HDAC inhibitors repress BARD1 isoform expression in acute myeloid leukemia cells via activation of miR-19a and/or b

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Lepore, Ilaria ^a   Dell'Aversana, Carmela ^a,b   Pilyugin, Maxim ^d   Conte, Mariarosaria ^a   Nebbioso, Angela ^a   De Bellis, Floriana ^a   Tambaro, Francesco P ^a,c   Izzo, Tiziana ^e   Garcia Manero, Guillermo ^c   Ferrara, Felicetto ^e   Irminger Finger, Irmgard ^d   Altucci, Lucia ^a,b  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^e CARDARELLI HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; ENTINOSTAT; MESSENGER RNA; MICRORNA; MICRORNA 19A; MICRORNA 19AB; UNCLASSIFIED DRUG; VORINOSTAT; BARD1 PROTEIN, HUMAN; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; ISOPROTEIN; MIRN19 MICRORNA, HUMAN; RNA; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE;

3' UNTRANSLATED REGION; ACUTE GRANULOCYTIC LEUKEMIA; ADULT; AGED; APOPTOSIS; ARTICLE; CLINICAL ARTICLE; EPIGENETICS; EXON; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; LEUKEMIA CELL; MALE; MIDDLE AGED; MORTALITY; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SOLID TUMOR; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HL 60 CELL LINE; K562 CELL LINE; LEUKEMIA, MYELOID, ACUTE; METABOLISM; U937 CELL LINE;

EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, LEUKEMIC; HISTONE DEACETYLASE INHIBITORS; HL-60 CELLS; HUMANS; HYDROXAMIC ACIDS; K562 CELLS; LEUKEMIA, MYELOID, ACUTE; MICRORNAS; PROTEIN ISOFORMS; RNA, NEOPLASM; TUMOR SUPPRESSOR PROTEINS; U937 CELLS; UBIQUITIN-PROTEIN LIGASES;

EID: 84892429247     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083018     Document Type: Article

References (45)

