Histone deacetylase inhibitor prevents cell growth in Burkitt's lymphoma by regulating PI3K/Akt pathways and leads to upregulation of miR-143, miR-145, and miR-101

Annals of Hematology

Volumn 93, Issue 6, 2014, Pages 983-993

  Dos Santos Ferreira, Ana Carolina ^a   Robaina, Marcela Cristina ^a   De Rezende, Lídia Maria Magalhães ^a   Severino, Patricia ^b   Klumb, Claudete Esteves ^a  

^a INSTITUTO NACIONAL DE CÂNCER   (Brazil)

^b HOSPITAL ISRAELITA ALBERT EINSTEIN   (Brazil)

Author keywords

Burkitt's lymphoma; Cell growth; HDACi; miRNA; PI3K

Indexed keywords

BUTYRIC ACID; ETOPOSIDE; HISTONE DEACETYLASE INHIBITOR; MICRORNA 101; MICRORNA 143; MICRORNA 145; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BURKITT LYMPHOMA; BURKITT LYMPHOMA CELL LINE; CANCER INHIBITION; CCND1 GENE; CDKN1A GENE; CELL VIABILITY; CELLULAR STRESS SIGNAL; CHEK2 GENE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME PHOSPHORYLATION; FAS GENE; G2 PHASE CELL CYCLE CHECKPOINT; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MDM4 GENE; NUCLEOTIDE SEQUENCE; ONTOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; S PHASE CELL CYCLE CHECKPOINT; SESN2 GENE; TUMOR SUPPRESSOR GENE; UPREGULATION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; BURKITT LYMPHOMA; BUTYRIC ACID; CELL CYCLE; CELL LINE, TUMOR; DRUG SYNERGISM; ETOPOSIDE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, MYC; HISTONE DEACETYLASE INHIBITORS; HUMANS; MICRORNAS; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, NEOPLASM; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84902344652     PISSN: 09395555     EISSN: 14320584     Source Type: Journal    
DOI: 10.1007/s00277-014-2021-4     Document Type: Article

References (49)

