Targeting cancer epigenetics: Linking basic biology to clinical medicine

Advanced Drug Delivery Reviews

Volumn 95, Issue , 2015, Pages 56-64

  Shinjo, Keiko ^a   Kondo, Yutaka ^a  

^a NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

Author keywords

Biomarker; DNA methylation; Epigenetic therapy; Histone modification; Liquid biopsy

Indexed keywords

ALKYLATION; BIOMARKERS; DIAGNOSIS; DNA; GENE EXPRESSION; METHYLATION; TUMORS;

DNA METHYLATION; EPIGENETIC ALTERATIONS; EPIGENETIC MECHANISMS; EPIGENETIC THERAPY; GENE EXPRESSION PATTERNS; HISTONE MODIFICATION; SELECTIVE INHIBITORS; TRANSCRIPTIONAL PROGRAM;

DISEASES;

AZACITIDINE; BROMODOMAIN INHIBITOR; CELL FREE DNA; DNA; DNA METHYLTRANSFERASE INHIBITOR; GLUTATHIONE TRANSFERASE P1; HISTONE DEACETYLASE INHIBITOR; ISOCITRATE DEHYDROGENASE 1; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PINOMETOSTAT; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; RETINOIC ACID; SEPTIN; SEPTIN 9; TAMOXIFEN; TAZEMETOSTAT; TEMOZOLOMIDE; TRANSCRIPTION FACTOR EZH2; TRANYLCYPROMINE; UNCLASSIFIED DRUG; BIOLOGICAL MARKER;

ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MYELOBLASTIC LEUKEMIA; ADJUVANT THERAPY; ARTICLE; B CELL LYMPHOMA; BLADDER CANCER; BREAST CANCER; CANCER DIAGNOSIS; CANCER GENETICS; CANCER PROGNOSIS; CANCER SCREENING; COLORECTAL CANCER; CUTANEOUS T CELL LYMPHOMA; DIFFERENTIAL DIAGNOSIS; DNA METHYLATION; EPIGENETICS; FECES ANALYSIS; GLIOMA; HISTONE MODIFICATION; HUMAN; MUTATIONAL ANALYSIS; MYELODYSPLASTIC SYNDROME; NEXT GENERATION SEQUENCING; NON SMALL CELL LUNG CANCER; NONHUMAN; PERIPHERAL T CELL LYMPHOMA; PERSONALIZED MEDICINE; PRIORITY JOURNAL; SOLID TUMOR; TREATMENT RESPONSE; URINALYSIS; CLINICAL MEDICINE; GENETIC EPIGENESIS; GENETICS; NEOPLASMS;

BIOMARKERS; CLINICAL MEDICINE; DNA METHYLATION; EPIGENESIS, GENETIC; HUMANS; NEOPLASMS;

EID: 84955197707     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2015.10.006     Document Type: Review

References (104)