1. Conte M, Altucci L (2012) Molecular pathways: the complexity of the epigenome in cancer and recent clinical advances. Clin Cancer Res 18: 5526-5534. doi:10.1158/1078-0432.CCR-12-2037. PubMed: 22904103.
2. Wu JY, Vlastos AT, Pelte MF, Caligo MA, Bianco A et al. (2006) Aberrant expression of BARD1 in breast and ovarian cancers with poor prognosis. Int J Cancer 118: 1215-1226. doi:10.1002/ijc.21428. PubMed: 16152612.
3. Li L, Ryser S, Dizin E, Pils D, Krainer M et al. (2007) Oncogenic BARD1 isoforms expressed in gynecological cancers. Cancer Res 67: 11876-11885. doi:10.1158/0008-5472.CAN-07-2370. PubMed: 18089818.
4. Sporn JC, Hothorn T, Jung B (2011) BARD1 expression predicts outcome in colon cancer. Clin Cancer Res 17: 5451-5462. doi: 10.1158/1078-0432.CCR-11-0263. PubMed: 21693656.
5. Zhang YQ, Bianco A, Malkinson AM, Leoni VP, Frau G et al. (2012) BARD1: an independent predictor of survival in non-small cell lung cancer. Int J Cancer 131: 83-94. doi:10.1002/ijc.26346. PubMed: 21815143.
6. Bosse KR, Diskin SJ, Cole KA, Wood AC, Schnepp RW et al. (2012) Common variation at BARD1 results in the expression of an oncogenic isoform that influences neuroblastoma susceptibility and oncogenicity. Cancer Res 72: 2068-2078. doi:10.1158/1538-7445.AM2012-2068. PubMed: 22350409.
7. Irminger-Finger I, Jefford CE (2006) Is there more to BARD1 than BRCA1? Nat Rev Cancer 6: 382-391. doi:10.1038/nrc1878. PubMed: 16633366.
8. Ryser S, Dizin E, Jefford CE, Delaval B, Gagos S et al. (2009) Distinct roles of BARD1 isoforms in mitosis: full-length BARD1 mediates Aurora B degradation, cancer-associated BARD1beta scaffolds Aurora B and BRCA2. Cancer Res 69: 1125-1134. doi: 10.1158/0008-5472.SABCS-1125. PubMed: 19176389.
9. Choudhury AD, Xu H, Modi AP, Zhang W, Ludwig T et al. (2005) Hyperphosphorylation of the BARD1 tumor suppressor in mitotic cells. J Biol Chem 280: 24669-24679. doi:10.1074/jbc.M502446200. PubMed: 15855157.
10. Edwards RA, Lee MS, Tsutakawa SE, Williams RS, Nazeer I et al. (2008) The BARD1 C-terminal domain structure and interactions with polyadenylation factor CstF-50. Biochemistry 47: 11446-11456. doi: 10.1021/bi801115g. PubMed: 18842000.
11. Henderson BR (2005) Regulation of BRCA1, BRCA2 and BARD1 intracellular trafficking. Bioessays 27: 884-893. doi:10.1002/bies.20277. PubMed: 16108063.
12. Feki A, Jefford CE, Berardi P, Wu JY, Cartier L et al. (2005) BARD1 induces apoptosis by catalysing phosphorylation of p53 by DNA-damage response kinase. Oncogene 24: 3726-3736. doi:10.1038/sj.onc.1208491. PubMed: 15782130.
13. Irminger-Finger I, Leung WC, Li J, Dubois-Dauphin M, Harb J et al. (2001) Identification of BARD1 as mediator between proapoptotic stress and p53-dependent apoptosis. Mol Cell 8: 1255-1266. doi: 10.1016/S1097-2765(01) 00406-3. PubMed: 11779501.
14. Jefford CE, Feki A, Harb J, Krause KH, Irminger-Finger I (2004) Nuclear-cytoplasmic translocation of BARD1 is linked to its apoptotic activity. Oncogene 23: 3509-3520. doi:10.1038/sj.onc.1207427. PubMed: 15077185.
15. Gautier F, Irminger-Finger I, Grégoire M, Meflah K, Harb J (2000) Identification of an apoptotic cleavage product of BARD1 as an autoantigen: a potential factor in the antitumoral response mediated by apoptotic bodies. Cancer Res 60: 6895-6900. PubMed: 11156388.
16. Tembe V, Henderson BR (2007) BARD1 translocation to mitochondria correlates with Bax oligomerization, loss of mitochondrial membrane potential, and apoptosis. J Biol Chem 282: 20513-20522. doi:10.1074/jbc.M702627200. PubMed: 17510055.
17. Irminger-Finger I (2010) BARD1, a possible biomarker for breast and ovarian cancer. Gynecol Oncol 117: 211-215. doi:10.1016/j.ygyno.2009.10.079. PubMed: 19959210.
18. Mahadevan D, DiMento J, Croce KD, Riley C, George B et al. (2006) Transcriptosome and serum cytokine profiling of an atypical case of myelodysplastic syndrome with progression to acute myelogenous leukemia. Am J Hematol 81: 779-786. doi:10.1002/ajh.20690. PubMed: 16838325.
19. Marks PA, Breslow R (2007) Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol 25: 84-90. doi:10.1038/nbt1272. PubMed: 17211407.
20. Mercurio C, Minucci S, Pelicci PG (2010) Histone deacetylases and epigenetic therapies of hematological malignancies. Pharmacol Res 62: 18-34. doi:10.1016/j.phrs.2010.02.010. PubMed: 20219679.
21. O'Connor OA, Heaney ML, Schwartz L, Richardson S, Willim R et al. (2006) Clinical experience with intravenous and oral formulations of the novel histone deacetylase inhibitor suberoylanilide hydroxamic acid in patients with advanced hematologic malignancies. J Clin Oncol 24: 166-173. doi:10.1200/JCO.2005.01. 9679. PubMed: 16330674.
22. Mann BS, Johnson JR, He K, Sridhara R, Abraham S et al. (2007) Vorinostat for treatment of cutaneous manifestations of advanced primary cutaneous T-cell lymphoma. Clin Cancer Res 13: 2318-2322. doi:10.1158/1078-0432.CCR-06-2672. PubMed: 17438089.