1. Gross TG, Termuhlen AM (2007) Pediatric non-Hodgkin's lymphoma. Curr Oncol Rep 9(6):459-465 (Pubitemid 350081482)
2. Dang CV (2012) MYC on the path to cancer. Cell 149(1):22-35. doi:10.1016/j.cell.2012.03.003
3. Klapproth K, Wirth T (2010) Advances in the understanding of MYC-induced lymphomagenesis. Br J Haematol 149(4):484-497. doi:10.1111/j.1365-2141.2010. 08159.x
4. Meyer N, Kim SS, Penn LZ (2006) The Oscar-worthy role of Myc in apoptosis. Semin Cancer Biol 16(4):275 -287. doi:10.1016/j.semcancer.2006.07.011
5. Hecht JL, Aster JC (2000) Molecular biology of Burkitt's lymphoma. J Clin Oncol Off J Am Soc Clin Oncol 18(21):3707-3721
6. Klumb CE, Furtado DR, de Resende LM, Carrico MK, Coelho AM, de Meis E, Maia RC, Rumjanek FD (2003) DNA sequence profile of TP53 gene mutations in childhood B-cell non-Hodgkin 's lymphomas: prognostic implications. Eur J Haematol 71(2):81-90 (Pubitemid 36951640)
7. Paschos K, Parker GA, Watanatanasup E, White RE, Allday MJ (2012) BIM promoter directly targeted by EBNA3C in polycomb-mediated repression by EBV. Nucleic Acids Res 40(15):7233-7246. doi:10.1093/nar/gks391
8. Paschos K, Smith P, Anderton E, Middeldorp JM, White RE, Allday MJ (2009) Epstein-Barr virus latency in B cells leads to epigenetic repression and CpG methylation of the tumour suppressor gene Bim. PLoS Pathog 5(6):e1000492. doi:10.1371/journal.ppat.1000492
9. Sander S, Calado DP, Srinivasan L, Kochert K, Zhang B, Rosolowski M, Rodig SJ, Holzmann K, Stilgenbauer S, Siebert R, Bullinger L, Rajewsky K (2012) Synergy between PI3K signaling and MYC in Burkitt lymphomagenesis. Cancer Cell 22(2):167-179. doi:10.1016/j.ccr.2012.06.012
10. Schmitz R, Young RM, Ceribelli M, Jhavar S, Xiao W, Zhang M, Wright G, Shaffer AL, Hodson DJ, Buras E, Liu X, Powell J, Yang Y, Xu W, Zhao H, Kohlhammer H, Rosenwald A, Kluin P, Muller-Hermelink HK, Ott G, Gascoyne RD, Connors JM, Rimsza LM, Campo E, Jaffe ES, Delabie J, Smeland EB, Ogwang MD, Reynolds SJ, Fisher RI, Braziel RM, Tubbs RR, Cook JR, Weisenburger DD, Chan WC, Pittaluga S, Wilson W, Waldmann TA, Rowe M, Mbulaiteye SM, Rickinson AB, Staudt LM (2012) Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature 490(7418):116-120. doi:10.1038/nature11378
11. Carnero A (2010) The PKB/AKT pathway in cancer. Curr Pharm Des 16(1):34-44
12. Rasul A, Ding C, Li X, Khan M, Yi F, Ali M, Ma T (2012) Dracorhodin perchlorate inhibits PI3K/Akt and NF-kappaB activation, up-regulates the expression of p53, and enhances apoptosis. Apoptosis: Int J Programmed Cell Death 17(10):1104-1119. doi:10.1007/s10495-012-0742-1
13. Lee KB, Byun HJ, Park SH, Park CY, Lee SH, Rho SB (2012) CYR61 controls p53 and NF-kappaB expression through PI3K/Akt/mTOR pathways in carboplatin-induced ovarian cancer cells. Cancer Lett 315(1):86-95. doi:10.1016/j.canlet.2011.10.016
14. Klangby U, Okan I, Magnusson KP, Wendland M, Lind P, Wiman KG (1998) p16/INK4a and p15/INK4b gene methylation and absence of p16/INK4a mRNA and protein expression in Burkitt's lymphoma. Blood 91(5):1680-1687 (Pubitemid 28110333)
15. de Yebenes VG, Bartolome-Izquierdo N, Ramiro AR (2013) Regulation of B-cell development and function by microRNAs. Immunol Rev 253(1):25-39. doi:10.1111/imr.12046
16. Jansson MD, Lund AH (2012) MicroRNA and cancer. Mol Oncol 6(6):590-610. doi:10.1016/j.molonc.2012.09.006
17. Dos Santos Ferreira AC, Fernandes RA, Kwee JK, Klumb CE (2012) Histone deacetylase inhibitor potentiates chemotherapy-induced apoptosis through Bim upregulation in Burkitt's lymphoma cells. J Cancer Res Clin Oncol 138(2):317-325. doi:10.1007/s00432-011-1093-y
18. Vasiljevic N, Wu K, Brentnall AR, Kim DC, Thorat MA, Kudahetti SC, Mao X, Xue L, Yu Y, Shaw GL, Beltran L, Lu YJ, Berney DM, Cuzick J, Lorincz AT (2011) Absolute quantitation of DNA methylation of 28 candidate genes in prostate cancer using pyrosequencing. Dis Markers 30(4):151-161. doi:10.3233/DMA-2011- 0790
