Crystal Structure of TET2-DNA Complex: Insight into TET-Mediated 5mC Oxidation

Cell

Volumn 155, Issue 7, 2013, Pages 1545-1555

  Hu, Lulu ^a,b   Li, Ze ^a   Cheng, Jingdong ^a   Rao, Qinhui ^a   Gong, Wei ^a   Liu, Mengjie ^a   Shi, Yujiang Geno ^a,c   Zhu, Jiayu ^a   Wang, Ping ^a   Xu, Yanhui ^a,b  

^a FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^b FUDAN UNIVERSITY   (China)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; CPG DINUCLEOTIDE; DINUCLEOTIDE; DNA; DOUBLE STRANDED DNA; FERROUS ION; GLYCINE DERIVATIVE; N OXALYLGLYCINE; TET2 PROTEIN; TUMOR MARKER; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; DNA BINDING PROTEIN; ONCOPROTEIN; TET2 PROTEIN, HUMAN; ZINC;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CPG ISLAND; CRYSTAL STRUCTURE; DNA BINDING; DNA METHYLATION; DNA PROTEIN COMPLEX; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; HYDROGEN BOND; OXIDATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN STABILITY; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY;

5-METHYLCYTOSINE; AMINO ACID SEQUENCE; CPG ISLANDS; CRYSTALLOGRAPHY, X-RAY; DNA; DNA METHYLATION; DNA-BINDING PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTO-ONCOGENE PROTEINS; SEQUENCE ALIGNMENT; ZINC;

EID: 84894560490     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.11.020     Document Type: Article

References (76)

1. P.D. Adams, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, N.W. Moriarty, R.J. Read, J.C. Sacchettini, N.K. Sauter, and T.C. Terwilliger PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr. D Biol. Crystallogr. 58 2002 1948 1954
2. A. Bird DNA methylation patterns and epigenetic memory Genes Dev. 16 2002 6 21
3. K. Blaschke, K.T. Ebata, M.M. Karimi, J.A. Zepeda-Martínez, P. Goyal, S. Mahapatra, A. Tam, D.J. Laird, M. Hirst, and A. Rao et al. Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in ES cells Nature 500 2013 222 226
4. M.R. Branco, G. Ficz, and W. Reik Uncovering the role of 5-hydroxymethylcytosine in the epigenome Nat. Rev. Genet. 13 2012 7 13
5. L. Cimmino, O. Abdel-Wahab, R.L. Levine, and I. Aifantis TET family proteins and their role in stem cell differentiation and transformation Cell Stem Cell 9 2011 193 204
6. L.J. Cliffe, R. Kieft, T. Southern, S.R. Birkeland, M. Marshall, K. Sweeney, and R. Sabatini JBP1 and JBP2 are two distinct thymidine hydroxylases involved in J biosynthesis in genomic DNA of African trypanosomes Nucleic Acids Res. 37 2009 1452 1462
7. M.M. Dawlaty, K. Ganz, B.E. Powell, Y.C. Hu, S. Markoulaki, A.W. Cheng, Q. Gao, J. Kim, S.W. Choi, D.C. Page, and R. Jaenisch Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development Cell Stem Cell 9 2011 166 175
