. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J 2011; 30: 249-62.
31. Seligson DB, Horvath S, Shi T et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature 2005; 435: 1262-6.
32. Park YS, Jin MY, Kim YJ, Yook JH, Kim BS, Jang SJ. The global histone modification pattern correlates with cancer recurrence and overall survival in gastric adenocarcinoma. Ann Surg Oncol 2008; 15: 1968-76.
33. Elsheikh SE, Green AR, Rakha EA et al. Global histone modifications in breast cancer correlate with tumor phenotypes, prognostic factors, and patient outcome. Cancer Res 2009; 69: 3802-9.
34. Manuyakorn A, Paulus R, Farrell J et al. Cellular histone modification patterns predict prognosis and treatment response in resectable pancreatic adenocarcinoma: results from RTOG 9704. J Clin Oncol 2010; 28: 1358-65.
35. Barlesi F, Giaccone G, Gallegos-Ruiz MI et al. Global histone modifications predict prognosis of resected non small-cell lung cancer. J Clin Oncol 2007; 25: 4358-64.
36. Yatouji S, Trussardi-Regnier A, Trentesaux C, Liautaud-Roger F, Dufer J. Nuclear texture and chromatin structure in OV1/VCR human multidrug-resistant cell line. Int J Oncol 2003; 23: 1225-30.
37. Wang Z, Zang C, Rosenfeld JA et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 2008; 40: 897-903.
38. Yoo CB, Jones PA. Epigenetic therapy of cancer: past, present and future. Nat Rev Drug Discov 2006; 5: 37-50.
39. Lee E, Furukubo T, Miyabe T, Yamauchi A, Kariya K. Involvement of histone hyperacetylation in triggering DNA fragmentation of rat thymocytes undergoing apoptosis. FEBS Lett 1996; 395: 183-7.
40. Lee TB, Park JH, Min YD, Kim KJ, Choi CH. Epigenetic mechanisms involved in differential MDR1 mRNA expression between gastric and colon cancer cell lines and rationales for clinical chemotherapy. BMC Gastroenterol 2008; 8: 33.
41. Hauswald S, Duque-Afonso J, Wagner MM et al. Histone deacetylase inhibitors induce a very broad, pleiotropic anticancer drug resistance phenotype in acute myeloid leukemia cells by modulation of multiple ABC transporter genes. Clin Cancer Res 2009; 15: 3705-15.
42. El-Osta A, Kantharidis P, Zalcberg JR, Wolffe AP. Precipitous release of methyl-CpG binding protein 2 and histone deacetylase 1 from the methylated human multidrug resistance gene (MDR1) on activation. Mol Cell Biol 2002; 22: 1844-57.
43. David GL, Yegnasubramanian S, Kumar A et al. MDR1 promoter hypermethylation in MCF-7 human breast cancer cells: changes in chromatin structure induced by treatment with 5-Aza-cytidine. Cancer Biol Ther 2004; 3: 540-8.
44. Tian K, Jurukovski V, Wang XP, Kaplan MH, Xu H. Epigenetic regulation of WTH3 in primary and cultured drug-resistant breast cancer cells. Cancer Res 2005; 65: 10024-31.
45. Schiltz RL, Mizzen CA, Vassilev A, Cook RG, Allis CD, Nakatani Y. Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J Biol Chem 1999; 274: 1189-92.
46. Liu X, Wang L, Zhao K et al. The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature 2008; 451: 846-50.
47. Shtil AA, Azare J. Redundancy of biological regulation as the basis of emergence of multidrug resistance. Int Rev Cytol 2005; 246: 1-29.