1. Feinberg A.P., Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983, 301:89-92.
2. Ohnishi K., Semi K., Yamamoto T., Shimizu M., Tanaka A., Mitsunaga K., Okita K., Osafune K., Arioka Y., Maeda T., Soejima H., Moriwaki H., Yamanaka S., Woltjen K., Yamada Y. Premature termination of reprogramming in vivo leads to cancer development through altered epigenetic regulation. Cell 2014, 156:663-677.
3. Jones P.A., Laird P.W. Cancer epigenetics comes of age. Nat. Genet. 1999, 21:163-167.
4. Jones P.A., Baylin S.B. The epigenomics of cancer. Cell 2007, 128:683-692.
5. Hegi M.E., Diserens A.C., Gorlia T., Hamou M.F., de Tribolet N., Weller M., Kros J.M., Hainfellner J.A., Mason W., Mariani L., Bromberg J.E., Hau P., Mirimanoff R.O., Cairncross J.G., Janzer R.C., Stupp R. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 2005, 352:997-1003.
6. Laird P.W. The power and the promise of DNA methylation markers. Nat. Rev. Cancer 2003, 3:253-266.
7. Schwarzenbach H., Hoon D.S., Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer 2011, 11:426-437.
8. Fleischhacker M., Schmidt B. Circulating nucleic acids (CNAs) and cancer-a survey. Biochim. Biophys. Acta 2007, 1775:181-232.
9. Dawson S.J., Tsui D.W., Murtaza M., Biggs H., Rueda O.M., Chin S.F., Dunning M.J., Gale D., Forshew T., Mahler-Araujo B., Rajan S., Humphray S., Becq J., Halsall D., Wallis M., Bentley D., Caldas C., Rosenfeld N. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N. Engl. J. Med. 2013, 368:1199-1209.
10. deVos T., Tetzner R., Model F., Weiss G., Schuster M., Distler J., Steiger K.V., Grutzmann R., Pilarsky C., Habermann J.K., Fleshner P.R., Oubre B.M., Day R., Sledziewski A.Z., Lofton-Day C. Circulating methylated SEPT9 DNA in plasma is a biomarker for colorectal cancer. Clin. Chem. 2009, 55:1337-1346.
11. Church T.R., Wandell M., Lofton-Day C., Mongin S.J., Burger M., Payne S.R., Castanos-Velez E., Blumenstein B.A., Rosch T., Osborn N., Snover D., Day R.W., Ransohoff D.F. Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut 2014, 63:317-325.
12. Johnson D.A., Barclay R.L., Mergener K., Weiss G., Konig T., Beck J., Potter N.T. Plasma Septin9 versus fecal immunochemical testing for colorectal cancer screening: a prospective multicenter study. PLoS One 2014, 9.
13. Fiegl H., Millinger S., Mueller-Holzner E., Marth C., Ensinger C., Berger A., Klocker H., Goebel G., Widschwendter M. Circulating tumor-specific DNA: a marker for monitoring efficacy of adjuvant therapy in cancer patients. Cancer Res. 2005, 65:1141-1145.
14. Van De Voorde L., Speeckaert R., Van Gestel D., Bracke M., De Neve W., Delanghe J., Speeckaert M. DNA methylation-based biomarkers in serum of patients with breast cancer. Mutat. Res. 2012, 751:304-325.
15. Toiyama Y., Okugawa Y., Goel A. DNA methylation and microRNA biomarkers for noninvasive detection of gastric and colorectal cancer. Biochem. Biophys. Res. Commun. 2014, 455:43-57.
16. Li M., Chen W.D., Papadopoulos N., Goodman S.N., Bjerregaard N.C., Laurberg S., Levin B., Juhl H., Arber N., Moinova H., Durkee K., Schmidt K., He Y., Diehl F., Velculescu V.E., Zhou S., Diaz L.A., Kinzler K.W., Markowitz S.D., Vogelstein B. Sensitive digital quantification of DNA methylation in clinical samples. Nat. Biotechnol. 2009, 27:858-863.
17. Ned R.M., Melillo S., Marrone M. Fecal DNA testing for Colorectal Cancer Screening: the ColoSure test. PLoS Curr. 2011, 3.
18. Imperiale T.F., Ransohoff D.F., Itzkowitz S.H., Levin T.R., Lavin P., Lidgard G.P., Ahlquist D.A., Berger B.M. Multitarget stool DNA testing for colorectal-cancer screening. N. Engl. J. Med. 2014, 370:1287-1297.
19. Hoque M.O., Begum S., Topaloglu O., Chatterjee A., Rosenbaum E., Van Criekinge W., Westra W.H., Schoenberg M., Zahurak M., Goodman S.N., Sidransky D. Quantitation of promoter methylation of multiple genes in urine DNA and bladder cancer detection. J. Natl. Cancer Inst. 2006, 98:996-1004.
