Epimutations mimic genomic mutations of DNMT3A in acute myeloid leukemia

Leukemia

Volumn 28, Issue 6, 2014, Pages 1227-1234

  Jost, E ^a   Lin, Q ^a   Weidner, C I ^b   Wilop, S ^a   Hoffmann, M ^a   Walenda, T ^b   Schemionek, M ^a   Herrmann, O ^a   Zenke, M ^a   Brummendorf T H ^a   Koschmieder, S ^a   Wagner, W ^b  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

acute myeloid leukemia; de novo methyltransferase DNMT3A; DNA methylation; epigenomics; epimutation; mutation

Indexed keywords

BISULFITE; DNA METHYLTRANSFERASE 3A; GENOMIC DNA; RNA;

ACUTE GRANULOCYTIC LEUKEMIA; ALLELE; ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CANCER RISK; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIMUTATION; EVENT FREE SURVIVAL; EXON; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; LEUKEMIA CELL; MAJOR CLINICAL STUDY; MUTATIONAL ANALYSIS; OVERALL SURVIVAL; PRIORITY JOURNAL; PROMOTER REGION; PYROSEQUENCING; RNA SEQUENCE; UPREGULATION; BLOOD; COMPUTER PROGRAM; CYTOGENETICS; DNA MICROARRAY; EPIGENETICS; GENETIC RISK; HOMEOBOX; HUMAN CELL; REAL TIME POLYMERASE CHAIN REACTION; SPECTROPHOTOMETER;

DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENOMICS; HUMANS; LEUKEMIA, MYELOID, ACUTE; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL;

EID: 84902082994     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2013.362     Document Type: Article

References (47)

1. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999; 99: 247-257. (Pubitemid 29519904)
2. Gopalakrishnan S, Van Emburgh BO, Shan J, Su Z, Fields CR, Vieweg J et al. A novel DNMT3B splice variant expressed in tumor and pluripotent cells modulates genomic DNA methylation patterns and displays altered DNA binding. Mol Cancer Res 2009; 7: 1622-1634.
3. Neri F, Krepelova A, Incarnato D, Maldotti M, Parlato C, Galvagni F et al. Dnmt3L antagonizes DNA methylation at bivalent promoters and favors DNA methylation at gene bodies in ESCs. Cell 2013; 155: 121-134.
4. Van Emburgh BO, Robertson KD. Modulation of Dnmt3b function in vitro by interactions with Dnmt3L, Dnmt3a and Dnmt3b splice variants. Nucleic Acids Res 2011; 39: 4984-5002.
5. Robertson KD, Uzvolgyi E, Liang G, Talmadge C, Sumegi J, Gonzales FA et al. The human DNA methyltransferases (DNMTs) 1, 3a and 3b: Coordinate mRNA expression in normal tissues and overexpression in tumors. Nucleic Acids Res 1999; 27: 2291-2298.
6. Weisenberger DJ, Velicescu M, Preciado-Lopez MA, Gonzales FA, Tsai YC, Liang G et al. Identification and characterization of alternatively spliced variants of DNA methyltransferase 3a in mammalian cells. Gene 2002; 298: 91-99. (Pubitemid 35284266)
7. Challen GA, Sun D, Jeong M, Luo M, Jelinek J, Berg JS et al. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet 2012; 44: 23-31.
8. Ley TJ, Ding L, Walter MJ, McLellan MD, Lamprecht T, Larson DE et al. DNMT3A mutations in acute myeloid leukemia. N Engl J Med 2010; 363: 2424-2433.
9. Ley TJ, Miller C, Ding L, Raphael BJ, Mungall AJ, Robertson AG et al. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med 2013; 368: 2059-2074.
10. Walter MJ, Ding L, Shen D, Shao J, Grillot M, McLellan M et al. Recurrent DNMT3A mutations in patients with myelodysplastic syndromes. Leukemia 2011; 25: 1153-1158.
11. Yan XJ, Xu J, Gu ZH, Pan CM, Lu G, Shen Y et al. Exome sequencing identifies somatic mutations of DNA methyltransferase gene DNMT3A in acute monocytic leukemia. Nat Genet 2011; 43: 309-315.
12. Ribeiro AF, Pratcorona M, Erpelinck-Verschueren C, Rockova V, Sanders M, Abbas S et al. Mutant DNMT3A: A marker of poor prognosis in acute myeloid leukemia. Blood 2012; 119: 5824-5831.
13. Fenaux P, Mufti GJ, Hellstrom-Lindberg E, Santini V, Finelli C, Giagounidis A et al. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: A randomised, open-label, phase III study. Lancet Oncol 2009; 10: 223-232.
14. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M et al. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 2011; 479: 74-79.
15. Dolnik A, Engelmann JC, Scharfenberger-Schmeer M, Mauch J, Kelkenberg-Schade S, Haldemann B et al. Commonly altered genomic regions in acute myeloid leukemia are enriched for somatic mutations involved in chromatin remodeling and splicing. Blood 2012; 120: E83-e92.
16. Bibikova M, Barnes B, Tsan C, Ho V, Klotzle B, Le JM et al. High density DNA methylation array with single CpG site resolution. Genomics 2011; 98: 288-295.
17. Renneville A, Boissel N, Nibourel O, Berthon C, Helevaut N, Gardin C et al. Prognostic significance of DNA methyltransferase 3A mutations in cytogenetically normal acute myeloid leukemia: A study by the Acute Leukemia French Association. Leukemia 2012; 26: 1247-1254.
18. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlen SE, Greco D et al. Differential DNA methylation in purified human blood cells: Implications for cell lineage and studies on disease susceptibility. PLoS One 2012; 7: E41361.
19. Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S et al. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell 2013; 49: 459-367.
20. Sandoval J, Heyn HA, Moran S, Serra-Musach J, Pujana MA, Bibikova M et al. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics 2011; 6: 692-702.
21. Weidner CI, Walenda T, Lin Q, Wölfler MM, Denecke B, Costa IG et al. Hematopoietic stem and progenitor cells acquire distinct DNA-hypermethylation during in vitro culture. Sci Rep 2013; 3: 3372.
22. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 2011; 474: 609-615.
23. Cancer Genome Atlas Research Network. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012; 489: 519-525.
24. Shen H, Laird PW. Interplay between the cancer genome and epigenome. Cell 2013; 153: 38-55.
25. Jourdan E, Boissel N, Chevret S, Delabesse E, Renneville A, Cornillet P et al. Prospective evaluation of gene mutations and minimal residual disease in patients with core binding factor acute myeloid leukemia. Blood 2013; 121: 2213-2223.