19. Bader AG, Kang S, Zhao L, Vogt PK (2005) Oncogenic PI3K deregulates transcription and translation. Nat Rev Cancer 5(12):921-929. doi:10.1038/nrc1753 (Pubitemid 41766781)
20. Ou JN, Torrisani J, Unterberger A, Provencal N, Shikimi K, Karimi M, Ekstrom TJ, Szyf M (2007) Histone deacetylase inhibitor Trichostatin A induces global and gene-specific DNA demethylation in human cancer cell lines. Biochem Pharmacol 73(9):1297-1307. doi:10.1016/j.bcp.2006.12.032 (Pubitemid 46452588)
21. Crump M, Coiffier B, Jacobsen ED, Sun L, Ricker JL, Xie H, Frankel SR, Randolph SS, Cheson BD (2008) Phase II trial of oral vorinostat (suberoylanilide hydroxamic acid) in relapsed diffuse large-B-cell lymphoma. Ann Oncol: Off J Eur Soc Med Oncol/ESMO 19(5):964-969. doi:10.1093/annonc/mdn031
22. Tan J, Cang S, Ma Y, Petrillo RL, Liu D (2010) Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J Hematol Oncol 3:5. doi:10.1186/1756-8722-3-5
23. Siegel D, Hussein M, Belani C, Robert F, Galanis E, Richon VM, Garcia-Vargas J, Sanz-Rodriguez C, Rizvi S (2009) Vorinostat in solid and hematologic malignancies. J Hematol Oncol 2:31. doi:10.1186/1756-8722-2-31
24. Atra A, Gerrard M, Hobson R, Imeson JD, Hann IM, Pinkerton CR (2001) Outcome of relapsed or refractory childhood B-cell acute lymphoblastic leukaemia and B-cell non-Hodgkin's lymphoma treated with the UKCCSG 9003/9002 protocols. Br J Haematol 112(4):965-968 (Pubitemid 32322922)
25. Cairo MS, Sposto R, Perkins SL, Meadows AT, Hoover-Regan ML, Anderson JR, Siegel SE, Lones MA, Tedeschi-Blok N, Kadin ME, Kjeldsberg CR, Wilson JF, Sanger W, Morris E, Krailo MD, Finlay JL (2003) Burkitt's and Burkitt-like lymphoma in children and adolescents: a review of the Children's Cancer Group experience. Br J Haematol 120(4):660-670 (Pubitemid 36255868)
26. Griffin TC, Weitzman S, Weinstein H, Chang M, Cairo M, Hutchison R, Shiramizu B, Wiley J, Woods D, Barnich M, Gross TG (2009) A study of rituximab and ifosfamide, carboplatin, and etoposide chemotherapy in children with recurrent/refractory B-cell (CD20+) non-Hodgkin lymphoma and mature B-cell acute lymphoblastic leukemia: a report from the Children's Oncology Group. Pediatr Blood Cancer 52(2):177-181. doi:10.1002/pbc.21753
27. Lambert MP, Herceg Z (2008) Epigenetics and cancer, 2nd IARC meeting, Lyon, France, 6 and 7 December 2007. Mol Oncol 2(1):33-40. doi:10.1016/j.molonc. 2008.03.005
28. Shao W, Growney JD, Feng Y, O'Connor G, Pu M, Zhu W, Yao YM, Kwon P, Fawell S, Atadja P (2010) Activity of deacetylase inhibitor panobinostat (LBH589) in cutaneous T-cell lymphoma models: defining molecular mechanisms of resistance. Int J Cancer J Int Du Cancer 127(9):2199-2208. doi:10.1002/ijc.25218
29. Garcia-Manero G, Kantarjian HM, Sanchez-Gonzalez B, Yang H, Rosner G, Verstovsek S, Rytting M, Wierda WG, Ravandi F, Koller C, Xiao L, Faderl S, Estrov Z, Cortes J, O'Brien S, Estey E, Bueso-Ramos C, Fiorentino J, Jabbour E, Issa JP (2006) Phase 1/2 study of the combination of 5-aza-2′- deoxycytidine with valproic acid in patients with leukemia. Blood 108(10):3271-3279. doi:10.1182/blood-2006-03-009142
30. Dominguez-Sola D, Dalla-Favera R (2012) Burkitt lymphoma: much more than MYC. Cancer Cell 22(2):141-142. doi:10.1016/j.ccr.2012.07.018
31. Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296(5573):1655-1657. doi:10.1126/science.296.5573.1655
32. Jasek E, Lis GJ, Jasinska M, Jurkowska H, Litwin JA (2012) Effect of histone deacetylase inhibitors trichostatin A and valproic acid on etoposide-induced apoptosis in leukemia cells. Anticancer Res 32(7):2791-2799
33. Guan H, Xie L, Klapproth K, Weitzer CD, Wirth T, Ushmorov A (2013) Decitabine represses translocated MYC oncogene in Burkitt lymphoma. J Pathol 229(5):775-783. doi:10.1002/path.4164
