E2F1 confers anticancer drug resistance by targeting ABC transporter family members and Bcl-2 via the p73/DNp73-miR-205 circuitry

Cell Cycle

Volumn 11, Issue 16, 2012, Pages 3067-3078

  Alla, Vijay ^a   Kowtharapu, Bhavani S ^a   Engelmann, David ^a   Emmrich, Stephan ^a,c   Schmitz, Ulf ^b   Steder, Marc ^a   Pützer, Brigitte M ^a  

^a ROSTOCK UNIVERSITY MEDICAL CENTER   (Germany)

^b UNIVERSITY OF ROSTOCK   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

ABC transporters; Cancer; Chemoresistance; DNp73; E2F1; Melanoma mouse model; miR 205; p73

Indexed keywords

ATP BINDING CASSETTE TRANSPORTER A2; ATP BINDING CASSETTE TRANSPORTERS A5; CISPLATIN; ISOPROTEIN; MEMBRANE PROTEIN; MICRORNA 205; PROTEIN BCL 2; PROTEIN P73; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER STAGING; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GENOTOXICITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MALIGNANT TRANSFORMATION; MELANOMA CELL; METASTATIC MELANOMA; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; TUMOR GROWTH;

EID: 84865344231     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.21476     Document Type: Article

References (41)

