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Review

Poor prognosis in acute lymphoblastic leukemia may relate to promoter hypermethylation of cancer-related genes

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Pages 1269-1282 | Received 22 Jan 2007, Accepted 16 Mar 2007, Published online: 01 Jul 2009

References

  • Laird P W. The power and the promise of DNA methylation markers. Nat Rev Cancer 2003; 3: 253–266
  • Clark S J, Harrison J, Paul C L, Frommer M. High sensitivity mapping of methylated cytosines. Nucleic Acids Res 1994; 22: 2990–2997
  • 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 USA 1996; 93: 9821–9826
  • Ahuja N, Issa J P. Aging, methylation and cancer. Histol Histopathol 2000; 15: 835–842
  • Cravo M L, Pinto A G, Chaves P, Cruz J A, Lage P, Nobre L C, et al. Effect of folate supplementation on DNA methylation of rectal mucosa in patients with colonic adenomas: correlation with nutrient intake. Clin Nutr 1998; 17: 45–49
  • James S J, Pogribny I P, Pogribna M, Miller B J, Jernigan S, Melnyk S. Mechanisms of DNA damage, DNA hypomethylation, and tumor progression in the folate/methyl-deficient rat model of hepatocarcinogenesis. J Nutr 2003; 133: 3740S–3747S
  • Pufulete M, Emery P W, Sanders T A. Folate, DNA methylation and colo-rectal cancer. Proc Nutr Soc 2003; 62: 437–445
  • Fang J Y, Xiao S D. Folic acid, polymorphism of methyl-group metabolism genes, and DNA methylation in relation to GI carcinogenesis. J Gastroenterol 2003; 38: 821–829
  • Matsuo K, Hamajima N, Suzuki R, Ogura M, Kagami Y, Taji H, et al. Methylenetetrahydrofolate reductase gene (MTHFR) polymorphisms and reduced risk of malignant lymphoma. Am J Hematol 2004; 77: 351–357
  • Esteller M. CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene 2002; 21: 5427–5440
  • Pui C-H, Evans W E. Acute lymphoblastic leukemia. N Engl J Med 1998; 339: 605–615
  • Pui C-H, Behm F G, Crist W M. Clinical and biologic relevance of immunologic marker studies in childhood acute lymphoblastic leukemia. Blood 1993; 82: 343–362
  • Ponder B AJ. Cancer genetics. Nature 2001; 411: 336–341
  • Pui C -H, Crist W M, Look A T. Biology and clinical significance of cytogenetic abnormalities in childhood acute lymphoblastic leukemia. Blood 1990; 76: 1449–1463
  • Faderl S, Kantarjian H M, Talpaz M, Estrov Z. Clinical significance of cytogenetic abnormalities in adult acute lymphoblastic leukemia. Blood 1998; 91: 3995–4019
  • Wada M, Bartram C R, Nakamura H, Hachiya M, Chen D L, Borenstein J, et al. Analysis of p53 mutations in a large series of lymphoid hematologic malignancies of childhood. Blood 1993; 82: 3163–3169
  • Jones P A, Laird P W. Cancer epigenetics comes of age. Nature Genet 1999; 21: 163–167
  • Wolffe A P, Matzke M A. Epigenetics: regulation through repression. Science 1999; 286: 481–486
  • Tycko B. Epigenetic gene silencing in cancer. J Clin Invest 2000; 105: 401–407
  • Herman J G, Baylin S B. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003; 349: 2042–2054
  • Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33: 245–254
  • Feinberg A P, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004; 4: 143–153
  • Singal R, Ginder G D. DNA methylation. Blood 1999; 93: 4059–4070
  • Struhl K. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev 1998; 12: 599–606
  • Nan X, Ng H H, Johnson C A, Laherty C D, Turner B M, Eisenman R N, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998; 393: 386–389
  • Jones P L, Veenstra G J, Wade P A, Vermaak D, Kass K U, Landsberger N, et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 1998; 19: 187–191
  • Mannervik M, Nibu Y, Zhang H, Levine M. Transcriptional coregulators in development. Science 1999; 284: 606–609
  • Hendrich B, Bird A. Mammalian methyltransferases and methyl-CpG binding domains: proteins involved in DNA methylation. Curr Top Microbiol Immunol 2000; 249: 55–74