20. Chan M.W., Chan L.W., Tang N.L., Tong J.H., Lo K.W., Lee T.L., Cheung H.Y., Wong W.S., Chan P.S., Lai F.M., To K.F. Hypermethylation of multiple genes in tumor tissues and voided urine in urinary bladder cancer patients. Clin. Cancer Res. 2002, 8:464-470.
21. Timp W., Feinberg A.P. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat. Rev. Cancer 2013, 13:497-510.
22. Cairns P., Esteller M., Herman J.G., Schoenberg M., Jeronimo C., Sanchez-Cespedes M., Chow N.H., Grasso M., Wu L., Westra W.B., Sidransky D. Molecular detection of prostate cancer in urine by GSTP1 hypermethylation. Clin. Cancer Res. 2001, 7:2727-2730.
23. Wu T., Giovannucci E., Welge J., Mallick P., Tang W.Y., Ho S.M. Measurement of GSTP1 promoter methylation in body fluids may complement PSA screening: a meta-analysis. Br. J. Cancer 2011, 105:65-73.
24. Brock M.V., Hooker C.M., Ota-Machida E., Han Y., Guo M., Ames S., Glockner S., Piantadosi S., Gabrielson E., Pridham G., Pelosky K., Belinsky S.A., Yang S.C., Baylin S.B., Herman J.G. DNA methylation markers and early recurrence in stage I lung cancer. N. Engl. J. Med. 2008, 358:1118-1128.
25. Toyota M., Ahuja N., Ohe-Toyota M., Herman J.G., Baylin S.B., Issa J.P. CpG island methylator phenotype in colorectal cancer. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:8681-8686.
26. Issa J.P. CpG island methylator phenotype in cancer. Nat. Rev. Cancer 2004, 4:988-993.
27. Grady W.M. CIMP and colon cancer gets more complicated. Gut 2007, 56:1498-1500.
28. Noushmehr H., Weisenberger D.J., Diefes K., Phillips H.S., Pujara K., Berman B.P., Pan F., Pelloski C.E., Sulman E.P., Bhat K.P., Verhaak R.G., Hoadley K.A., Hayes D.N., Perou C.M., Schmidt H.K., Ding L., Wilson R.K., Van Den Berg D., Shen H., Bengtsson H., Neuvial P., Cope L.M., Buckley J., Herman J.G., Baylin S.B., Laird P.W., Aldape K., Cancer Genome Atlas Research N. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010, 17:510-522.
29. Fang F., Turcan S., Rimner A., Kaufman A., Giri D., Morris L.G., Shen R., Seshan V., Mo Q., Heguy A., Baylin S.B., Ahuja N., Viale A., Massague J., Norton L., Vahdat L.T., Moynahan M.E., Chan T.A. Breast cancer methylomes establish an epigenomic foundation for metastasis. Sci. Transl. Med. 2011, 3:75ra25.
30. Shinjo K., Okamoto Y., An B., Yokoyama T., Takeuchi I., Fujii M., Osada H., Usami N., Hasegawa Y., Ito H., Hida T., Fujimoto N., Kishimoto T., Sekido Y., Kondo Y. Integrated analysis of genetic and epigenetic alterations reveals CpG island methylator phenotype associated with distinct clinical characters of lung adenocarcinoma. Carcinogenesis 2012, 33:1277-1285.
31. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., Agarwal S., Iyer L.M., Liu D.R., Aravind L., Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
32. Ito S., D'Alessio A.C., Taranova O.V., Hong K., Sowers L.C., Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010, 466:1129-1133.
33. Belinsky S.A. Gene-promoter hypermethylation as a biomarker in lung cancer. Nat. Rev. Cancer 2004, 4:707-717.
34. Schmidt B., Liebenberg V., Dietrich D., Schlegel T., Kneip C., Seegebarth A., Flemming N., Seemann S., Distler J., Lewin J., Tetzner R., Weickmann S., Wille U., Liloglou T., Raji O., Walshaw M., Fleischhacker M., Witt C., Field J.K. SHOX2 DNA methylation is a biomarker for the diagnosis of lung cancer based on bronchial aspirates. BMC Cancer 2010, 10:600.
35. Kneip C., Schmidt B., Seegebarth A., Weickmann S., Fleischhacker M., Liebenberg V., Field J.K., Dietrich D. SHOX2 DNA methylation is a biomarker for the diagnosis of lung cancer in plasma. J. Thorac. Oncol. 2011, 6:1632-1638.
