LTR12 promoter activation in a broad range of human tumor cells by HDAC inhibition

Oncotarget

Volumn 7, Issue 23, 2016, Pages 33484-33497

  Krönung, Sonja K ^a   Beyer, Ulrike ^a,b   Chiaramonte, Maria Luisa ^c   Dolfini, Diletta ^c   Mantovani, Roberto ^c   Dobbelstein, Matthias ^a  

^a University of Göttingen   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

Factor binding; Genome wide gene expression analysis

Indexed keywords

CASPASE 3; DROXINOSTAT; ENTINOSTAT; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; MESSENGER RNA; MOCETINOSTAT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUCLEAR FACTOR Y; PCI 34051; SHORT HAIRPIN RNA; TRICHOSTATIN A; TUBASTATIN A HYDROCHLORIDE; UNCLASSIFIED DRUG; VORINOSTAT;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; CANCER CELL LINE; CARCINOMA CELL LINE; CGREF1 GENE; COMPUTER MODEL; CONTROLLED STUDY; DHRS2 GENE; DRUG EFFECT; DRUG MECHANISM; ENZYME INHIBITION; FEMALE; GENE; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENOMIC BINDING; HELA CELL LINE; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LONG TERMINAL REPEAT; LONG TERMINAL REPEAT 12; MALE; MOLECULAR DYNAMICS; OSTEOSARCOMA CELL LINE; PROMOTER REGION; SEMA4D GENE; TESTICULAR CANCER CELL LINE; TNFRSF10B GENE; TP63 GENE; TRANSCRIPTION REGULATION; TUMOR CELL; DRUG EFFECTS; ENDOGENOUS RETROVIRUS; GENE EXPRESSION REGULATION; GENETICS; NEOPLASM; TUMOR CELL LINE;

CELL LINE, TUMOR; ENDOGENOUS RETROVIRUSES; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASE INHIBITORS; HUMANS; NEOPLASMS; PROMOTER REGIONS, GENETIC; TERMINAL REPEAT SEQUENCES;

EID: 84973619392     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.9255     Document Type: Article

References (65)

