TP53-independent function of miR-34a via HDAC1 and p21 CIP1/WAF1

Molecular Therapy

Volumn 21, Issue 9, 2013, Pages 1678-1686

  Zhao, Jane ^a   Lammers, Paul ^a   Torrance, Chris J ^b   Bader, Andreas G ^a  

^a SYNLOGIC   (United States)

^b Horizon Discovery Ltd ^*  (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; HISTONE DEACETYLASE 1; MESSENGER RNA; MICRORNA 192; MICRORNA 215; MICRORNA 34A; MICRORNA 34C; PROTEIN P53; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER PATIENT; CANCER TISSUE; CONTROLLED STUDY; ENZYME INHIBITION; GENE FUNCTION; GENETIC REGULATION; HUMAN; HUMAN TISSUE; LUNG NON SMALL CELL CANCER; POSITIVE FEEDBACK; PROTEIN DEPLETION; PROTEIN INDUCTION; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; UPREGULATION;

CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; ENZYME REPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASE 1; HUMANS; MICRORNAS; NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84883743256     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.148     Document Type: Article

References (42)

1. Lodygin, D, Tarasov, V, Epanchintsev, A, Berking, C, Knyazeva, T, Körner, H et al. (2008). Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 7: 2591-2600.
2. Calin, GA, Sevignani, C, Dumitru, CD, Hyslop, T, Noch, E, Yendamuri, S et al. (2004). Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 101: 2999-3004. (Pubitemid 38327724)
3. Gallardo, E, Navarro, A, Viñolas, N, Marrades, RM, Diaz, T, Gel, B et al. (2009). miR-34a as a prognostic marker of relapse in surgically resected non-small-cell lung cancer. Carcinogenesis 30: 1903-1909.
4. Chim, CS, Wong, KY, Qi, Y, Loong, F, Lam, WL, Wong, LG et al. (2010). Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 31: 745-750.
5. Hermeking, H (2010). The miR-34 family in cancer and apoptosis. Cell Death Differ 17: 193-199.
6. Bader, AG (2012). miR-34-a microRNA replacement therapy is headed to the clinic. Front Genet 3: 120.
7. Ji, Q, Hao, X, Zhang, M, Tang, W, Yang, M, Li, L et al. (2009). MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS ONE 4: e6816.
8. Liu, C, Kelnar, K, Liu, B, Chen, X, Calhoun-Davis, T, Li, H et al. (2011). The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 17: 211-215.
9. Trang, P, Wiggins, JF, Daige, CL, Cho, C, Omotola, M, Brown, D et al. (2011). Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol Ther 19: 1116-1122.
10. Wiggins, JF, Ruffino, L, Kelnar, K, Omotola, M, Patrawala, L, Brown, D et al. (2010). Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res 70: 5923-5930.
11. Craig, VJ, Tzankov, A, Flori, M, Schmid, CA, Bader, AG and Müller, A (2012). Systemic microRNA-34a delivery induces apoptosis and abrogates growth of diffuse large B-cell lymphoma in vivo. Leukemia 26: 2421-2424.
12. Bommer, GT, Gerin, I, Feng, Y, Kaczorowski, AJ, Kuick, R, Love, RE et al. (2007). p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 17: 1298-1307. (Pubitemid 47176893)
13. Chang, TC, Wentzel, EA, Kent, OA, Ramachandran, K, Mullendore, M, Lee, KH et al. (2007). Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 26: 745-752. (Pubitemid 46856245)
14. He, L, He, X, Lim, LP, de Stanchina, E, Xuan, Z, Liang, Y et al. (2007). A microRNA component of the p53 tumour suppressor network. Nature 447: 1130-1134. (Pubitemid 47014436)
15. Raver-Shapira, N, Marciano, E, Meiri, E, Spector, Y, Rosenfeld, N, Moskovits, N et al. (2007). Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 26: 731-743. (Pubitemid 46856247)
16. Tarasov, V, Jung, P, Verdoodt, B, Lodygin, D, Epanchintsev, A, Menssen, A et al. (2007). 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 6: 1586-1593. (Pubitemid 47327945)
17. Braun, CJ, Zhang, X, Savelyeva, I, Wolff, S, Moll, UM, Schepeler, T et al. (2008). p53-Responsive microRNAs 192 and 215 are capable of inducing cell cycle arrest. Cancer Res 68: 10094-10104.
18. Georges, SA, Biery, MC, Kim, SY, Schelter, JM, Guo, J, Chang, AN et al. (2008). Coordinated regulation of cell cycle transcripts by p53-Inducible microRNAs, miR-192 and miR-215. Cancer Res 68: 10105-10112.
19. Pichiorri, F, Suh, SS, Rocci, A, De Luca, L, Taccioli, C, Santhanam, R et al. (2010). Downregulation of p53-inducible microRNAs 192, 194, and 215 impairs the p53/MDM2 autoregulatory loop in multiple myeloma development. Cancer Cell 18: 367-381.