36. Toyooka S., Pass H.I., Shivapurkar N., Fukuyama Y., Maruyama R., Toyooka K.O., Gilcrease M., Farinas A., Minna J.D., Gazdar A.F. Aberrant methylation and simian virus 40 tag sequences in malignant mesothelioma. Cancer Res. 2001, 61:5727-5730.
37. Herman J.G., Graff J.R., Myohanen S., Nelkin B.D., Baylin S.B. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:9821-9826.
38. Eads C.A., Danenberg K.D., Kawakami K., Saltz L.B., Blake C., Shibata D., Danenberg P.V., Laird P.W. MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res. 2000, 28.
39. Kristensen L.S., Mikeska T., Krypuy M., Dobrovic A. Sensitive Melting Analysis after Real Time- Methylation Specific PCR (SMART-MSP): high-throughput and probe-free quantitative DNA methylation detection. Nucleic Acids Res. 2008, 36:e42.
40. Mikeska T., Felsberg J., Hewitt C.A., Dobrovic A. Analysing DNA methylation using bisulphite pyrosequencing. Methods Mol. Biol. (Clifton, N. J.) 2011, 791:33-53.
41. Ehrich M., Nelson M.R., Stanssens P., Zabeau M., Liloglou T., Xinarianos G., Cantor C.R., Field J.K., van den Boom D. Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15785-15790.
42. Coolen M.W., Statham A.L., Gardiner-Garden M., Clark S.J. Genomic profiling of CpG methylation and allelic specificity using quantitative high-throughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Res. 2007, 35:e119.
43. Campan M., Moffitt M., Houshdaran S., Shen H., Widschwendter M., Daxenbichler G., Long T., Marth C., Laird-Offringa I.A., Press M.F., Dubeau L., Siegmund K.D., Wu A.H., Groshen S., Chandavarkar U., Roman L.D., Berchuck A., Pearce C.L., Laird P.W. Genome-scale screen for DNA methylation-based detection markers for ovarian cancer. PLoS One 2011, 6.
44. Dedeurwaerder S., Defrance M., Calonne E., Denis H., Sotiriou C., Fuks F. Evaluation of the Infinium Methylation 450K technology. Epigenomics 2011, 3:771-784.
45. Hansen K.D., Timp W., Bravo H.C., Sabunciyan S., Langmead B., McDonald O.G., Wen B., Wu H., Liu Y., Diep D., Briem E., Zhang K., Irizarry R.A., Feinberg A.P. Increased methylation variation in epigenetic domains across cancer types. Nat. Genet. 2011, 43:768-775.
46. Lee E.J., Luo J., Wilson J.M., Shi H. Analyzing the cancer methylome through targeted bisulfite sequencing. Cancer Lett. 2013, 340:171-178.
47. Laird P.W. Principles and challenges of genomewide DNA methylation analysis. Nat. Rev. Genet. 2010, 11:191-203.
48. Meissner A., Mikkelsen T.S., Gu H., Wernig M., Hanna J., Sivachenko A., Zhang X., Bernstein B.E., Nusbaum C., Jaffe D.B., Gnirke A., Jaenisch R., Lander E.S. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008, 454:766-770.
49. Gu H., Smith Z.D., Bock C., Boyle P., Gnirke A., Meissner A. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat. Protoc. 2011, 6:468-481.
50. Rauch T., Li H., Wu X., Pfeifer G.P. MIRA-assisted microarray analysis, a new technology for the determination of DNA methylation patterns, identifies frequent methylation of homeodomain-containing genes in lung cancer cells. Cancer Res. 2006, 66:7939-7947.
51. Jung M., Kadam S., Xiong W., Rauch T.A., Jin S.G., Pfeifer G.P. MIRA-seq for DNA methylation analysis of CpG islands. Epigenomics 2015, 1-12.
52. Ruike Y., Imanaka Y., Sato F., Shimizu K., Tsujimoto G. Genome-wide analysis of aberrant methylation in human breast cancer cells using methyl-DNA immunoprecipitation combined with high-throughput sequencing. BMC Genomics 2010, 11:137.
53. Thress K.S., Paweletz C.P., Felip E., Cho B.C., Stetson D., Dougherty B., Lai Z., Markovets A., Vivancos A., Kuang Y., Ercan D., Matthews S.E., Cantarini M., Barrett J.C., Janne P.A., Oxnard G.R. Acquired EGFR C797S mutation mediates resistance to AZD9291 in non-small cell lung cancer harboring EGFR T790M. Nat. Med. 2015, 21:560-562.