1. Soengas MS, Lowe SW. Apoptosis and melanoma chemoresistance. Oncogene 2003; 22:3138-51; PMID:12789290; http://dx.doi.org/10.1038/sj.onc.1206454.
2. Halaban R, Cheng E, Smicun Y, Germino J. Deregulated E2F transcriptional activity in autonomously growing melanoma cells. J Exp Med 2000; 191:1005-16; PMID:10727462; http://dx.doi.org/10.1084/jem.191.6.1005.
3. Tuve S, Wagner SN, Schittek B, Pützer BM. Alterations of DeltaTA-p73 splice transcripts during melanoma development and progression. Int J Cancer 2004; 108:162-6; PMID:14618632; http://dx.doi.org/10.1002/ijc.11552.
4. Alla V, Engelmann D, Niemetz A, Pahnke J, Schmidt A, Kunz M, et al. E2F1 in melanoma progression and metastasis. J Natl Cancer Inst 2010; 102:127-33; PMID:20026813; http://dx.doi.org/10.1093/jnci/djp458.
5. Pützer BM, Tuve S, Tannapfel A, Stiewe T. Increased DeltaN-p73 expression in tumors by upregulation of the E2F1-regulated, TA-promoter-derived DeltaN'-p73 transcript. Cell Death Differ 2003; 10:612-4; PMID:12728260; http://dx.doi.org/10.1038/sj.cdd.4401205.
6. Seelan RS, Irwin M, van der Stoop P, Qian C, Kaelin WG Jr., Liu W. The human p73 promoter: characterization and identification of functional E2F binding sites. Neoplasia 2002; 4:195-203; PMID:11988839; http://dx.doi.org/10. 1038/sj.neo.7900237.
7. Stiewe T, Theseling CC, Pützer BM. Transactivation-deficient Delta TA-p73 inhibits p53 by direct competition for DNA binding: implications for tumorigenesis. J Biol Chem 2002; 277:14177-85; PMID:11844800; http://dx.doi.org/10.1074/jbc.M200480200.
8. Emmrich S, Wang W, John K, Li W, Pützer BM. Antisense gapmers selectively suppress individual oncogenic p73 splice isoforms and inhibit tumor growth in vivo. Mol Cancer 2009; 8:61; PMID:19671150; http://dx.doi.org/10.1186/ 1476-4598-8-61.
9. Mueller DW, Bosserhoff AK. Role of miRNAs in the progression of malignant melanoma. Br J Cancer 2009; 101:551-6; PMID:19638982; http://dx.doi.org/10. 1038/sj.bjc.6605204.
10. Lai EC. Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 2002; 30:363-4; PMID:11896390; http://dx.doi.org/10.1038/ng865.
11. Segura MF, Belitskaya-Lévy I, Rose AE, Zakrzewski J, Gaziel A, Hanniford D, et al. Melanoma MicroRNA signature predicts post-recurrence survival. Clin Cancer Res 2010; 16:1577-86; PMID:20179230; http://dx.doi.org/10. 1158/1078-0432.CCR-09-2721.
12. Ozsolak F, Poling LL, Wang Z, Liu H, Liu XS, Roeder RG, et al. Chromatin structure analyses identify miRNA promoters. Genes Dev 2008; 22:3172-83; PMID:19056895; http://dx.doi.org/10.1101/gad.1706508.
13. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K. Modulation of microRNA processing by p53. Nature 2009; 460:529-33; PMID:19626115; http://dx.doi.org/10.1038/nature08199.
14. Soengas MS, Capodieci P, Polsky D, Mora J, Esteller M, Opitz-Araya X, et al. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature 2001; 409:207-11; PMID:11196646; http://dx.doi.org/10.1038/35051606.
15. Stiewe T, Pützer BM. Role of the p53-homologue p73 in E2F1-induced apoptosis. Nat Genet 2000; 26:464-9; PMID:11101847; http://dx.doi.org/10.1038/ 82617.
16. Irwin MS, Kondo K, Marin MC, Cheng LS, Hahn WC, Kaelin WG Jr. Chemosensitivity linked to p73 function. Cancer Cell 2003; 3:403-10; PMID:12726865; http://dx.doi.org/10.1016/S1535-6108(03)00078-3.
17. Müller M, Schilling T, Sayan AE, Kairat A, Lorenz K, Schulze-Bergkamen H, et al. TAp73/DeltaNp73 influences apoptotic response, chemosensitivity and prognosis in hepatocellular carcinoma. Cell Death Differ 2005; 12:1564-77; PMID:16195739; http://dx.doi.org/10.1038/sj.cdd.4401774.
18. Stiewe T, Zimmermann S, Frilling A, Esche H, Pützer BM. Transactivation-deficient DeltaTA-p73 acts as an oncogene. Cancer Res 2002; 62:3598-602; PMID:12097259.
19. Deyoung MP, Ellisen LW. p63 and p73 in human cancer: defining the network. Oncogene 2007; 26:5169-83; PMID:17334395; http://dx.doi.org/10.1038/sj. onc.1210337.
20. Jiang M, Milner J. Bcl-2 constitutively suppresses p53-dependent apoptosis in colorectal cancer cells. Genes Dev 2003; 17:832-7; PMID:12670866; http://dx.doi.org/10.1101/gad.252603.
21. Gatti L, Cossa G, Beretta GL, Zaffaroni N, Perego P. Novel insights into targeting ATP-binding cassette transporters for antitumor therapy. Curr Med Chem 2011; 18:4237-49; PMID:21838682; http://dx.doi.org/10.2174/092986711797189682.
