6-Thioguanine reactivates epigenetically silenced genes in acute lymphoblastic leukemia cells by facilitating proteasome-mediated degradation of DNMT

Cancer Research

Volumn 71, Issue 5, 2011, Pages 1904-1911

  Yuan, Bifeng ^a   Zhang, Jing ^a,b   Wang, Hongxia ^a   Xiong, Lei ^a   Cai, Qian ^a   Wang, Tina ^a   Jacobsen, Steven ^c   Pradhan, Sriharsa ^d   Wang, Yinsheng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHAANXI NORMAL UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NEW ENGLAND BIOLABS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; CYTOSINE; DNA METHYLTRANSFERASE 1; LYSINE; LYSINE SPECIFIC DEMETHYLASE 1; PROTEASOME; TIOGUANINE; TRANSCRIPTION FACTOR; UBIQUITIN; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; DRUG BLOOD LEVEL; DRUG MECHANISM; ENZYME DEGRADATION; EPIGENETICS; EXON; GENE ACTIVATION; GENE EXPRESSION; GENE REACTIVATION; GENE SEQUENCE; GENE SILENCING; HUMAN; HUMAN CELL; LEUKEMIA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION;

ANTIMETABOLITES, ANTINEOPLASTIC; BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; GENE EXPRESSION; GENE SILENCING; HUMANS; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEASOME ENDOPEPTIDASE COMPLEX; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THIOGUANINE;

EID: 79952236603     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3430     Document Type: Article

References (48)

1. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33:245-54. (Pubitemid 36278835)
2. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002;16:6-21. (Pubitemid 34049633)
3. Scarano MI, Strazzullo M, Matarazzo MR, D'Esposito M. DNA methylation 40 years later: its role in human health and disease. J Cell Physiol 2005;204:21-35. (Pubitemid 40776803)
4. Robertson KD. DNA methylation and human disease. Nat Rev Genet 2005;6:597-610. (Pubitemid 41044297)
5. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;349:2042-54. (Pubitemid 37448928)
6. Costello JF, Fruhwald MC, Smiraglia DJ, Rush LJ, Robertson GP, Gao X, et al. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet 2000;24:132-8.
7. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 2005;74:481-514. (Pubitemid 40995515)
8. Bestor TH. Activation of mammalian DNA methyltransferase by cleavage of a Zn binding regulatory domain. EMBO J 1992;11:2611-7.
9. Leonhardt H, Page AW, Weier HU, Bestor TH. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 1992;71:865-73.
10. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999;99:247-57. (Pubitemid 29519904)
11. Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998;19:219-20. (Pubitemid 28309328)
12. Szyf M. DNA methylation properties: consequences for pharmacology. Trends Pharmacol Sci 1994;15:233-8. (Pubitemid 24210728)
13. Wu J, Issa JP, Herman J, Bassett DE Jr., Nelkin BD, Baylin SB. Expression of an exogenous eukaryotic DNA methyltransferase gene induces transformation of NIH 3T3 cells. Proc Natl Acad Sci U S A 1993;90:8891-5. (Pubitemid 23306416)
14. Laird PW, Jackson-Grusby L, Fazeli A, Dickinson SL, Jung WE, Li E, et al. Suppression of intestinal neoplasia by DNA hypomethylation. Cell 1995;81:197-205.
15. Przybylski M, Kozlowska A, Pietkiewicz PP, Lutkowska A, Lianeri M, Jagodzinski PP. Increased CXCR4 expression in AsPC1 pancreatic carcinoma cells with RNA interference-mediated knockdown of DNMT1 and DNMT3B. Biomed Pharmacother 2010;64:254-8.
16. Fournel M, Sapieha P, Beaulieu N, Besterman JM, MacLeod AR. Down-regulation of human DNA-(cytosine-5) methyltransferase induces cell cycle regulators p16(ink4A) and p21(WAF/Cip1) by distinct mechanisms. J Biol Chem 1999;274:24250-6.
17. Issa JP, Vertino PM, Wu J, Sazawal S, Celano P, Nelkin BD, et al. Increased cytosine DNA-methyltransferase activity during colon cancer progression. J Natl Cancer Inst 1993;85:1235-40. (Pubitemid 23223530)
18. 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;27:2291-8.
19. Baylin SB, Esteller M, Rountree MR, Bachman KE, Schuebel K, Herman JG. Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum Mol Genet 2001;10:687-92. (Pubitemid 32331576)
20. Ramchandani S, MacLeod AR, Pinard M, von Hofe E, Szyf M. Inhibition of tumorigenesis by a cytosine-DNA, methyltransferase, antisense oligodeoxynucleotide. Proc Natl Acad Sci U S A 1997;94:684-9. (Pubitemid 27053694)
21. Elion GB. Symposium on immunosuppressive drugs. Biochemistry and pharmacology of purine analogues. Fed Proc 1967;26:898-904.
22. Elion GB. The purine path to chemotherapy. Science 1989;244:41-7. (Pubitemid 19130741)
23. Burchenal JH, Murphy ML, Ellison RR, Sykes MP, Tan TC, Leone LA, et al. Clinical evaluation of a new antimetabolite, 6-mercaptopurine, in the treatment of leukemia and allied diseases. Blood 1953;8:965-99.
24. Murray JE, Merrill JP, Harrison JH, Wilson RE, Dammin GJ. Prolonged survival of human-kidney homografts by immunosuppressive drug therapy. N Engl J Med 1963;268:1315-23.
25. Lennard L. The clinical pharmacology of 6-mercaptopurine. Eur J Clin Pharmacol 1992;43:329-39.
26. Bertino JR. Improving the curability of acute leukemia: pharmacologic approaches. Semin Hematol 1991;28:9-11.
27. Karran P, Attard N. Thiopurines in current medical practice: molecular mechanisms and contributions to therapy-related cancer. Nat Rev Cancer 2008;8:24-36.
28. Yuan B, O'Connor TR, Wang Y. 6-Thioguanine and S6-Methylthioguanine are mutagenic in human cells. ACS Chem Biol 2010;5:1021-7.
29. 6-methylthioguanine in genomic DNA of human cancer cells treated with 6-thioguanine. Anal Chem 2010;82:5797-803.
30. 6-sulfonic acid. J Biol Chem 2008;283:23665-70.
31. Krynetski EY, Krynetskaia NF, Gallo AE, Murti KG, Evans WE. A novel protein complex distinct from mismatch repair binds thioguanylated DNA. Mol Pharmacol 2001;59:367-74. (Pubitemid 32108571)
32. Wang H, Wang Y. 6-Thioguanine perturbs cytosine methylation at the CpG dinucleotide site by DNA methyltransferases in vitro and acts as a DNA demethylating agent in vivo. Biochemistry 2009;48:2290-9.
33. Lambooy LH, Leegwater PA, Van Den Heuvel LP, Bokkerink JP, De Abreu RA. Inhibition of DNA methylation in malignant MOLT F4 lymphoblasts by 6-mercaptopurine. Clin Chem 1998;44:556-9. (Pubitemid 28141351)
34. Hogarth LA, Redfern CP, Teodoridis JM, Hall AG, Anderson H, Case MC, et al. The effect of thiopurine drugs on DNA methylation in relation to TPMT expression. Biochem Pharmacol 2008;76:1024-35.
35. Ghoshal K, Datta J, Majumder S, Bai S, Kutay H, Motiwala T, et al. 5- Aza-deoxycytidine induces selective degradation of DNA methyltransferase 1 by a proteasomal pathway that requires the KEN box, bromo-adjacent homology domain, and nuclear localization signal. Mol Cell Biol 2005;25:4727-41. (Pubitemid 40705775)
36. Esteve PO, Chin HG, Benner J, Feehery GR, Samaranayake M, Horwitz GA, et al. Regulation of DNMT1 stability through SET7-mediated lysine methylation in mammalian cells. Proc Natl Acad Sci U S A 2009;106:5076-81.
37. Wang J, Hevi S, Kurash JK, Lei H, Gay F, Bajko J, et al. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet 2009;41:125-9.
38. -ΔΔCT Method. Methods 2001;25:402-8.
39. Taylor KH, Pena-Hernandez KE, Davis JW, Arthur GL, Duff DJ, Shi H, et al. Large-scale CpG methylation analysis identifies novel candidate genes and reveals methylation hotspots in acute lymphoblastic leukemia. Cancer Res 2007;67:2617-25. (Pubitemid 46548948)
40. Lowe ES, Kitchen BJ, Erdmann G, Stork LC, Bostrom BC, Hutchinson R, et al. Plasma pharmacokinetics and cerebrospinal fluid penetration of thioguanine in children with acute lymphoblastic leukemia: a collaborative Pediatric Oncology Branch, NCI, and Children's Cancer Group study. Cancer Chemother Pharmacol 2001; 47:199-205. (Pubitemid 32640753)
41. McLeod SJ, Shum AJ, Lee RL, Takei F, Gold MR. The Rap GTPases regulate integrin-mediated adhesion, cell spreading, actin polymerization, and Pyk2 tyrosine phosphorylation in B lymphocytes. J Biol Chem 2004;279:12009-19. (Pubitemid 38445762)
42. Baker EK, Johnstone RW, Zalcberg JR, El-Osta A. Epigenetic changes to the MDR1 locus in response to chemotherapeutic drugs. Oncogene 2005;24:8061-75. (Pubitemid 41746749)
43. Arakawa H. Netrin-1 and its receptors in tumorigenesis. Nat Rev Cancer 2004;4:978-87. (Pubitemid 39626221)
44. Hankins GR, Sasaki T, Lieu AS, Saulle D, Karimi K, Li JZ, et al. Identification of the deleted in liver cancer 1 gene, DLC1, as a candidate meningioma tumor suppressor. Neurosurgery 2008;63:771-80; discussion 80-1.
45. Liu CX, Musco S, Lisitsina NM, Yaklichkin SY, Lisitsyn NA. Genomic organization of a new candidate tumor suppressor gene, LRP1B. Genomics 2000;69:271-4.
46. Rizzari C, Zucchetti M, Conter V, Diomede L, Bruno A, Gavazzi L, et al. L-asparagine depletion and L-asparaginase activity in children with acute lymphoblastic leukemia receiving i.m. or i.v. Erwinia C. or E. coli L-asparaginase as first exposure. Ann Oncol 2000;11:189-93. (Pubitemid 30148733)
47. Tsurusawa M, Chin M, Iwai A, Nomura K, Maeba H, Taga T, et al. L-Asparagine depletion levels and L-asparaginase activity in plasma of children with acute lymphoblastic leukemia under asparaginase treatment. Cancer Chemother Pharmacol 2004;53:204-8. (Pubitemid 38293717)
48. Pui CH, Robison LL, Look AT. Acute lymphoblastic leukaemia. Lancet 2008;371:1030-43. (Pubitemid 351389536)