54. Vaca-Paniagua F., Oliver J., Nogueira da Costa A., Merle P., McKay J., Herceg Z., Holmila R. Targeted deep DNA methylation analysis of circulating cell-free DNA in plasma using massively parallel semiconductor sequencing. Epigenomics 2015, 7:353-362.
55. Branton D., Deamer D.W., Marziali A., Bayley H., Benner S.A., Butler T., Di Ventra M., Garaj S., Hibbs A., Huang X., Jovanovich S.B., Krstic P.S., Lindsay S., Ling X.S., Mastrangelo C.H., Meller A., Oliver J.S., Pershin Y.V., Ramsey J.M., Riehn R., Soni G.V., Tabard-Cossa V., Wanunu M., Wiggin M., Schloss J.A. The potential and challenges of nanopore sequencing. Nat. Biotechnol. 2008, 26:1146-1153.
56. Flusberg B.A., Webster D.R., Lee J.H., Travers K.J., Olivares E.C., Clark T.A., Korlach J., Turner S.W. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat. Methods 2010, 7:461-465.
57. Dawson M.A., Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell 2012, 150:12-27.
58. Knutson S.K., Kawano S., Minoshima Y., Warholic N.M., Huang K.C., Xiao Y., Kadowaki T., Uesugi M., Kuznetsov G., Kumar N., Wigle T.J., Klaus C.R., Allain C.J., Raimondi A., Waters N.J., Smith J.J., Porter-Scott M., Chesworth R., Moyer M.P., Copeland R.A., Richon V.M., Uenaka T., Pollock R.M., Kuntz K.W., Yokoi A., Keilhack H. Selective inhibition of EZH2 by EPZ-6438 leads to potent antitumor activity in EZH2-mutant non-Hodgkin lymphoma. Mol. Cancer Ther. 2014, 13:842-854.
59. IDH1 inhibitor shows promising early results. Cancer Discov. 2015, 5:4.
60. Issa J.P., Kantarjian H.M. Targeting DNA methylation. Clin. Cancer Res. 2009, 15:3938-3946.
61. Chen J., Odenike O., Rowley J.D. Leukaemogenesis: more than mutant genes. Nat. Rev. Cancer 2010, 10:23-36.
62. Dombret H., Seymour J.F., Butrym A., Wierzbowska A., Selleslag D., Jang J.H., Kumar R., Cavenagh J., Schuh A.C., Candoni A., Recher C., Sandhu I., Bernal Del Castillo T., Al-Ali H.K., Martinelli G., Falantes J., Noppeney R., Stone R.M., Minden M.D., McIntyre H., Songer S., Lucy L.M., Beach C.L., Dohner H. International phase 3 study of azacitidine vs conventional care regimens in older patients with newly diagnosed AML with >30% blasts. Blood 2015, 126:291-299.
63. Juergens R.A., Wrangle J., Vendetti F.P., Murphy S.C., Zhao M., Coleman B., Sebree R., Rodgers K., Hooker C.M., Franco N., Lee B., Tsai S., Delgado I.E., Rudek M.A., Belinsky S.A., Herman J.G., Baylin S.B., Brock M.V., Rudin C.M. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer. Cancer Discov. 2011, 1:598-607.
64. Paschka P., Schlenk R.F., Gaidzik V.I., Habdank M., Kronke J., Bullinger L., Spath D., Kayser S., Zucknick M., Gotze K., Horst H.A., Germing U., Dohner H., Dohner K. IDH1 and IDH2 mutations are frequent genetic alterations in acute myeloid leukemia and confer adverse prognosis in cytogenetically normal acute myeloid leukemia with NPM1 mutation without FLT3 internal tandem duplication. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2010, 28:3636-3643.
65. Yan H., Parsons D.W., Jin G., McLendon R., Rasheed B.A., Yuan W., Kos I., Batinic-Haberle I., Jones S., Riggins G.J., Friedman H., Friedman A., Reardon D., Herndon J., Kinzler K.W., Velculescu V.E., Vogelstein B., Bigner D.D. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 2009, 360:765-773.
66. Dang L., White D.W., Gross S., Bennett B.D., Bittinger M.A., Driggers E.M., Fantin V.R., Jang H.G., Jin S., Keenan M.C., Marks K.M., Prins R.M., Ward P.S., Yen K.E., Liau L.M., Rabinowitz J.D., Cantley L.C., Thompson C.B., Vander Heiden M.G., Su S.M. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2010, 465:966.
67. Wang F., Travins J., DeLaBarre B., Penard-Lacronique V., Schalm S., Hansen E., Straley K., Kernytsky A., Liu W., Gliser C., Yang H., Gross S., Artin E., Saada V., Mylonas E., Quivoron C., Popovici-Muller J., Saunders J.O., Salituro F.G., Yan S., Murray S., Wei W., Gao Y., Dang L., Dorsch M., Agresta S., Schenkein D.P., Biller S.A., Su S.M., de Botton S., Yen K.E. Targeted inhibition of mutant IDH2 in leukemia cells induces cellular differentiation. Science 2013, 340:622-626.