  • Rountree M R, Bachman K E, Herman J G, Baylin S B. DNA methylation, chromatin inheritance, and cancer. Oncogene 2001; 20: 3156–3165
  • Im H, Grass J A, Christensen H M, Perkins A, Bresnick E H. Histone deacetylase-dependent establishment and maintenance of broad low-level histone acetylation within a tissue-specific chromatin domain. Biochemistry 2002; 41: 15152–15160
  • El Osta A. DNMT cooperativity – the developing links between methylation, chromatin structure and cancer. Bioessays 2003; 25: 1071–1084
  • Pietenpol J A, Bohlander S K, Sato Y, Papadopoulus N, Liu B, Friedman C, et al. Assignment of the human p27kip1 gene to 12p13 and its analysis in leukemias. Cancer Res 1995; 55: 1206–1210
  • Hsieh C L. Dependence of transcriptional repression on CpG methylation density. Mol Cell Biol 1994; 14: 5487–5494
  • Vertino P M, Yen R W, Grao J, Baylin S B. De novo methylation of CpG island sequences in human fibroblasts overexpressing DNA (cytosine-5)-methyltransferase. Mol Cell Biol 1996; 16: 4555–4565
  • Graff J R, Herman J G, Myohanen S, Baylin S B, Vertino P M. Mapping patterns of CpG island methylation in normal and neoplastic cells implicates both upstream and downstream regions in de novo methylation. J Biol Chem 1997; 272: 22322–22329
  • Myohanen S K, Baylin S B, Herman J G. Hypermethylation can selectively silence individual p16ink4a alleles in neoplasia. Cancer Res 1998; 58: 591–593
  • Esteller M, Corn P G, Baylin S B, Herman J G. A gene hypermethylation profile of human cancer. Cancer Res 2001; 61: 3225–3229
  • Costello J F, Fruhwald M C, Smiraglia D J, Rush L J, Robertson G P, Gao X, et al. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet 2000; 24: 132–138
  • Sakashita K, Koike K, Kinoshita T, Shiohara M, Kamijo T, Taniguchi S, et al. Dynamic DNA methylation change in the CpG island region of p15 during human myeloid development. J Clin Invest 2001; 108: 1195–1204
  • Roman-Gomez J, Castillejo J A, Jimenez A, Gonzalez M G, Moreno F, Rodriguez M C, et al. 5′ CpG island hypermethylation is associated with transcriptional silencing of the p21CIP1/WAF1/SDI1gene and confers poor prognosis in acute lymphoblastic leukemia. Blood 2002; 99: 2291–2296
  • Agirre X, Vizmanos J L, Calazans M J, Garcia-Delgado M, Larrayoz M J, Novo F J. Methylation of CpG dinucleotides and/or CCWGG motifs at the promoter of TP53 correlates with decreased gene expression in a subset of acute lymphoblastic leukemia patients. Oncogene 2003; 22: 1070–1072
  • Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo J A, Barrios M, Andreu E J, et al. The normal epithelial cell-specific 1 (NES1) gene, a candidate tumor suppressor gene on chromosome 19q13.3 – 4, is downregulated by hypermethylation in acute lymphoblastic leukemia. Leukemia 2004; 18: 362–365
  • Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo J A, Navarro G, Barrios M, et al. Transcriptional silencing of the Dickkopfs-3 (Dkk-3) gene by CpG hypermethylation in acute lymphoblastic leukaemia. Br J Cancer 2004; 91: 707–713
  • Jimenez-Velasco A, Roman-Gomez J, Agirre X, Barrios M, Navarro G, Vazquez I, et al. Downregulation of the large tumor suppressor 2 (LATS2 / KPM) gene confers poor prognosis in acute lymphoblastic leukemia. Leukemia 2005; 19: 2347–2350
  • Agirre X, Roman-Gomez J, Vazquez I, Jimenez-Velasco A, Garate L, Montiel-Duarte C, et al. Abnormal methylation of the common PARK2 and PACRG promoter is associated with downregulation of gene expression in Acute Lymphoblastic Leukemia (ALL) and Chronic Myeloid Leukemia (CML). Int J Cancer 2006; 118: 1945–1953
  • Agirre X, Roman-Gomez J, Jimenez-Velasco A, Garate L, Montiel-Duarte C, Navarro G, et al. ASPP1, a common activator of TP53, is inactivated by aberrant methylation of its promoter in acute lymphoblastic leukemia. Oncogene 2006; 25: 1862–1870