8. DeLano, W.L. (2002). The PyMOL Molecular Graphics System. http://www.pymol.org.
9. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
10. S.A. Forbes, G. Tang, N. Bindal, S. Bamford, E. Dawson, C. Cole, C.Y. Kok, M. Jia, R. Ewing, and A. Menzies et al. COSMIC (the Catalogue of Somatic Mutations in Cancer): a resource to investigate acquired mutations in human cancer Nucleic Acids Res. 38 Database issue 2010 D652 D657
11. D. Globisch, M. Münzel, M. Müller, S. Michalakis, M. Wagner, S. Koch, T. Brückl, M. Biel, and T. Carell Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates PLoS ONE 5 2010 e15367
12. M.G. Goll, and T.H. Bestor Eukaryotic cytosine methyltransferases Annu. Rev. Biochem. 74 2005 481 514
13. T.P. Gu, F. Guo, H. Yang, H.P. Wu, G.F. Xu, W. Liu, Z.G. Xie, L. Shi, X. He, and S.G. Jin et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes Nature 477 2011 606 610
14. Z. Han, T. Niu, J. Chang, X. Lei, M. Zhao, Q. Wang, W. Cheng, J. Wang, Y. Feng, and J. Chai Crystal structure of the FTO protein reveals basis for its substrate specificity Nature 464 2010 1205 1209
15. Y.F. He, B.Z. Li, Z. Li, P. Liu, Y. Wang, Q. Tang, J. Ding, Y. Jia, Z. Chen, and L. Li et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA Science 333 2011 1303 1307
16. W.A. Hendrickson Determination of macromolecular structures from anomalous diffraction of synchrotron radiation Science 254 1991 51 58
17. L. Holm, and P. Rosenström Dali server: conservation mapping in 3D Nucleic Acids Res. 38 Web Server issue 2010 W545 W549
18. S. Ito, A.C. D'Alessio, O.V. Taranova, K. Hong, L.C. Sowers, and Y. Zhang Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification Nature 466 2010 1129 1133
19. S. Ito, L. Shen, Q. Dai, S.C. Wu, L.B. Collins, J.A. Swenberg, C. He, and Y. Zhang Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine Science 333 2011 1300 1303
20. L.M. Iyer, M. Tahiliani, A. Rao, and L. Aravind Prediction of novel families of enzymes involved in oxidative and other complex modifications of bases in nucleic acids Cell Cycle 8 2009 1698 1710
21. M. Ko, Y. Huang, A.M. Jankowska, U.J. Pape, M. Tahiliani, H.S. Bandukwala, J. An, E.D. Lamperti, K.P. Koh, and R. Ganetzky et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2 Nature 468 2010 839 843
22. M. Ko, J. An, H.S. Bandukwala, L. Chavez, T. Aijö, W.A. Pastor, M.F. Segal, H. Li, K.P. Koh, and H. Lähdesmäki et al. Modulation of TET2 expression and 5-methylcytosine oxidation by the CXXC domain protein IDAX Nature 497 2013 122 126
23. S. Kriaucionis, and N. Heintz The nuclear DNA base 5- hydroxymethylcytosine is present in Purkinje neurons and the brain Science 324 2009 929 930
24. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Cryst. 26 1993 283 291
25. C.G. Lian, Y. Xu, C. Ceol, F. Wu, A. Larson, K. Dresser, W. Xu, L. Tan, Y. Hu, and Q. Zhan et al. Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma Cell 150 2012 1135 1146
26. R.B. Lorsbach, J. Moore, S. Mathew, S.C. Raimondi, S.T. Mukatira, and J.R. Downing TET1, a member of a novel protein family, is fused to MLL in acute myeloid leukemia containing the t(10;11)(q22;q23) Leukemia 17 2003 637 641
27. R. Ono, T. Taki, T. Taketani, M. Taniwaki, H. Kobayashi, and Y. Hayashi LCX, leukemia-associated protein with a CXXC domain, is fused to MLL in acute myeloid leukemia with trilineage dysplasia having t(10;11)(q22;q23) Cancer Res. 62 2002 4075 4080
28. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
29. W.A. Pastor, L. Aravind, and A. Rao TETonic shift: biological roles of TET proteins in DNA demethylation and transcription Nat. Rev. Mol. Cell Biol. 14 2013 341 356