26. Mullighan CG, Kennedy A, Zhou X, Radtke I, Phillips LA, Shurtleff SA et al. Pediatric acute myeloid leukemia with NPM1 mutations is characterized by a gene expression profile with dysregulated HOX gene expression distinct from MLL-rearranged leukemias. Leukemia 2007; 21: 2000-2009. (Pubitemid 47299976)
27. Verhaak RG, Goudswaard CS, van PW, Bijl MA, Sanders MA, Hugens W et al. Mutations in nucleophosmin (NPM1) in acute myeloid leukemia (AML): Association with other gene abnormalities and previously established gene expression signatures and their favorable prognostic significance. Blood 2005; 106: 3747-3754. (Pubitemid 41739008)
28. Alcalay M, Tiacci E, Bergomas R, Bigerna B, Venturini E, Minardi SP et al. Acute myeloid leukemia bearing cytoplasmic nucleophosmin (NPMc+ AML) shows a distinct gene expression profile characterized by up-regulation of genes involved in stem-cell maintenance. Blood 2005; 106: 899-902. (Pubitemid 41076430)
29. Takeda A, Goolsby C, Yaseen NR. NUP98-HOXA9 induces long-Term proliferation and blocks differentiation of primary human CD34+ hematopoietic cells. Cancer Res 2006; 66: 6628-6637. (Pubitemid 44085619)
30. Hayette S, Thomas X, Jallades L, Chabane K, Charlot C, Tigaud I et al. High DNA methyltransferase DNMT3B levels: A poor prognostic marker in acute myeloid leukemia. PLoS One 2012; 7: E51527.
31. Marcucci G, Metzeler KH, Schwind S, Becker H, Maharry K, Mrozek K et al. Age-related prognostic impact of different types of DNMT3A mutations in adults with primary cytogenetically normal acute myeloid leukemia. J Clin Oncol 2012; 30: 742-750.
32. Holliday R. The inheritance of epigenetic defects. Science 1987; 238: 163-170. (Pubitemid 17139717)
33. Jeggo PA, Holliday R. Azacytidine-induced reactivation of a DNA repair gene in Chinese hamster ovary cells. Mol Cell Biol 1986; 6: 2944-2949. (Pubitemid 17190838)
34. Banno K, Kisu I, Yanokura M, Tsuji K, Masuda K, Ueki A et al. Epimutation and cancer: A new carcinogenic mechanism of Lynch syndrome (Review). Int J Oncol 2012; 41: 793-797.
35. Greger V, Passarge E, Hopping W, Messmer E, Horsthemke B. Epigenetic changes may contribute to the formation and spontaneous regression of retinoblastoma. Hum Genet 1989; 83: 155-158.
36. Herman JG, Latif F, Weng Y, Lerman MI, Zbar B, Liu S et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci USA 1994; 91: 9700-9704. (Pubitemid 24311875)
37. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, Goldman H et al. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res 1997; 57: 808-811. (Pubitemid 27097998)
38. Dobrovic A, Simpfendorfer D. Methylation of the BRCA1 gene in sporadic breast cancer. Cancer Res 1997; 57: 3347-3350. (Pubitemid 27355472)
39. Hansmann T, Pliushch G, Leubner M, Kroll P, Endt D, Gehrig A et al. Constitutive promoter methylation of BRCA1 and RAD51C in patients with familial ovarian cancer and early-onset sporadic breast cancer. Hum Mol Genet 2012; 21: 4669-4679.
40. Yamashita Y, Yuan J, Suetake I, Suzuki H, Ishikawa Y, Choi YL et al. Array-based genomic resequencing of human leukemia. Oncogene 2010; 29: 3723-3731.
41. Eklund EA. The role of HOX genes in malignant myeloid disease. Curr Opin Hematol 2007; 14: 85-89. (Pubitemid 46175091)
42. Shah N, Sukumar S. The Hox genes and their roles in oncogenesis. Nat Rev Cancer 2010; 10: 361-371.
43. Schiedlmeier B, Santos AC, Ribeiro A, Moncaut N, Lesinski D, Auer H et al. HOXB4's road map to stem cell expansion. Proc Natl Acad Sci USA 2007; 104: 16952-16957. (Pubitemid 350210971)
44. Wakita S, Yamaguchi H, Omori I, Terada K, Ueda T, Manabe E et al. Mutations of the epigenetics-modifying gene (DNMT3a, TET2, IDH1/2) at diagnosis may induce FLT3-ITD at relapse in de novo acute myeloid leukemia. Leukemia 2013; 27: 1044-1052.
45. Schoofs T, Rohde C, Hebestreit K, Klein HU, Gollner S, Schulze I et al. DNA methylation changes are a late event in acute promyelocytic leukemia and coincide with loss of transcription factor binding. Blood 2013; 121: 178-187.
46. Champion C, Guianvarc'h D, Senamaud-Beaufort C, Jurkowska RZ, Jeltsch A, Ponger L et al. Mechanistic insights on the inhibition of c5 DNA methyltransferases by zebularine. PLoS One 2010; 5: E12388.
47. Patel JP, Gonen M, Figueroa ME, Fernandez H, Sun Z, Racevskis J et al. Prognostic relevance of integrated genetic profiling in acute myeloid leukemia. N Engl J Med 2012; 366: 1079-1089.