  • San Jose-Eneriz E, Agirre X, Roman-Gomez J, Cordeu L, Garate L, Jimenez-Velasco A, et al. Downregulation of DBC1 expression in acute lymphoblastic leukaemia is mediated by aberrant methylation of its promoter. Br J Haematol 2006; 134: 137–144
  • Shen L, Toyota M, Kondo Y, Obata T, Daniel S, Pierce S, et al. Aberrant DNA methylation of p57KIP2 identifies a cell-cycle regulatory pathway with prognostic impact in adult acute lymphocytic leukemia. Blood 2003; 101: 4131–4136
  • Roman-Gomez J, Jimenez-Velasco A, Castillejo J A, Agirre X, Barrios M, Navarro G, et al. Promoter hypermethylation of cancer-related genes: a strong independent prognostic factor in acute lymphoblastic leukemia. Blood 2004; 104: 2492–2498
  • Roman-Gomez J, Jimenez-Velasco A, Agirre X, Prosper F, Heiniger A, Torres A. Lack of CpG island methylator phenotype defines a clinical subtype of T-cell acute lymphoblastic leukemia associated with good prognosis. J Clin Oncol 2005; 23: 7043–7049
  • Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo J A, Navarro G, Calasanz M J, et al. CpG island methylator phenotype redefines the prognostic effect of t(12;21) in childhood acute lymphoblastic leukemia. Clin Cancer Res 2006; 12: 4845–4850
  • Roman-Gomez J, Cordeu L, Agirre X, Jimenez-Velasco A, San Jose-Eneriz E, Garate L, et al. Epigenetic regulation of WNT signaling pathway in acute lymphoblastic leukemia. Blood 2007; 109: 3462–3469
  • Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo J A, Navarro G, Garate L, et al. Promoter hypermethylation and global hypomethylation are independent epigenetic events in lymphoid leukemogenesis with opposing effects on clinical outcome. Leukemia 2006; 20: 1445–1448
  • Roman-Gomez J, Castillejo J A, Jimenez A, Gonzalez M G, Reina M L, Rodriguez M C, et al. Hypermethylation of the calcitonin gene in acute lymphoblastic leukemia is associated with unfavourable clinical outcome. Br J Haematol 2001; 113: 329–338
  • Garcia-Manero G, Daniel I, Smith T L, Kornblau S M, Kantarjian H M, Issa J-P. DNA methylation of multiple promoter-associated CpG islands in adult acute lymphocytic leukemia. Clin Cancer Res 2002; 8: 2217–2224
  • Gutierrez M I, Siraj A K, Bhargava M, Ozbek U, Banavali S, Chaudhary M A, et al. Concurrent methylation of multiple genes in childhood ALL: correlation with phenotype and molecular subgroup. Leukemia 2003; 17: 1845–1850
  • Takahashi T, Shivapurkar N, Reddy J, Shigematsu H, Miyajima K, Suzuki M, et al. DNA methylation profiles of lymphoid and hematopoietic malignancies. Clin Cancer Res 2004; 10: 2928–2935
  • Garcia-Manero G, Bueso-Ramos C, Daniel J, Williamson J, Kantarjian H M, Issa J P. DNA methylation patterns at relapse in adult acute lymphocytic leukemia. Clin Cancer Res 2002; 8: 1897–1903
  • Matsushita C, Yang Y, Takeuchi S, Matsushita M, van Dongen J J, Szczepanski T, et al. Aberrant methylation in promoter-associated CpG islands of multiple genes in relapsed childhood acute lymphoblastic leukemia. Oncol Rep 2004; 12: 97–99
  • Uehara E, Takeuchi S, Tasaka T, Matsuhashi Y, Yang Y, Fujita M, et al. Aberrant methylation in promoter-associated CpG islands of multiple genes in therapy-related leukemia. Int J Oncol 2003; 23: 693–696
  • Ren Y, Roy S, Ding Y, Iqbal J, Broome J D. Methylation of the asparagine synthetase promoter in human leukemic cell lines is associated with a specific methyl binding protein. Oncogene 2004; 23: 3953–3961
  • Roman-Gomez J, Castillejo J A, Jimenez A, Barrios M, Heiniger A, Torres A. The role of DNA hypermethylation in the pathogenesis and prognosis of acute lymphoblastic leukemia. Leuk Lymphoma 2003; 44: 1855–1864
  • Scholz C, Nimmrich I, Burger M, Becker E, Dorken B, Ludwig W D, et al. Distinction of acute lymphoblastic leukemia from acute myeloid leukemia through microarray-based DNA methylation analysis. Ann Hematol 2005; 84: 236–244