22. Gomez-Manzano C, Mitlianga P, Fueyo J, Lee H-Y, Hu M, Spurgers KB, et al. Transfer of E2F-1 to human glioma cells results in transcriptional up-regulation of Bcl-2. Cancer Res 2001; 61:6693-7; PMID:11559537.
23. Talantov D, Mazumder A, Yu JX, Briggs T, Jiang Y, Backus J, et al. Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin Cancer Res 2005; 11:7234-42; PMID:16243793; http://dx.doi.org/10.1158/1078- 0432.CCR-05-0683.
24. Yu YP, Landsittel D, Jing L, Nelson J, Ren B, Liu L, et al. Gene expression alterations in prostate cancer predicting tumor aggression and preceding development of malignancy. J Clin Oncol 2004; 22:2790-9; PMID:15254046; http://dx.doi.org/10.1200/JCO.2004.05.158.
25. Bhatnagar N, Li X, Padi SK, Zhang Q, Tang MS, Guo B. Downregulation of miR-205 and miR-31 confers resistance to chemotherapy-induced apoptosis in prostate cancer cells. Cell Death Dis 2010; 1:e105; PMID:21368878; http://dx.doi.org/10.1038/cddis.2010.85.
26. Dar AA, Majid S, de Semir D, Nosrati M, Bezrookove V, Kashani-Sabet M. miRNA-205 suppresses melanoma cell proliferation and induces senescence via regulation of E2F1 protein. J Biol Chem 2011; 286:16606-14; PMID:21454583; http://dx.doi.org/10.1074/jbc.M111.227611.
27. Sempere LF, Christensen M, Silahtaroglu A, Bak M, Heath CV, Schwartz G, et al. Altered MicroRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res 2007; 67:11612-20; PMID:18089790; http://dx.doi.org/10.1158/0008-5472.CAN-07-5019.
28. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005; 65:7065-70; PMID:16103053; http://dx.doi.org/10.1158/0008-5472.CAN-05-1783.
29. Wu H, Zhu S, Mo YY. Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Res 2009; 19:439-48; PMID:19238171; http://dx.doi.org/10. 1038/cr.2009.18.
30. Iorio MV, Casalini P, Piovan C, Di Leva G, Merlo A, Triulzi T, et al. microRNA-205 regulates HER3 in human breast cancer. Cancer Res 2009; 69:2195-200; PMID:19276373; http://dx.doi.org/10.1158/0008-5472.CAN-08-2920.
31. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10:593-601; PMID:18376396; http://dx.doi.org/10.1038/ncb1722.
32. Engelmann D, Pützer BM. Translating DNA damage into cancer cell death-A roadmap for E2F1 apoptotic signalling and opportunities for new drug combinations to overcome chemoresistance. Drug Resist Updat 2010; 13:119-31; PMID:20675184; http://dx.doi.org/10.1016/j.drup.2010.06.001.
33. Hirano G, Izumi H, Kidani A, Yasuniwa Y, Han B, Kusaba H, et al. Enhanced expression of PCAF endows apoptosis resistance in cisplatin-resistant cells. Mol Cancer Res 2010; 8:864-72; PMID:20530585; http://dx.doi.org/10.1158/1541- 7786.MCR-09-0458.
34. Millour J, de Olano N, Horimoto Y, Monteiro LJ, Langer JK, Aligue R, et al. ATM and p53 regulate FOXM1 expression via E2F in breast cancer epirubicin treatment and resistance. Mol Cancer Ther 2011; 10:1046-58; PMID:21518729; http://dx.doi.org/10.1158/1535-7163.MCT-11-0024.
35. Shukla A, Hillegass JM, MacPherson MB, Beuschel SL, Vacek PM, Pass HI, et al. Blocking of ERK1 and ERK2 sensitizes human mesothelioma cells to doxorubicin. Mol Cancer 2010; 9:314; PMID:21159167; http://dx.doi.org/10.1186/ 1476-4598-9-314.
36. Laing NM, Belinsky MG, Kruh GD, Bell DW, Boyd JT, Barone L, et al. Amplification of the ATP-binding cassette 2 transporter gene is functionally linked with enhanced efflux of estramustine in ovarian carcinoma cells. Cancer Res 1998; 58:1332-7; PMID:9537224.
37. Engelmann D, Pützer BM. The dark side of E2F1: in transit beyond apoptosis. Cancer Res 2012; 72:571-5; PMID:22298593; http://dx.doi.org/10.1158/ 0008-5472.CAN-11-2575.
38. Mack JT, Helke KL, Normand G, Green C, Townsend DM, Tew KD. ABCA2 transporter deficiency reduces incidence of TRAMP prostate tumor metastasis and cellular chemotactic migration. Cancer Lett 2011; 300:154-61; PMID:21041019; http://dx.doi.org/10.1016/j.canlet.2010.09.017.
39. John K, Alla V, Meier C, Pützer BM. GRAMD4 mimics p53 and mediates the apoptotic function of p73 at mitochondria. Cell Death Differ 2011; 18:874-86; PMID:21127500; http://dx.doi.org/10.1038/cdd.2010.153.
40. Salmon P, Trono D. Production and titration of lentiviral vectors. Curr Protoc Hum Genet 2007; Chapter 12:Unit 12.10.
41. Engelmann D, Knoll S, Ewerth D, Steder M, Stoll A, Pützer BM. Functional interplay between E2F1 and chemotherapeutic drugs defines immediate E2F1 target genes crucial for cancer cell death. Cell Mol Life Sci 2010; 67:931-48; PMID:20013022; http://dx.doi.org/10.1007/s00018-009-0222-0.