23. Rosato RR, Almenara JA, Grant S (2003) The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21CIP1/WAF1 1. Cancer Res 63: 3637-3645. PubMed: 12839953.
24. Bracker TU, Sommer A, Fichtner I, Faus H, Haendler B et al. (2009) Efficacy of MS-275, a selective inhibitor of class I histone deacetylases, in human colon cancer models. Int J Oncol 35: 909-920. PubMed: 19724929.
25. Hess-Stumpp H, Bracker TU, Henderson D, Politz O (2007) MS-275, a potent orally available inhibitor of histone deacetylases - the development of an anticancer agent. Int J Biochem Cell Biol 39: 1388-1405. PubMed: 17383217.
26. Ryan QC, Headlee D, Acharya M, Sparreboom A, Trepel JB et al. (2005) Phase I and pharmacokinetic study of MS-275, a histone deacetylase inhibitor, in patients with advanced and refractory solid tumors or lymphoma. Journal of Clinical Oncology : Official Journal of the American Society Of Clinical Oncology 23: 3912-3922. doi:10.1200/JCO.2005.02.188.
27. Mai A, Massa S, Pezzi R, Simeoni S, Rotili D, et al. (2005) Class II (IIa)-selective histone deacetylase inhibitors. 1. Synthesis and biological evaluation of novel (aryloxopropenyl)pyrrolyl hydroxyamides. Journal of medicinal chemistry 48: 3344-3353.
28. Nebbioso A, Manzo F, Miceli M, Conte M, Manente L et al. (2009) Selective class II HDAC inhibitors impair myogenesis by modulating the stability and activity of HDAC-MEF2 complexes. EMBO Rep 10: 776-782. doi:10.1038/embor.2009. 88. PubMed: 19498465.
29. Scott GK, Marx C, Berger CE, Saunders LR, Verdin E et al. (2008) Destabilization of ERBB2 transcripts by targeting 3′ untranslated region messenger RNA associated HuR and histone deacetylase-6. Mol Cancer Res 6: 1250-1258. doi:10.1158/1541-7786.MCR-07-2110. PubMed: 18644987.
30. Breving K, Esquela-Kerscher A (2010) The complexities of microRNA regulation: mirandering around the rules. Int J Biochem Cell Biol 42: 1316-1329. PubMed: 19800023.
31. Wang Y, Blelloch R (2011) Cell cycle regulation by microRNAs in stem cells. Results Probl Cell Differ 53: 459-472. PubMed: 21630156.
32. Chan SP, Slack FJ. (2007) (2007) And now introducing mammalian mirtrons. Dev Cell 13: 605-607. doi:10.1016/j.devcel.2007.10.010. PubMed: 17981129.
33. Shan G (2010) RNA interference as a gene knockdown technique. Int J Biochem Cell Biol 42: 1243-1251. PubMed: 19442757.
34. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297. doi:10.1016/S0092-8674(04)00045-5. PubMed: 14744438.
35. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP et al. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105. doi:10.1016/j.molcel.2007.06.017. PubMed: 17612493.
36. Brueckner B, Stresemann C, Kuner R, Mund C, Musch T et al. (2007) The human let-7a-3 locus contains an epigenetically regulated microRNA gene with oncogenic function. Cancer Res 67: 1419-1423. doi:10.1158/0008-5472.CAN-06-4074. PubMed: 17308078.
37. Sato F, Tsuchiya S, Meltzer SJ, Shimizu K (2011) MicroRNAs and epigenetics. FEBS J 278: 1598-1609. doi:10.1111/j.1742-4658.2011.08089.x. PubMed: 21395977.
38. Garcia-Manero G, Tambaro FP, Bekele NB, Yang H, Ravandi F et al. (2012) Phase II trial of vorinostat with idarubicin and cytarabine for patients with newly diagnosed acute myelogenous leukemia or myelodysplastic syndrome. Journal of Clinical Oncology : Official Journal of the American Society Of Clinical Oncology 30: 2204-2210. doi:10.1200/JCO.2011.38.3265.
39. Beckett D, Kovaleva E, Schatz PJ (1999) A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Science : a Publication of the Protein Society 8: 921-929.
40. Olive V, Jiang I, He L (2010) mir-17-92, a cluster of miRNAs in the midst of the cancer network. International Journal of Biochemistry and Cell Biology 42: 1348-1354.
41. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K et al. (2005) A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 65: 9628-9632. doi:10.1158/0008-5472.CAN-05-2352. PubMed: 16266980.
42. Mavrakis KJ, Wolfe AL, Oricchio E, Palomero T, de Keersmaecker K et al. (2010) Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nat Cell Biol 12: 372-379. doi:10.1038/ncb2037. PubMed: 20190740.
43. Lin YW, Sheu JC, Liu LY, Chen CH, Lee HS et al. (1999) Loss of heterozygosity at chromosome 13q in hepatocellular carcinoma: identification of three independent regions. Eur J Cancer 35: 1730-1734. doi:10.1016/S0959- 8049(99)00205-1. PubMed: 10674021.
44. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146: 353-358. doi:10.1016/j.cell.2011.07.014. PubMed: 21802130.
45. Xu XM, Wang XB, Chen MM, Liu T, Li YX et al. (2012) MicroRNA-19a and -19b regulate cervical carcinoma cell proliferation and invasion by targeting CUL5. Cancer Lett 322: 148-158. doi:10.1016/j.canlet.2012.02.038. PubMed: 22561557.