68. Arrowsmith C.H., Bountra C., Fish P.V., Lee K., Schapira M. Epigenetic protein families: a new frontier for drug discovery. Nat. Rev. Drug Discov. 2012, 11:384-400.
69. Federico M., Bagella L. Histone deacetylase inhibitors in the treatment of hematological malignancies and solid tumors. J. Biomed. Biotechnol. 2011, 2011:475641.
70. Olsen E.A., Kim Y.H., Kuzel T.M., Pacheco T.R., Foss F.M., Parker S., Frankel S.R., Chen C., Ricker J.L., Arduino J.M., Duvic M. Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2007, 25:3109-3115.
71. Piekarz R.L., Frye R., Turner M., Wright J.J., Allen S.L., Kirschbaum M.H., Zain J., Prince H.M., Leonard J.P., Geskin L.J., Reeder C., Joske D., Figg W.D., Gardner E.R., Steinberg S.M., Jaffe E.S., Stetler-Stevenson M., Lade S., Fojo A.T., Bates S.E. Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2009, 27:5410-5417.
72. O'Connor O.A., Horwitz S., Masszi T., Van Hoof A., Brown P., Doorduijn J., Hess G., Jurczak W., Knoblauch P., Chawla S., Bhat G., Choi M.R., Walewski J., Savage K., Foss F., Allen L.F., Shustov A. Belinostat in patients with relapsed or refractory peripheral T-cell lymphoma: results of the pivotal phase II BELIEF (CLN-19) study. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2015, 33:2492-2499.
73. Mottamal M., Zheng S., Huang T.L., Wang G. Histone deacetylase inhibitors in clinical studies as templates for new anticancer agents. Molecules (Basel, Switz.) 2015, 20:3898-3941.
74. Boyer L.A., Plath K., Zeitlinger J., Brambrink T., Medeiros L.A., Lee T.I., Levine S.S., Wernig M., Tajonar A., Ray M.K., Bell G.W., Otte A.P., Vidal M., Gifford D.K., Young R.A., Jaenisch R. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006, 441:349-353.
75. Lee T.I., Jenner R.G., Boyer L.A., Guenther M.G., Levine S.S., Kumar R.M., Chevalier B., Johnstone S.E., Cole M.F., Isono K., Koseki H., Fuchikami T., Abe K., Murray H.L., Zucker J.P., Yuan B., Bell G.W., Herbolsheimer E., Hannett N.M., Sun K., Odom D.T., Otte A.P., Volkert T.L., Bartel D.P., Melton D.A., Gifford D.K., Jaenisch R., Young R.A. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006, 125:301-313.
76. Margueron R., Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011, 469:343-349.
77. Varambally S., Dhanasekaran S.M., Zhou M., Barrette T.R., Kumar-Sinha C., Sanda M.G., Ghosh D., Pienta K.J., Sewalt R.G., Otte A.P., Rubin M.A., Chinnaiyan A.M. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002, 419:624-629.
78. Kleer C.G., Cao Q., Varambally S., Shen R., Ota I., Tomlins S.A., Ghosh D., Sewalt R.G., Otte A.P., Hayes D.F., Sabel M.S., Livant D., Weiss S.J., Rubin M.A., Chinnaiyan A.M. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:11606-11611.
79. Morin R.D., Johnson N.A., Severson T.M., Mungall A.J., An J., Goya R., Paul J.E., Boyle M., Woolcock B.W., Kuchenbauer F., Yap D., Humphries R.K., Griffith O.L., Shah S., Zhu H., Kimbara M., Shashkin P., Charlot J.F., Tcherpakov M., Corbett R., Tam A., Varhol R., Smailus D., Moksa M., Zhao Y., Delaney A., Qian H., Birol I., Schein J., Moore R., Holt R., Horsman D.E., Connors J.M., Jones S., Aparicio S., Hirst M., Gascoyne R.D., Marra M.A. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat. Genet. 2010, 42:181-185.
80. McCabe M.T., Graves A.P., Ganji G., Diaz E., Halsey W.S., Jiang Y., Smitheman K.N., Ott H.M., Pappalardi M.B., Allen K.E., Chen S.B., Della Pietra A., Dul E., Hughes A.M., Gilbert S.A., Thrall S.H., Tummino P.J., Kruger R.G., Brandt M., Schwartz B., Creasy C.L. Mutation of A677 in histone methyltransferase EZH2 in human B-cell lymphoma promotes hypertrimethylation of histone H3 on lysine 27 (H3K27). Proc. Natl. Acad. Sci. U. S. A. 2012, 109:2989-2994.
