Reduced TET2 function leads to T-cell lymphoma with follicular helper T-cell-like features in mice

Blood Cancer Journal

Volumn 4, Issue 12, 2014, Pages e264-

  Muto, H ^a,b   Sakata Yanagimoto, M ^a,b   Nagae, G ^c   Shiozawa, Y ^d   Miyake, Y ^b   Yoshida, K ^d   Enami, T ^b   Kamada, Y ^b   Kato, T ^b   Uchida, K ^b   Nanmoku, T ^e   Obara, N ^a,b   Suzukawa, K ^a,b,e   Sanada, M ^d   Nakamura, N ^f   Aburatani, H ^c   Ogawa, S ^d   Chiba, S ^a,b  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e UNIVERSITY OF TSUKUBA HOSPITAL   (Japan)

^f TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD45 ANTIGEN; DIOXYGENASE; TEN ELEVEN TRANSLOCATION 2; TRANSCRIPTOME; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; ONCOPROTEIN; TET2 PROTEIN, MOUSE;

ANGIOIMMUNOBLASTIC T CELL LYMPHOMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; COMPARATIVE STUDY; CONTROLLED STUDY; CPG ISLAND; EPIGENETICS; FETUS; GENE EXPRESSION; GENE SILENCING; GRANULOCYTE; HELPER CELL; LOSS OF FUNCTION MUTATION; LYMPHOMA CELL; MOUSE; NONHUMAN; PERIPHERAL T CELL LYMPHOMA; PHENOTYPE; SPLEEN CELL; T CELL LYMPHOMA; TRANSCRIPTION INITIATION SITE; ANIMAL; BIOSYNTHESIS; CELL TRANSFORMATION; EXPERIMENTAL NEOPLASM; FOLLICULAR LYMPHOMA; GENETICS; HUMAN; METABOLISM; MUTATION; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DNA-BINDING PROTEINS; GENE KNOCKDOWN TECHNIQUES; HUMANS; LYMPHOMA, FOLLICULAR; LYMPHOMA, T-CELL; MICE; MICE, TRANSGENIC; MUTATION; NEOPLASMS, EXPERIMENTAL; PROTO-ONCOGENE PROTEINS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84927917194     PISSN: None     EISSN: 20445385     Source Type: Journal    
DOI: 10.1038/bcj.2014.83     Document Type: Article

References (52)

1. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324: 930-935.
2. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, 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.
3. Branco MR, Ficz G, Reik W. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 2011; 13: 7-13.
4. Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature 2010; 468: 839-843.
5. Kriukiene E, Liutkeviciute Z, Klimasauskas S. 5-Hydroxymethylcytosine-the elusive epigenetic mark in mammalian DNA. Chem Soc Rev 2012; 41: 6916-6930.
6. Abdel-Wahab O, Mullally A, Hedvat C, Garcia-Manero G, Patel J, Wadleigh M et al. Genetic characterization of TET1, TET2, and TET3 alterations in myeloid malignancies. Blood 2009; 114: 144-147.
7. Delhommeau F, Dupont S, Della Valle V, James C, Trannoy S, Masse A et al. Mutation in TET2 in myeloid cancers. N Engl J Med 2009; 360: 2289-2301.
8. Langemeijer SM, Kuiper RP, Berends M, Knops R, Aslanyan MG, Massop M et al. Acquired mutations in TET2 are common in myelodysplastic syndromes. Nat Genet 2009; 41: 838-842.
9. Jankowska AM, Szpurka H, Tiu RV, Makishima H, Afable M, Huh J et al. Loss of heterozygosity 4q24 and TET2 mutations associated with myelodysplastic/myeloproliferative neoplasms. Blood 2009; 113: 6403-6410.
10. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 2010; 18: 553-567.
11. Perez C, Martinez-Calle N, Martin-Subero JI, Segura V, Delabesse E, Fernandez- Mercado M et al. TET2 mutations are associated with specific 5-methylcytosine and 5-hydroxymethylcytosine profiles in patients with chronic myelomonocytic leukemia. PLoS One 2012; 7: e31605.
12. Sakata-Yanagimoto M, Enami T, Yoshida K, Shiraishi Y, Ishii R, Miyake Y et al. Somatic RHOA mutation in angioimmunoblastic T cell lymphoma. Nat Genet 2014; 46: 171-175.
13. Lemonnier F, Couronne L, Parrens M, Jais JP, Travert M, Lamant L et al. Recurrent TET2 mutations in peripheral T-cell lymphomas correlate with TFH-like features and adverse clinical parameters. Blood 2012; 120: 1466-1469.
14. Quivoron C, Couronne L, Della Valle V, Lopez CK, Plo I, Wagner-Ballon O et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 2011; 20: 25-38.
15. de Leval L, Gisselbrecht C, Gaulard P. Advances in the understanding and management of angioimmunoblastic T-cell lymphoma. Br J Haematol 2010; 148: 673-689.
16. de Leval L, Rickman DS, Thielen C, Reynies A, Huang YL, Delsol G et al. The gene expression profile of nodal peripheral T-cell lymphoma demonstrates a molecular link between angioimmunoblastic T-cell lymphoma (AITL) and follicular helper T (TFH) cells. Blood 2007; 109: 4952-4963.
17. Vinuesa CG, Tangye SG, Moser B, Mackay CR. Follicular B helper T cells in antibody responses and autoimmunity. Nat Rev Immunol 2005; 5: 853-865.
18. Fazilleau N, Mark L, McHeyzer-Williams LJ, McHeyzer-Williams MG. Follicular helper T cells: lineage and location. Immunity 2009; 30: 324-335.
19. Kroenke MA, Eto D, Locci M, Cho M, Davidson T, Haddad EK et al. Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation. J Immunol 2012; 188: 3734-3744.
20. Yu D, Rao S, Tsai LM, Lee SK, He Y, Sutcliffe EL et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 2009; 31: 457-468.
21. Nurieva RI, Chung Y, Martinez GJ, Yang XO, Tanaka S, Matskevitch TD et al. Bcl6 mediates the development of T follicular helper cells. Science 2009; 325: 1001-1005.
22. Ree HJ, Kadin ME, Kikuchi M, Ko YH, Suzumiya J, Go JH. Bcl-6 expression in reactive follicular hyperplasia, follicular lymphoma, and angioimmunoblastic T-cell lymphoma with hyperplastic germinal centers: heterogeneity of intrafollicular T-cells and their altered distribution in the pathogenesis of angioimmunoblastic T-cell lymphoma. Hum Pathol 1999; 30: 403-411.
23. Natkunam Y, Tedoldi S, Paterson JC, Zhao S, Rodriguez-Justo M, Beck AH et al. Characterization of c-Maf transcription factor in normal and neoplastic hematolymphoid tissue and its relevance in plasma cell neoplasia. Am J Clin Pathol 2009; 132: 361-371.
24. Hiramatsu Y, Suto A, Kashiwakuma D, Kanari H, Kagami S, Ikeda K et al. c-Maf activates the promoter and enhancer of the IL-21 gene, and TGF-beta inhibits c-Maf-induced IL-21 production in CD4+ T cells. J Leukoc Biol 2010; 87: 703-712.
25. Chen M, Guo Z, Ju W, Ryffel B, He X, Zheng SG. The development and function of follicular helper T cells in immune responses. Cell Mol Immunol 2012; 9: 375-379.
26. Moran-Crusio K, Reavie L, Shih A, Abdel-Wahab O, Ndiaye-Lobry D, Lobry C et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 2011; 20: 11-24.