  • Gemmati D, Ongaro A, Scapoli G L, Della P M, Tognazzo S, Serino M L, et al. Common gene polymorphisms in the metabolic folate and methylation pathway and the risk of acute lymphoblastic leukemia and non-Hodgkin's lymphoma in adults. Cancer Epidemiol Biomarkers Prev 2004; 13: 787–794
  • Moore L E, Huang W Y, Chung J, Hayes R B. Epidemiologic considerations to assess altered DNA methylation from environmental exposures in cancer. Ann N Y Acad Sci 2003; 983: 181–196
  • Shivapurkar N, Takahashi T, Reddy J, Zheng Y, Stastny V, Collins R, et al. Presence of simian virus 40 DNA sequences in human lymphoid and hematopoietic malignancies and their relationship to aberrant promoter methylation of multiple genes. Cancer Res 2004; 64: 3757–3760
  • Oka T, Ouchida M, Koyama M, Ogama Y, Takada S, Nakatani Y, et al. Gene silencing of the tyrosine phosphatase SHP1 gene by aberrant methylation in leukemias/lymphomas. Cancer Res 2002; 62: 6390–6394
  • Goodman P A, Burkhardt N, Juran B, Tibbles H E, Uckun F M. Hypermethylation of the spleen tyrosine kinase promoter in T-lineage acute lymphoblastic leukemia. Oncogene 2003; 22: 2504–2514
  • Ponder B AJ. Cancer genetics. Nature 2001; 411: 336–341
  • Wada M, Bartram C R, Nakamura H, Hachiya M, Chen D L, Borenstein J, et al. Analysis of p53 mutations in a large series of lymphoid hematologic malignancies of childhood. Blood 1993; 82: 3163–3169
  • Plasschaert S L, Kamps W A, Vellenga E, de Vries E G, de Bont E S. Prognosis in childhood and adult acute lymphoblastic leukaemia: a question of maturation?. Cancer Treat Rev 2004; 30: 37–51
  • Yasunaga J, Taniguchi Y, Nosaka K, Yoshida M, Satou Y, Sakai T, et al. Identification of aberrantly methylated genes in association with adult T-cell leukemia. Cancer Res 2004; 64: 6002–6009
  • Nakatsuka S, Takakuwa T, Tomita Y, Hoshida Y, Nishiu M, Yamaguchi M, et al. Hypermethylation of death-associated protein (DAP) kinase CpG island is frequent not only in B-cell but also in T- and natural killer (NK)/T-cell malignancies. Cancer Sci 2003; 94: 87–91
  • Yang Y, Takeuchi S, TsukasakI K, Yamada Y, Hata T, Mori N, et al. Methylation analysis of the adenomatous polyposis coli (APC) gene in adult T-cell leukemia/lymphoma. Leuk Res 2005; 29: 47–51
  • Salvatore P, Benvenuto G, Pero R, Lembo F, Bruni C B, Chiariotti L. Galectin-1 gene expression and methylation state in human T leukemia cell lines. Int J Oncol 2000; 17: 1015–1018
  • Hoshino K, Asou N, Okubo T, Suzushima H, Kiyokawa T, Kawano F, et al. The absence of the p15INK4B gene alterations in adult patients with precursor B-cell acute lymphoblastic leukaemia is a favourable prognostic factor. Br J Haematol 2002; 117: 531–540
  • Wong I H, Ng M H, Huang D P, Lee J C. Aberrant p15 promoter methylation in adult and childhood acute leukemias of nearly all morphologic subtypes: potential prognostic implications. Blood 2000; 95: 1942–1949
  • Chim C S, Tam C Y, Liang R, Kwong Y L. Methylation of p15 and p16 genes in adult acute leukemia: lack of prognostic significance. Cancer 2001; 91: 2222–2229
  • Chim C S, Wong A S, Kwong Y L. Epigenetic dysregulation of the Jak/STAT pathway by frequent aberrant methylation of SHP1 but not SOCS1 in acute leukaemias. Ann Hematol 2004; 83: 527–532
  • Roman-Gomez J, Jimenez-Velasco A, Agirre X, Cervantes F, Sanchez J, Garate J, et al. Promoter hypomethylation of the LINE-1 retrotransposable elements activates sense/antisense transcription and marks the progression of chronic myeloid leukemia. Oncogene 2005; 24: 7213–7223
  • Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002; 21: 5400–5413