30. E.S. Radisky, C.J. Lu, G. Kwan, and D.E. Koshland Jr. Role of the intramolecular hydrogen bond network in the inhibitory power of chymotrypsin inhibitor 2 Biochemistry 44 2005 6823 6830
31. R.J. Roberts, and X. Cheng Base flipping Annu. Rev. Biochem. 67 1998 181 198
32. C.J. Schofield, and Z. Zhang Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes Curr. Opin. Struct. Biol. 9 1999 722 731
33. B. Sedgwick Repairing DNA-methylation damage Nat. Rev. Mol. Cell Biol. 5 2004 148 157
34. O. Sundheim, C.B. Vågbø, M. Bjørås, M.M. Sousa, V. Talstad, P.A. Aas, F. Drabløs, H.E. Krokan, J.A. Tainer, and G. Slupphaug Human ABH3 structure and key residues for oxidative demethylation to reverse DNA/RNA damage EMBO J. 25 2006 3389 3397
35. A. Szwagierczak, S. Bultmann, C.S. Schmidt, F. Spada, and H. Leonhardt Sensitive enzymatic quantification of 5-hydroxymethylcytosine in genomic DNA Nucleic Acids Res. 38 2010 e181
36. M. Tahiliani, K.P. Koh, Y. Shen, W.A. Pastor, H. Bandukwala, Y. Brudno, S. Agarwal, L.M. Iyer, D.R. Liu, L. Aravind, and A. Rao Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1 Science 324 2009 930 935
37. L. Tan, and Y.G. Shi Tet family proteins and 5-hydroxymethylcytosine in development and disease Development 139 2012 1895 1902
38. S.D. Taverna, H. Li, A.J. Ruthenburg, C.D. Allis, and D.J. Patel How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers Nat. Struct. Mol. Biol. 14 2007 1025 1040
39. K. Williams, J. Christensen, M.T. Pedersen, J.V. Johansen, P.A. Cloos, J. Rappsilber, and K. Helin TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity Nature 473 2011 343 348
40. K. Williams, J. Christensen, and K. Helin DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep. 13 2012 28 35
41. H. Wu, and Y. Zhang Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation Genes Dev. 25 2011 2436 2452
42. G.R. Wyatt, and S.S. Cohen The bases of the nucleic acids of some bacterial and animal viruses: the occurrence of 5-hydroxymethylcytosine Biochem. J. 55 1953 774 782
43. Y. Xu, C. Xu, A. Kato, W. Tempel, J.G. Abreu, C. Bian, Y. Hu, D. Hu, B. Zhao, and T. Cerovina et al. Tet3 CXXC domain and dioxygenase activity cooperatively regulate key genes for Xenopus eye and neural development Cell 151 2012 1200 1213
44. C.G. Yang, C. Yi, E.M. Duguid, C.T. Sullivan, X. Jian, P.A. Rice, and C. He Crystal structures of DNA/RNA repair enzymes AlkB and ABH2 bound to dsDNA Nature 452 2008 961 965
45. C.G. Yang, K. Garcia, and C. He Damage detection and base flipping in direct DNA alkylation repair ChemBioChem 10 2009 417 423
46. R. Yin, S.Q. Mao, B. Zhao, Z. Chong, Y. Yang, C. Zhao, D. Zhang, H. Huang, J. Gao, and Z. Li et al. Ascorbic acid enhances Tet-mediated 5-methylcytosine oxidation and promotes DNA demethylation in mammals J. Am. Chem. Soc. 135 2013 10396 10403
47. B. Yu, W.C. Edstrom, J. Benach, Y. Hamuro, P.C. Weber, B.R. Gibney, and J.F. Hunt Crystal structures of catalytic complexes of the oxidative DNA/RNA repair enzyme AlkB Nature 439 2006 879 884
48. Z. Yu, P.A. Genest, B. ter Riet, K. Sweeney, C. DiPaolo, R. Kieft, E. Christodoulou, A. Perrakis, J.M. Simmons, and R.P. Hausinger et al. The protein that binds to DNA base J in trypanosomatids has features of a thymidine hydroxylase Nucleic Acids Res. 35 2007 2107 2115
49. M. Yu, G.C. Hon, K.E. Szulwach, C.X. Song, L. Zhang, A. Kim, X. Li, Q. Dai, Y. Shen, and B. Park et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome Cell 149 2012 1368 1380
50. U. Bacher, S. Weissmann, A. Kohlmann, S. Schindela, T. Alpermann, S. Schnittger, W. Kern, T. Haferlach, and C. Haferlach TET2 deletions are a recurrent but rare phenomenon in myeloid malignancies and are frequently accompanied by TET2 mutations on the remaining allele Br. J. Haematol. 156 2012 67 75