27. Li Z, Cai X, Cai CL, Wang J, Zhang W, Petersen BE et al. Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood 2011; 118: 4509-4518.
28. Ko M, Bandukwala HS, An J, Lamperti ED, Thompson EC, Hastie R et al. Ten-Eleven- Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proc Natl Acad Sci USA 2011; 108: 14566-14571.
29. Kunimoto H, Fukuchi Y, Sakurai M, Sadahira K, Ikeda Y, Okamoto S et al. Tet2 disruption leads to enhanced self-renewal and altered differentiation of fetal liver hematopoietic stem cells. Sci Rep 2012; 2: 273.
30. Shide K, Kameda T, Shimoda H, Yamaji T, Abe H, Kamiunten A et al. TET2 is essential for survival and hematopoietic stem cell homeostasis. Leukemia 2012; 26: 2216-2223.
31. Tang H, Araki K, Li Z, Yamamura K. Characterization of Ayu17-449 gene expression and resultant kidney pathology in a knockout mouse model. Transgenic Res 2008; 17: 599-608.
32. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011; 473: 398-402.
33. Gaulard P, de Leval L. Follicular helper T cells: implications in neoplastic hematopathology. Semin Diagn Pathol 2011; 28: 202-213.
34. Ogata H, Goto S, Fujibuchi W, Kanehisa M. Computation with the KEGG pathway database. Biosystems 1998; 47: 119-128.
35. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genomewide expression profiles. Proc Natl Acad Sci USA 2005; 102(43): 15545-15550.
36. Chtanova T, Tangye SG, Newton R, Frank N, Hodge MR, Rolph MS et al. T follicular helper cells express a distinctive transcriptional profile, reflecting their role as non-Th1/Th2 effector cells that provide help for B cells. J Immunol 2004; 173: 68-78.
37. Chtanova T, Newton R, Liu SM, Weininger L, Young TR, Silva DG et al. Identification of T cell-restricted genes, and signatures for different T cell responses, using a comprehensive collection of microarray datasets. J Immunol 2005; 175: 7837-7847.
38. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE et al. Modelbased analysis of ChIP-Seq (MACS). Genome Biol 2008; 9: R137.
39. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012; 13(7): 484-492.
40. Robertson J, Robertson AB, Klungland A. The presence of 5-hydroxymethylcytosine at the gene promoter and not in the gene body negatively regulates gene expression. Biochem Biophys Res Commun 2011; 411: 40-43.
41. Lai AY, Fatemi M, Dhasarathy A, Malone C, Sobol SE, Geigerman C et al. DNA methylation prevents CTCF-mediated silencing of the oncogene BCL6 in B cell lymphomas. J Exp Med 2010; 207: 1939-1950.
42. Palomero T, Couronne L, Khiabanian H, Kim MY, Ambesi-Impiombato A, Perez-Garcia A et al. Recurrent mutations in epigenetic regulators, RHOA and FYN kinase in peripheral T cell lymphomas. Nat Genet 2014; 46: 166-170.
43. Yoo HY, Sung MK, Lee SH, Kim S, Lee H, Park S et al. A recurrent inactivating mutation in RHOA GTPase in angioimmunoblastic T cell lymphoma. Nat Genet 2014; 46: 371-375.
44. Auguste T, Travert M, Tarte K, Ame-Thomas P, Artchounin C, Martin-Garcia N et al. ROQUIN/RC3H1 alterations are not found in angioimmunoblastic T-cell lymphoma. PLoS One 2013; 8: e64536.
45. Ellyard JI, Chia T, Rodriguez-Pinilla SM, Martin JL, Hu X, Navarro-Gonzalez M et al. Heterozygosity for Roquinsan leads to angioimmunoblastic T-cell lymphoma-like tumors in mice. Blood 2012; 120: 812-821.
46. Vinuesa CG, Cook MC, Angelucci C, Athanasopoulos V, Rui L, Hill KM et al. A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature 2005; 435: 452-458.
47. Baron BW, Anastasi J, Montag A, Huo D, Baron RM, Karrison T et al. The human BCL6 transgene promotes the development of lymphomas in the mouse. Proc Natl Acad Sci USA 2004; 101: 14198-14203.
48. Busque L, Patel JP, Figueroa ME, Vasanthakumar A, Provost S, Hamilou Z et al. Recurrent somatic TET2 mutations in normal elderly individuals with clonal hematopoiesis. Nat Genet 2012; 44: 1179-1181.
49. Asmar F, Punj V, Christensen J, Pedersen MT, Pedersen A, Nielsen AB et al. Genome-wide profiling identifies a DNA methylation signature that associates with TET2 mutations in diffuse large B-cell lymphoma. Haematologica 2013; 98: 1912-1920.
50. Pastor WA, Pape UJ, Huang Y, Henderson HR, Lister R, Ko M et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 2011; 473: 394-397.
51. Kantarjian H, Oki Y, Garcia-Manero G, Huang X, O'Brien S, Cortes J et al. Results of a randomized study of 3 schedules of low-dose decitabine in higher-risk myelodysplastic syndrome and chronic myelomonocytic leukemia. Blood 2007; 109: 52-57.
52. 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.