  • Kaneda A, Tsukamoto T, Takamura-Enya T, Watanabe N, Kaminishi M, Sugimura T, et al. Frequent hypomethylation in multiple promoter CpG island is associated with global hypomethylation, but not with frequent promoter hypermethylation. Cancer Sci 2004; 95: 58–64
  • Pini J T, Franchina M, Taylor J ME, Kay P H. Evidence that general genomic hypomethylation and focal hypermethylation are two independent molecular events of non-Hodgkin's lymphoma. Oncol Res 2004; 14: 399–405
  • Frigola J, Sole X, Paz M F, Moreno V, Esteller M, Capella G, et al. Differential DNA hypermethylation and hypomethylation signatures in corectal cancer. Hum Mol Genet 2005; 14: 319–326
  • Yoshida M, Nosaka K, Yasunaga J, Nishikata I, Morishita K, Matsuoka M. Aberrant expression of the MEL1S gene identified in association with hypomethylation in adult T-cell leukemia cells. Blood 2004; 103: 2753–2760
  • Watt P M, Kumar R, Kees U R. Promoter demethylation accompanies reactivation of the HOX11 proto-oncogene in leukemia. Genes Chromosomes. Cancer 2000; 29: 371–377
  • Jones P A, Taylor S M. Cellular differentiation, cytidine analogs and DNA methylation. Cell 1980; 20: 85–93
  • Lubbert M. DNA methylation inhibitors in the treatment of leukemias, myelodisplastic syndromes and hemoglobinopathies: clinical results and possible mechanisms of action. Curr Top Microbiol Immunol 2000; 249: 135–164
  • Claus R, Lubbert M. Epigenetic targets in hematopoietic malignancies. Oncogene 2003; 22: 6489–6496
  • Szyf M, Pakneshan P, Rabbani S A. DNA demethylation and cancer: therapeutic implications. Cancer Lett 2004; 211: 133–143
  • Ruter B, Wijermans P W, Lubbert M. DNA methylation as a therapeutic target in hematologic disorders: recent results in older patients with myelodysplasia and acute myeloid leukemia. Int J Hematol 2004; 80: 128–135
  • Avramis V I, Mecum R A, Nyce J, Steele D A, Holcenberg J S. Pharmacodynamic and DNA methylation studies of high-dose 1-β-D-arabinofuranosyl cytosine before and after in vivo 5-azacytidine treatment in pediatric patients with refractory acute lymphocytic leukemia. Cancer Chemother Pharmacol 1989; 24: 203–210
  • Youssef E M, Chen X Q, Higuchi E, Kondo Y, Garcia-Manero G, Lotan R, et al. Hypermethylation and silencing of the putative tumor suppressor Tazarotene-induced gene 1 in human cancers. Cancer Res 2004; 64: 2411–2417
  • Schmelz K, Sattler N, Wagner M, Lubbert M, Dorken B, Tamm I. Induction of gene expression by 5-aza-2′-deoxycytidine in acute myeloid leukemia (AML) and myelodysplastic syndrome (MDS) but not epithelial cells by DNA-methylation-dependent and -independent mechanisms. Leukemia 2005; 19: 103–111
  • Shaker S, Bernstein M, Momparler L F, Momparler R L. Preclinical evaluation of antineoplastic activity of inhibitors of DNA methylation (5-aza-2′-deoxycytidine) and histone deacetylation (trichostatin A, depsipeptide) in combination against myeloid leukemic cells. Leuk Res 2003; 27: 437–444
  • El Osta A, Kantharidis P, Zalcberg J R, Wolffe A P. Precipitous release of methyl-CpG binding protein 2 and histone deacetylase 1 from the methylated human multidrug resistance gene (MDR1) on activation. Mol Cell Biol 2002; 22: 1844–1857
  • Lemaire M, Momparler L F, Farinha N J, Bernstein M, Momparler R L. Enhancement of antineoplastic action of 5-aza-2′-deoxycytidine by phenylbutyrate on L1210 leukemic cells. Leuk Lymphoma 2004; 45: 147–154
  • Park C H, Chang J Y, Hahm E R, Park S, Kim H K, Yang C H. Quercetin, a potent inhibitor against β-catenin/Tcf signaling in SW480 colon cancer cells. Biochem Biophys Res Commun 2005; 328: 227–234
  • Lepourcelet M, Chen Y N, France D S, Wang H, Crews P, Petersen F, et al. Small-molecule antagonists of the oncogenic Tcf/β-catenin protein complex. Cancer Cell 2004; 5: 91–102
  • Fenaux P. Inhibitors of DNA methylation: beyond myelodysplastic syndromes. Nat Clin Pract Oncol 2005; 2(Suppl 1)S36–S44

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