51. M. Brecqueville, J. Rey, F. Bertucci, E. Coppin, P. Finetti, N. Carbuccia, N. Cervera, V. Gelsi-Boyer, C. Arnoulet, and O. Gisserot et al. Mutation analysis of ASXL1, CBL, DNMT3A, IDH1, IDH2, JAK2, MPL, NF1, SF3B1, SUZ12, and TET2 in myeloproliferative neoplasms Genes Chromosomes Cancer 51 2012 743 755
52. W.C. Chou, S.C. Chou, C.Y. Liu, C.Y. Chen, H.A. Hou, Y.Y. Kuo, M.C. Lee, B.S. Ko, J.L. Tang, and M. Yao et al. TET2 mutation is an unfavorable prognostic factor in acute myeloid leukemia patients with intermediate-risk cytogenetics Blood 118 2011 3803 3810
53. F. Delhommeau, S. Dupont, V. Della Valle, C. James, S. Trannoy, A. Massé, O. Kosmider, J.P. Le Couedic, F. Robert, and A. Alberdi et al. Mutation in TET2 in myeloid cancers N. Engl. J. Med. 360 2009 2289 2301
54. A.M. Jankowska, H. Szpurka, R.V. Tiu, H. Makishima, M. Afable, J. Huh, C.L. O'Keefe, R. Ganetzky, M.A. McDevitt, and J.P. Maciejewski Loss of heterozygosity 4q24 and TET2 mutations associated with myelodysplastic/ myeloproliferative neoplasms Blood 113 2009 6403 6410
55. G. Jia, Y. Fu, X. Zhao, Q. Dai, G. Zheng, Y. Yang, C. Yi, T. Lindahl, T. Pan, Y.G. Yang, and C. He N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO Nat. Chem. Biol. 7 2011 885 887
56. A. Kohlmann, V. Grossmann, H.U. Klein, S. Schindela, T. Weiss, B. Kazak, F. Dicker, S. Schnittger, M. Dugas, and W. Kern et al. Next-generation sequencing technology reveals a characteristic pattern of molecular mutations in 72.8% of chronic myelomonocytic leukemia by detecting frequent alterations in TET2, CBL, RAS, and RUNX1 Journal of clinical oncology: official journal of the American Society of Clinical Oncology 28 2010 3858 3865
57. A. Kohlmann, H.U. Klein, S. Weissmann, S. Bresolin, T. Chaplin, H. Cuppens, E. Haschke-Becher, B. Garicochea, V. Grossmann, and B. Hanczaruk et al. The Interlaboratory RObustness of Next-generation sequencing (IRON) study: a deep sequencing investigation of TET2, CBL and KRAS mutations by an international consortium involving 10 laboratories Leukemia 25 2011 1840 1848
58. O. Kosmider, V. Gelsi-Boyer, M. Cheok, S. Grabar, V. Della-Valle, F. Picard, F. Viguié, B. Quesnel, O. Beyne-Rauzy, E. Solary Groupe Francophone des Myélodysplasies TET2 mutation is an independent favorable prognostic factor in myelodysplastic syndromes (MDSs) Blood 114 2009 3285 3291
59. O. Kosmider, V. Gelsi-Boyer, M. Ciudad, C. Racoeur, V. Jooste, N. Vey, B. Quesnel, P. Fenaux, J.N. Bastie, O. Beyne-Rauzy Groupe Francophone des Myélodysplasies TET2 gene mutation is a frequent and adverse event in chronic myelomonocytic leukemia Haematologica 94 2009 1676 1681
60. S.M. Langemeijer, R.P. Kuiper, M. Berends, R. Knops, M.G. Aslanyan, M. Massop, E. Stevens-Linders, P. van Hoogen, A.G. van Kessel, and R.A. Raymakers et al. Acquired mutations in TET2 are common in myelodysplastic syndromes Nat. Genet. 41 2009 838 842
61. H. Makishima, A.M. Jankowska, M.A. McDevitt, C. O'Keefe, S. Dujardin, H. Cazzolli, B. Przychodzen, C. Prince, J. Nicoll, and H. Siddaiah et al. CBL, CBLB, TET2, ASXL1, and IDH1/2 mutations and additional chromosomal aberrations constitute molecular events in chronic myelogenous leukemia Blood 117 2011 e198 e206
62. K.H. Metzeler, K. Maharry, M.D. Radmacher, K. Mrozek, D. Margeson, H. Becker, J. Curfman, K.B. Holland, S. Schwind, and S.P. Whitman et al. TET2 mutations improve the new European LeukemiaNet risk classification of acute myeloid leukemia: a Cancer and Leukemia Group B study J. Clin. Oncol. 29 2011 1373 1381