34. Milutinovic S, D'Alessio AC, Detich N, Szyf M (2007) Valproate induces widespread epigenetic reprogramming which involves demethylation of specific genes. Carcinogenesis 28(3):560-571. doi:10.1093/carcin/bgl167 (Pubitemid 46523352)
35. Schwartz B, Avivi-Green C, Polak-Charcon S (1998) Sodium butyrate induces retinoblastoma protein dephosphorylation, p16 expression and growth arrest of colon cancer cells. Mol Cell Biochem 188(1-2):21-30 (Pubitemid 28493314)
36. Sanchez-Beato M, Sanchez-Aguilera A, Piris MA (2003) Cell cycle deregulation in B-cell lymphomas. Blood 101(4):1220-1235. doi:10.1182/blood- 2002-07-2009 (Pubitemid 36182489)
37. Iio A, Nakagawa Y, Hirata I, Naoe T, Akao Y (2010) Identification of non-coding RNAs embracing microRNA-143/145 cluster. Mol Cancer 9:136. doi:10.1186/1476-4598-9-136
38. Di Lisio L, Sanchez-Beato M, Gomez-Lopez G, Rodriguez ME, Montes-Moreno S, Mollejo M, Menarguez J, Martinez MA, Alves FJ, Pisano DG, Piris MA, Martinez N (2012) MicroRNA signatures in B-cell lymphomas. Blood Cancer J 2(2):e57. doi:10.1038/bcj.2012.1
39. Akao Y, Nakagawa Y, Hirata I, Iio A, Itoh T, Kojima K, Nakashima R, Kitade Y, Naoe T (2010) Role of anti-oncomirs miR-143 and -145 in human colorectal tumors. Cancer Gene Ther 17(6):398-408. doi:10.1038/cgt.2009.88
40. Akao Y, Nakagawa Y, Kitade Y, Kinoshita T, Naoe T (2007) Downregulation of microRNAs-143 and -145 in B-cell malignancies. Cancer Sci 98(12):1914-1920. doi:10.1111/j.1349-7006.2007.00618.x (Pubitemid 350002197)
41. Sachdeva M, Zhu S, Wu F, Wu H, Walia V, Kumar S, Elble R, Watabe K, Mo YY (2009) p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc Natl Acad Sci U S A 106(9):3207-3212. doi:10.1073/pnas.0808042106
42. He XP, Shao Y, Li XL, Xu W, Chen GS, Sun HH, Xu HC, Xu X, Tang D, Zheng XF, Xue YP, Huang GC, Sun WH (2012) Downregulation of miR-101 in gastric cancer correlates with cyclooxygenase-2 overexpression and tumor growth. FEBS J 279(22):4201-4212. doi:10.1111/febs.12013
43. Wang HJ, Ruan HJ, He XJ, Ma YY, Jiang XT, Xia YJ, Ye ZY, Tao HQ (2010) MicroRNA-101 is down-regulated in gastric cancer and involved in cell migration and invasion. Eur J Cancer 46(12):2295-2303. doi:10.1016/j.ejca.2010.05.012
44. Smits M, Nilsson J, Mir SE, van der Stoop PM, Hulleman E, Niers JM, de Witt Hamer PC, Marquez VE, Cloos J, Krichevsky AM, Noske DP, Tannous BA, Wurdinger T (2010) miR-101 is down-regulated in glioblastoma resulting in EZH2-induced proliferation, migration, and angiogenesis. Oncotarget 1(8):710-720
45. Cho HM, Jeon HS, Lee SY, Jeong KJ, Park SY, Lee HY, Lee JU, Kim JH, Kwon SJ, Choi E, Na MJ, Kang J, Son JW (2011) microRNA-101 inhibits lung cancer invasion through the regulation of enhancer of zeste homolog 2. Exp Ther Med 2(5):963-967. doi:10.3892/etm.2011.284
46. Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM, Dang CV, Thomas-Tikhonenko A, Mendell JT (2008) Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 40(1):43-50. doi:10.1038/ng.2007.30
47. Robertus JL, Kluiver J, Weggemans C, Harms G, Reijmers RM, Swart Y, Kok K, Rosati S, Schuuring E, van Imhoff G, Pals ST, Kluin P, van den Berg A (2010) MiRNA profiling in B non-Hodgkin lymphoma: a MYC-related miRNA profile characterizes Burkitt lymphoma. Br J Haematol 149(6):896-899. doi:10.1111/j.1365-2141.2010.08111.x
48. Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG, Jin DY, Costello JF, Liang R (2010) Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 31(4):745-750. doi:10.1093/carcin/bgq033
49. Bueno MJ, Perez de Castro I, Gomez de Cedron M, Santos J, Calin GA, Cigudosa JC, Croce CM, Fernandez-Piqueras J, Malumbres M (2008) Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell 13(6):496-506. doi:10.1016/j.ccr.2008.04.018 (Pubitemid 351763902)