20. Momand, J, Zambetti, GP, Olson, DC, George, D and Levine, AJ (1992). The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69: 1237-1245.
21. Oliner, JD, Kinzler, KW, Meltzer, PS, George, DL and Vogelstein, B (1992). Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 358: 80-83.
22. Yamakuchi, M, Ferlito, M and Lowenstein, CJ (2008). miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci USA 105: 13421-13426.
23. Mandke, P, Wyatt, N, Fraser, J, Bates, B, Berberich, SJ and Markey, MP (2012). MicroRNA-34a modulates MDM4 expression via a target site in the open reading frame. PLoS ONE 7: e42034.
24. Chen, QR, Yu, LR, Tsang, P, Wei, JS, Song, YK, Cheuk, A et al. (2011). Systematic proteome analysis identifies transcription factor YY1 as a direct target of miR-34a. J Proteome Res 10: 479-487.
25. Sur, S, Pagliarini, R, Bunz, F, Rago, C, Diaz, LA Jr, Kinzler, KW et al. (2009). A panel of isogenic human cancer cells suggests a therapeutic approach for cancers with inactivated p53. Proc Natl Acad Sci USA 106: 3964-3969.
26. Weiss, MB, Vitolo, MI, Mohseni, M, Rosen, DM, Denmeade, SR, Park, BH et al. (2010). Deletion of p53 in human mammary epithelial cells causes chromosomal instability and altered therapeutic response. Oncogene 29: 4715-4724.
27. Brady, CA, Jiang, D, Mello, SS, Johnson, TM, Jarvis, LA, Kozak, MM et al. (2011). Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression. Cell 145: 571-583.
28. Dötsch, V, Bernassola, F, Coutandin, D, Candi, E and Melino, G (2010). p63 and p73, the ancestors of p53. Cold Spring Harb Perspect Biol 2: a004887.
29. Lagger, G, Doetzlhofer, A, Schuettengruber, B, Haidweger, E, Simboeck, E, Tischler, J et al. (2003). The tumor suppressor p53 and histone deacetylase 1 are antagonistic regulators of the cyclin-dependent kinase inhibitor p21/WAF1/CIP1 gene. Mol Cell Biol 23: 2669-2679. (Pubitemid 36403069)
30. Sowa, Y, Orita, T, Minamikawa, S, Nakano, K, Mizuno, T, Nomura, H et al. (1997). Histone deacetylase inhibitor activates the WAF1/Cip1 gene promoter through the Sp1 sites. Biochem Biophys Res Commun 241: 142-150. (Pubitemid 28033553)
31. Lagger, G, O'Carroll, D, Rembold, M, Khier, H, Tischler, J, Weitzer, G et al. (2002). Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J 21: 2672-2681. (Pubitemid 34619383)
32. Toledo, F, Krummel, KA, Lee, CJ, Liu, CW, Rodewald, LW, Tang, M et al. (2006). A mouse p53 mutant lacking the proline-rich domain rescues Mdm4 deficiency and provides insight into the Mdm2-Mdm4-p53 regulatory network. Cancer Cell 9: 273-285.
33. Abbas, T and Dutta, A (2009). p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 9: 400-414.
34. Christoffersen, NR, Shalgi, R, Frankel, LB, Leucci, E, Lees, M, Klausen, M et al. (2010). p53-independent upregulation of miR-34a during oncogene-induced senescence represses MYC. Cell Death Differ 17: 236-245.
35. Concepcion, CP, Han, YC, Mu, P, Bonetti, C, Yao, E, D'Andrea, A et al. (2012). Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet 8: e1002797.
36. Martín-Caballero, J, Flores, JM, García-Palencia, P and Serrano, M (2001). Tumor susceptibility of p21(Waf1/Cip1)-deficient mice. Cancer Res 61: 6234-6238.
37. Teramen, H, Tsukuda, K, Tanaka, N, Ueno, T, Kubo, T, Ando, M et al. (2011). Aberrant methylation of p21 gene in lung cancer and malignant pleural mesothelioma. Acta Med Okayama 65: 179-184.
38. Weil, D, Garçon, L, Harper, M, Duménil, D, Dautry, F and Kress, M (2002). Targeting the kinesin Eg5 to monitor siRNA transfection in mammalian cells. BioTechniques 33: 1244-1248. (Pubitemid 36008179)
39. Esquela-Kerscher, A, Trang, P, Wiggins, JF, Patrawala, L, Cheng, A, Ford, L et al. (2008). The let-7 microRNA reduces tumor growth in mouse models of lung cancer. Cell Cycle 7: 759-764. (Pubitemid 351520040)
40. Nakayama, GR, Caton, MC, Nova, MP and Parandoosh, Z (1997). Assessment of the Alamar Blue assay for cellular growth and viability in vitro. J Immunol Methods 204: 205-208. (Pubitemid 27262014)
41. Peltier, HJ and Latham, GJ (2008). Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 14: 844-852. (Pubitemid 351574906)
42. Trang, P, Medina, PP, Wiggins, JF, Ruffino, L, Kelnar, K, Omotola, M et al. (2010). Regression of murine lung tumors by the let-7 microRNA. Oncogene 29: 1580-1587.