63. A.M. Mohamedali, A.E. Smith, J. Gaken, N.C. Lea, S.A. Mian, N.B. Westwood, C. Strupp, N. Gattermann, U. Germing, and G.J. Mufti Novel TET2 mutations associated with UPD4q24 in myelodysplastic syndrome J. Clin. Oncol. 27 2009 4002 4006
64. J. Nomdedéu, M. Hoyos, M. Carricondo, J. Esteve, E. Bussaglia, C. Estivill, J.M. Ribera, R. Duarte, O. Salamero, and D. Gallardo et al. Adverse impact of IDH1 and IDH2 mutations in primary AML: experience of the Spanish CETLAM group Leuk. Res. 36 2012 990 997
65. C. Quivoron, L. Couronné, V. Della Valle, C.K. Lopez, I. Plo, O. Wagner-Ballon, M. Do Cruzeiro, F. Delhommeau, B. Arnulf, and M.H. Stern et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis Cancer Cell 20 2011 25 38
66. J. Rocquain, N. Carbuccia, V. Trouplin, S. Raynaud, A. Murati, M. Nezri, Z. Tadrist, S. Olschwang, N. Vey, and D. Birnbaum et al. Combined mutations of ASXL1, CBL, FLT3, IDH1, IDH2, JAK2, KRAS, NPM1, NRAS, RUNX1, TET2 and WT1 genes in myelodysplastic syndromes and acute myeloid leukemias BMC Cancer 10 2010 401
67. A.E. Smith, A.M. Mohamedali, A. Kulasekararaj, Z. Lim, J. Gäken, N.C. Lea, B. Przychodzen, S.A. Mian, E.E. Nasser, and C. Shooter et al. Next-generation sequencing of the TET2 gene in 355 MDS and CMML patients reveals low-abundance mutant clones with early origins, but indicates no definite prognostic value Blood 116 2010 3923 3932
68. P.S. Tarpey, S. Behjati, S.L. Cooke, P. Van Loo, D.C. Wedge, N. Pillay, J. Marshall, S. O'Meara, H. Davies, and S. Nik-Zainal et al. Frequent mutation of the major cartilage collagen gene COL2A1 in chondrosarcoma Nat. Genet. 45 2013 923 926
69. A. Tefferi, R.L. Levine, K.H. Lim, O. Abdel-Wahab, T.L. Lasho, J. Patel, C.M. Finke, A. Mullally, C.Y. Li, A. Pardanani, and D.G. Gilliland Frequent TET2 mutations in systemic mastocytosis: clinical, KITD816V and FIP1L1-PDGFRA correlates Leukemia 23 2009 900 904
70. A. Thiel, M. Beier, D. Ingenhag, K. Servan, M. Hein, V. Moeller, B. Betz, B. Hildebrandt, C. Evers, U. Germing, and B. Royer-Pokora Comprehensive array CGH of normal karyotype myelodysplastic syndromes reveals hidden recurrent and individual genomic copy number alterations with prognostic relevance Leukemia 25 2011 387 399
71. F. Traina, V. Visconte, A.M. Jankowska, H. Makishima, C.L. O'Keefe, P. Elson, Y. Han, F.H. Hsieh, M.A. Sekeres, and R.S. Mali et al. Single nucleotide polymorphism array lesions, TET2, DNMT3A, ASXL1 and CBL mutations are present in systemic mastocytosis PLoS ONE 7 2012 e43090
72. M.T. Voso, E. Fabiani, A. Piciocchi, C. Matteucci, L. Brandimarte, C. Finelli, E. Pogliani, E. Angelucci, G. Fioritoni, and P. Musto et al. Role of BCL2L10 methylation and TET2 mutations in higher risk myelodysplastic syndromes treated with 5-azacytidine Leukemia 25 2011 1910 1913
73. J. Wang, X. Ai, R.P. Gale, Z. Xu, T. Qin, L. Fang, H. Zhang, L. Pan, N. Hu, Y. Zhang, and Z. Xiao TET2, ASXL1 and EZH2 mutations in Chinese with myelodysplastic syndromes Leuk. Res. 37 2013 305 311
74. S. Weissmann, T. Alpermann, V. Grossmann, A. Kowarsch, N. Nadarajah, C. Eder, F. Dicker, A. Fasan, C. Haferlach, and T. Haferlach et al. Landscape of TET2 mutations in acute myeloid leukemia Leukemia 26 2012 934 942
75. J. Yamazaki, R. Taby, A. Vasanthakumar, T. Macrae, K.R. Ostler, L. Shen, H.M. Kantarjian, M.R. Estecio, J. Jelinek, and L.A. Godley et al. Effects of TET2 mutations on DNA methylation in chronic myelomonocytic leukemia Epigenetics 7 2012 201 207
76. K. Yoshida, M. Sanada, Y. Shiraishi, D. Nowak, Y. Nagata, R. Yamamoto, Y. Sato, A. Sato-Otsubo, A. Kon, and M. Nagasaki et al. Frequent pathway mutations of splicing machinery in myelodysplasia Nature 478 2011 64 69