81. Ernst T., Chase A.J., Score J., Hidalgo-Curtis C.E., Bryant C., Jones A.V., Waghorn K., Zoi K., Ross F.M., Reiter A., Hochhaus A., Drexler H.G., Duncombe A., Cervantes F., Oscier D., Boultwood J., Grand F.H., Cross N.C. Inactivating mutations of the histone methyltransferase gene EZH2 in myeloid disorders. Nat. Genet. 2010, 42:722-726.
82. McCabe M.T., Ott H.M., Ganji G., Korenchuk S., Thompson C., Van Aller G.S., Liu Y., Graves A.P., Della Pietra A., Diaz E., LaFrance L.V., Mellinger M., Duquenne C., Tian X., Kruger R.G., McHugh C.F., Brandt M., Miller W.H., Dhanak D., Verma S.K., Tummino P.J., Creasy C.L. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 2012, 492:108-112.
83. Qi W., Chan H., Teng L., Li L., Chuai S., Zhang R., Zeng J., Li M., Fan H., Lin Y., Gu J., Ardayfio O., Zhang J.H., Yan X., Fang J., Mi Y., Zhang M., Zhou T., Feng G., Chen Z., Li G., Yang T., Zhao K., Liu X., Yu Z., Lu C.X., Atadja P., Li E. Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:21360-21365.
84. Konze K.D., Ma A., Li F., Barsyte-Lovejoy D., Parton T., Macnevin C.J., Liu F., Gao C., Huang X.P., Kuznetsova E., Rougie M., Jiang A., Pattenden S.G., Norris J.L., James L.I., Roth B.L., Brown P.J., Frye S.V., Arrowsmith C.H., Hahn K.M., Wang G.G., Vedadi M., Jin J. An orally bioavailable chemical probe of the lysine methyltransferases EZH2 and EZH1. ACS Chem. Biol. 2013, 8:1324-1334.
85. Kim W., Bird G.H., Neff T., Guo G., Kerenyi M.A., Walensky L.D., Orkin S.H. Targeted disruption of the EZH2-EED complex inhibits EZH2-dependent cancer. Nat. Chem. Biol. 2013, 9:643-650.
86. Meyer C., Hofmann J., Burmeister T., Groger D., Park T.S., Emerenciano M., Pombo de Oliveira M., Renneville A., Villarese P., Macintyre E., Cave H., Clappier E., Mass-Malo K., Zuna J., Trka J., De Braekeleer E., De Braekeleer M., Oh S.H., Tsaur G., Fechina L., van der Velden V.H., van Dongen J.J., Delabesse E., Binato R., Silva M.L., Kustanovich A., Aleinikova O., Harris M.H., Lund-Aho T., Juvonen V., Heidenreich O., Vormoor J., Choi W.W., Jarosova M., Kolenova A., Bueno C., Menendez P., Wehner S., Eckert C., Talmant P., Tondeur S., Lippert E., Launay E., Henry C., Ballerini P., Lapillone H., Callanan M.B., Cayuela J.M., Herbaux C., Cazzaniga G., Kakadiya P.M., Bohlander S., Ahlmann M., Choi J.R., Gameiro P., Lee D.S., Krauter J., Cornillet-Lefebvre P., Te Kronnie G., Schafer B.W., Kubetzko S., Alonso C.N., zur Stadt U., Sutton R., Venn N.C., Izraeli S., Trakhtenbrot L., Madsen H.O., Archer P., Hancock J., Cerveira N., Teixeira M.R., Lo Nigro L., Moricke A., Stanulla M., Schrappe M., Sedek L., Szczepanski T., Zwaan C.M., Coenen E.A., van den Heuvel-Eibrink M.M., Strehl S., Dworzak M., Panzer-Grumayer R., Dingermann T., Klingebiel T., Marschalek R. The MLL recombinome of acute leukemias in 2013. Leukemia 2013, 27:2165-2176.
87. De Braekeleer M., Morel F., Le Bris M.J., Herry A., Douet-Guilbert N. The MLL gene and translocations involving chromosomal band 11q23 in acute leukemia. Anticancer Res. 2005, 25:1931-1944.
88. Okada Y., Feng Q., Lin Y., Jiang Q., Li Y., Coffield V.M., Su L., Xu G., Zhang Y. hDOT1L links histone methylation to leukemogenesis. Cell 2005, 121:167-178.
89. Daigle S.R., Olhava E.J., Therkelsen C.A., Basavapathruni A., Jin L., Boriack-Sjodin P.A., Allain C.J., Klaus C.R., Raimondi A., Scott M.P., Waters N.J., Chesworth R., Moyer M.P., Copeland R.A., Richon V.M., Pollock R.M. Potent inhibition of DOT1L as treatment of MLL-fusion leukemia. Blood 2013, 122:1017-1025.
90. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., Casero R.A., Shi Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
91. Metzger E., Wissmann M., Yin N., Muller J.M., Schneider R., Peters A.H., Gunther T., Buettner R., Schule R. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005, 437:436-439.