1. Pray L. Transposons, or jumping genes: Not junk DNA. Nature Education. 2008; 1:32.
2. de Koning AP, Gu W, Castoe TA, Batzer MA and Pollock DD. Repetitive elements may comprise over two-thirds of the human genome. PLoS genetics. 2011; 7:e1002384.
3. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, et al. Initial sequencing and analysis of the human genome. Nature. 2001; 409:860-921.
4. Consortium EP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012; 489:57-74.
5. Boeke JD and Stoye JP. (1997). Retrotransposons, Endogenous Retroviruses, and the Evolution of Retroelements. In: Coffin JM, Hughes SH and Varmus HE, eds. Retroviruses. (Cold Spring Harbor (NY).
6. Bannert N and Kurth R. The evolutionary dynamics of human endogenous retroviral families. Annual review of genomics and human genetics. 2006; 7:149-173.
7. Stoye JP. Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nature reviews Microbiology. 2012; 10:395-406.
8. Jern P and Coffin JM. Effects of retroviruses on host genome function. Annual review of genetics. 2008; 42:709-732.
9. Weiss RA. The discovery of endogenous retroviruses. Retrovirology. 2006; 3:67.
10. Larsson E, Kato N and Cohen M. Human endogenous proviruses. Current topics in microbiology and immunology. 1989; 148:115-132.
11. Stoye JP. Endogenous retroviruses: still active after all these years? Current biology. 2001; 11:R914-916.
12. Gifford WD, Pfaff SL and Macfarlan TS. Transposable elements as genetic regulatory substrates in early development. Trends in cell biology. 2013; 23:218-226.
13. Temin HM. Structure, variation and synthesis of retrovirus long terminal repeat. Cell. 1981; 27:1-3.
14. Cohen CJ, Lock WM and Mager DL. Endogenous retroviral LTRs as promoters for human genes: a critical assessment. Gene. 2009; 448:105-114.
15. Levin HL and Moran JV. Dynamic interactions between transposable elements and their hosts. Nature reviews Genetics. 2011; 12:615-627.
16. Crichton JH, Dunican DS, Maclennan M, Meehan RR and Adams IR. Defending the genome from the enemy within: mechanisms of retrotransposon suppression in the mouse germline. Cellular and molecular life sciences. 2014; 71:1581-1605.
17. Rowe HM and Trono D. Dynamic control of endogenous retroviruses during development. Virology. 2011; 411:273-287.
18. Leung DC and Lorincz MC. Silencing of endogenous retroviruses: when and why do histone marks predominate? Trends in biochemical sciences. 2012; 37:127-133.
19. Beyer U, Kronung SK, Leha A, Walter L and Dobbelstein M. Comprehensive identification of genes driven by ERV9-LTRs reveals TNFRSF10B as a re-activatable mediator of testicular cancer cell death. Cell death and differentiation. 2016; 23:64-75.
20. Beyer U, Moll-Rocek J, Moll UM and Dobbelstein M. Endogenous retrovirus drives hitherto unknown proapoptotic p63 isoforms in the male germ line of humans and great apes. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108:3624-3629.
21. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O and Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenetic and genome research. 2005; 110:462-467.
22. Wu GS, Burns TF, McDonald ER, 3rd, Jiang W, Meng R, Krantz ID, Kao G, Gan DD, Zhou JY, Muschel R, Hamilton SR, Spinner NB, Markowitz S, Wu G and el-Deiry WS. KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nature genetics. 1997; 17:141-143.
23. Dejosez M, Ramp U, Mahotka C, Krieg A, Walczak H, Gabbert HE and Gerharz CD. Sensitivity to TRAIL/APO-2L-mediated apoptosis in human renal cell carcinomas and its enhancement by topotecan. Cell death and differentiation. 2000; 7:1127-1136.
24. Romier C, Cocchiarella F, Mantovani R and Moras D. The NF-YB/NF-YC structure gives insight into DNA binding and transcription regulation by CCAAT factor NF-Y. The Journal of biological chemistry. 2003; 278:1336-1345.
25. Nardini M, Gnesutta N, Donati G, Gatta R, Forni C, Fossati A, Vonrhein C, Moras D, Romier C, Bolognesi M and Mantovani R. Sequence-specific transcription factor NF-Y displays histone-like DNA binding and H2B-like ubiquitination. Cell. 2013; 152:132-143.
26. Yu X, Zhu X, Pi W, Ling J, Ko L, Takeda Y and Tuan D. The long terminal repeat (LTR) of ERV-9 human endogenous retrovirus binds to NF-Y in the assembly of an active LTR enhancer complex NF-Y/MZF1/GATA-2. The Journal of biological chemistry. 2005; 280:35184-35194.
27. Fleming JD, Pavesi G, Benatti P, Imbriano C, Mantovani R and Struhl K. NF-Y coassociates with FOS at promoters, enhancers, repetitive elements, and inactive chromatin regions, and is stereo-positioned with growth-controlling transcription factors. Genome research. 2013; 23:1195-1209.
28. Salsi V, Caretti G, Wasner M, Reinhard W, Haugwitz U, Engeland K and Mantovani R. Interactions between p300 and multiple NF-Y trimers govern cyclin B2 promoter function. The Journal of biological chemistry. 2003; 278:6642-6650.
29. Jin S and Scotto KW. Transcriptional regulation of the MDR1 gene by histone acetyltransferase and deacetylase is mediated by NF-Y. Molecular and cellular biology. 1998; 18:4377-4384.
30. Peng Y and Jahroudi N. The NFY transcription factor functions as a repressor and activator of the von Willebrand factor promoter. Blood. 2002; 99:2408-2417.
31. Currie RA. NF-Y is associated with the histone acetyltransferases GCN5 and P/CAF. The Journal of biological chemistry. 1998; 273:1430-1434.
32. Peng Y, Stewart D, Li W, Hawkins M, Kulak S, Ballermann B and Jahroudi N. Irradiation modulates association of NF-Y with histone-modifying cofactors PCAF and HDAC. Oncogene. 2007; 26:7576-7583.
33. Johnstone RW. Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nature reviews Drug discovery. 2002; 1:287-299.
34. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I and Zhao K. High-resolution profiling of histone methylations in the human genome. Cell. 2007; 129:823-837.
35. Peng L and Seto E. Deacetylation of nonhistone proteins by HDACs and the implications in cancer. Handb Exp Pharmacol. 2011; 206:39-56.
36. Singh BN, Zhang G, Hwa YL, Li J, Dowdy SC and Jiang SW. Nonhistone protein acetylation as cancer therapy targets. Expert review of anticancer therapy. 2010; 10:935-954.
37. Falkenberg KJ and Johnstone RW. Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nature reviews Drug discovery. 2014; 13:673-691.
38. Glozak MA and Seto E. Histone deacetylases and cancer. Oncogene. 2007; 26:5420-5432.
39. Ropero S and Esteller M. The role of histone deacetylases (HDACs) in human cancer. Molecular oncology. 2007; 1:19-25.
40. Yang XJ and Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nature reviews Molecular cell biology. 2008; 9:206-218.
41. Bertrand P. Inside HDAC with HDAC inhibitors. European journal of medicinal chemistry. 2010; 45:2095-2116.
42. Martinet N and Bertrand P. Interpreting clinical assays for histone deacetylase inhibitors. Cancer management and research. 2011; 3:117-141.
43. Witt O, Deubzer HE, Milde T and Oehme I. HDAC family: What are the cancer relevant targets? Cancer letters. 2009; 277:8-21.
44. West AC and Johnstone RW. New and emerging HDAC inhibitors for cancer treatment. The Journal of clinical investigation. 2014; 124:30-39.
45. Mann BS, Johnson JR, Cohen MH, Justice R and Pazdur R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. The oncologist. 2007; 12:1247-1252.
46. Dokmanovic M, Clarke C and Marks PA. Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res. 2007; 5:981-989.
47. Grant S, Easley C and Kirkpatrick P. Vorinostat. Nature reviews Drug discovery. 2007; 6:21-22.
48. Chen HJ, Carr K, Jerome RE and Edenberg HJ. A retroviral repetitive element confers tissue-specificity to the human alcohol dehydrogenase 1C (ADH1C) gene. DNA and cell biology. 2002; 21:793-801.
49. Benatti P, Dolfini D, Vigano A, Ravo M, Weisz A and Imbriano C. Specific inhibition of NF-Y subunits triggers different cell proliferation defects. Nucleic acids research. 2011; 39:5356-5368.
50. Oldfield AJ, Yang P, Conway AE, Cinghu S, Freudenberg JM, Yellaboina S and Jothi R. Histone-fold domain protein NF-Y promotes chromatin accessibility for cell type-specific master transcription factors. Mol Cell. 2014; 55:708-722.
51. Chuang DM, Leng Y, Marinova Z, Kim HJ and Chiu CT. Multiple roles of HDAC inhibition in neurodegenerative conditions. Trends Neurosci. 2009; 32:591-601.
52. Yasui W, Oue N, Ono S, Mitani Y, Ito R and Nakayama H. Histone acetylation and gastrointestinal carcinogenesis. Annals of the New York Academy of Sciences. 2003; 983:220-231.
53. Fraga MF, Ballestar E, Villar-Garea A, Boix-Chornet M, Espada J, Schotta G, Bonaldi T, Haydon C, Ropero S, Petrie K, Iyer NG, Perez-Rosado A, Calvo E, Lopez JA, Cano A, Calasanz MJ, et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nature genetics. 2005; 37:391-400.
54. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, Greven MC, Pierce BG, Dong X, Kundaje A, Cheng Y, Rando OJ, Birney E, Myers RM, Noble WS, Snyder M and Weng Z. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome research. 2012; 22:1798-1812.
55. Butler LM, Zhou X, Xu WS, Scher HI, Rifkind RA, Marks PA and Richon VM. The histone deacetylase inhibitor SAHA arrests cancer cell growth, up-regulates thioredoxinbinding protein-2, and down-regulates thioredoxin. Proceedings of the National Academy of Sciences of the United States of America. 2002; 99:11700-11705.
56. Kato T, Shimono Y, Hasegawa M, Jijiwa M, Enomoto A, Asai N, Murakumo Y and Takahashi M. Characterization of the HDAC1 complex that regulates the sensitivity of cancer cells to oxidative stress. Cancer Res. 2009; 69:3597-3604.
57. Grant C, Rahman F, Piekarz R, Peer C, Frye R, Robey RW, Gardner ER, Figg WD and Bates SE. Romidepsin: a new therapy for cutaneous T-cell lymphoma and a potential therapy for solid tumors. Expert review of anticancer therapy. 2010; 10:997-1008.
58. Gojo I, Jiemjit A, Trepel JB, Sparreboom A, Figg WD, Rollins S, Tidwell ML, Greer J, Chung EJ, Lee MJ, Gore SD, Sausville EA, Zwiebel J and Karp JE. Phase 1 and pharmacologic study of MS-275, a histone deacetylase inhibitor, in adults with refractory and relapsed acute leukemias. Blood. 2007; 109:2781-2790.
59. Siu LL, Pili R, Duran I, Messersmith WA, Chen EX, Sullivan R, MacLean M, King S, Brown S, Reid GK, Li Z, Kalita AM, Laille EJ, Besterman JM, Martell RE and Carducci MA. Phase I study of MGCD0103 given as a three-times-per-week oral dose in patients with advanced solid tumors. Journal of clinical oncology. 2008; 26:1940-1947.
60. Denissov S, van Driel M, Voit R, Hekkelman M, Hulsen T, Hernandez N, Grummt I, Wehrens R and Stunnenberg H. Identification of novel functional TBP-binding sites and general factor repertoires. The EMBO journal. 2007; 26:944-954.
61. Messeguer X, Escudero R, Farre D, Nunez O, Martinez J and Alba MM. PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics. 2002; 18:333-334.
62. Farre D, Roset R, Huerta M, Adsuara JE, Rosello L, Alba MM and Messeguer X. Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic acids research. 2003; 31:3651-3653.
63. Liu T, Ortiz JA, Taing L, Meyer CA, Lee B, Zhang Y, Shin H, Wong SS, Ma J, Lei Y, Pape UJ, Poidinger M, Chen Y, Yeung K, Brown M, Turpaz Y, et al. Cistrome: an integrative platform for transcriptional regulation studies. Genome biology. 2011; 12:R83.
64. Benatti P, Belluti S, Miotto B, Neusiedler J, Dolfini D, Drac M, Basile V, Schwob E, Mantovani R, Blow JJ and Imbriano C. Direct non transcriptional role of NF-Y in DNA replication. Biochim Biophys Acta. 2015; 1863:673-685.
65. Kohany O, Gentles AJ, Hankus L and Jurka J. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC bioinformatics. 2006; 7:474.