92. Hayami S., Kelly J.D., Cho H.S., Yoshimatsu M., Unoki M., Tsunoda T., Field H.I., Neal D.E., Yamaue H., Ponder B.A., Nakamura Y., Hamamoto R. Overexpression of LSD1 contributes to human carcinogenesis through chromatin regulation in various cancers. Int. J. Cancer J. Int. Cancer 2011, 128:574-586.
93. Harris W.J., Huang X., Lynch J.T., Spencer G.J., Hitchin J.R., Li Y., Ciceri F., Blaser J.G., Greystoke B.F., Jordan A.M., Miller C.J., Ogilvie D.J., Somervaille T.C. The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells. Cancer Cell 2012, 21:473-487.
94. Mohammad H., van Aller K.S.G., Cusan M., Kamat S., Liu Y., Johnson N., Hann C., Armstrong S., Kruger R. Novel anti-tumor activity of targeted LSD1 inhibition by GSK2879552. European Journal of Cancer 26th EORTC - NCI - AACR Symposium on Molecular Targets and Cancer Therapeutics 2014, 50:72.
95. Song M.S., Matveychuk D., MacKenzie E.M., Duchcherer M., Mousseau D.D., Baker G.B. An update on amine oxidase inhibitors: multifaceted drugs. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2013, 44:118-124.
96. Hill J.M., Quenelle D.C., Cardin R.D., Vogel J.L., Clement C., Bravo F.J., Foster T.P., Bosch-Marce M., Raja P., Lee J.S., Bernstein D.I., Krause P.R., Knipe D.M., Kristie T.M. Inhibition of LSD1 reduces herpesvirus infection, shedding, and recurrence by promoting epigenetic suppression of viral genomes. Sci. Transl. Med. 2014, 6:265ra169.
97. French C.A., Miyoshi I., Kubonishi I., Grier H.E., Perez-Atayde A.R., Fletcher J.A. BRD4-NUT fusion oncogene: a novel mechanism in aggressive carcinoma. Cancer Res. 2003, 63:304-307.
98. Filippakopoulos P., Qi J., Picaud S., Shen Y., Smith W.B., Fedorov O., Morse E.M., Keates T., Hickman T.T., Felletar I., Philpott M., Munro S., McKeown M.R., Wang Y., Christie A.L., West N., Cameron M.J., Schwartz B., Heightman T.D., La Thangue N., French C.A., Wiest O., Kung A.L., Knapp S., Bradner J.E. Selective inhibition of BET bromodomains. Nature 2010, 468:1067-1073.
99. Nicodeme E., Jeffrey K.L., Schaefer U., Beinke S., Dewell S., Chung C.W., Chandwani R., Marazzi I., Wilson P., Coste H., White J., Kirilovsky J., Rice C.M., Lora J.M., Prinjha R.K., Lee K., Tarakhovsky A. Suppression of inflammation by a synthetic histone mimic. Nature 2010, 468:1119-1123.
100. Dawson M.A., Prinjha R.K., Dittmann A., Giotopoulos G., Bantscheff M., Chan W.I., Robson S.C., Chung C.W., Hopf C., Savitski M.M., Huthmacher C., Gudgin E., Lugo D., Beinke S., Chapman T.D., Roberts E.J., Soden P.E., Auger K.R., Mirguet O., Doehner K., Delwel R., Burnett A.K., Jeffrey P., Drewes G., Lee K., Huntly B.J., Kouzarides T. Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 2011, 478:529-533.
101. Delmore J.E., Issa G.C., Lemieux M.E., Rahl P.B., Shi J., Jacobs H.M., Kastritis E., Gilpatrick T., Paranal R.M., Qi J., Chesi M., Schinzel A.C., McKeown M.R., Heffernan T.P., Vakoc C.R., Bergsagel P.L., Ghobrial I.M., Richardson P.G., Young R.A., Hahn W.C., Anderson K.C., Kung A.L., Bradner J.E., Mitsiades C.S. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 2011, 146:904-917.
102. Puissant A., Frumm S.M., Alexe G., Bassil C.F., Qi J., Chanthery Y.H., Nekritz E.A., Zeid R., Gustafson W.C., Greninger P., Garnett M.J., McDermott U., Benes C.H., Kung A.L., Weiss W.A., Bradner J.E., Stegmaier K. Targeting MYCN in neuroblastoma by BET bromodomain inhibition. Cancer Discov. 2013, 3:308-323.
103. Romanoski C.E., Glass C.K., Stunnenberg H.G., Wilson L., Almouzni G. Epigenomics: roadmap for regulation. Nature 2015, 518:314-316.
104. Kisiel J.B., Yab T.C., Taylor W.R., Chari S.T., Petersen G.M., Mahoney D.W., Ahlquist D.A. Stool DNA testing for the detection of pancreatic cancer: assessment of methylation marker candidates. Cancer 2012, 118:2623-2631.