Mutant IDH1 Downregulates ATM and Alters DNA Repair and Sensitivity to DNA Damage Independent of TET2

Cancer Cell

Volumn 30, Issue 2, 2016, Pages 337-348

  Inoue, Satoshi ^a   Li, Wanda Y ^a   Tseng, Alan ^a,b   Beerman, Isabel ^c,d   Elia, Andrew J ^a   Bendall, Sean C ^e   Lemonnier, François ^a   Kron, Ken J ^a,b   Cescon, David W ^a   Hao, Zhenyue ^a   Lind, Evan F ^a   Takayama, Naoya ^a   Planello, Aline C ^a,b,f   Shen, Shu Yi ^a,b   Shih, Alan H ^g   Larsen, Dana M ^h   Li, Qinxi ^a   Snow, Bryan E ^a   Wakeham, Andrew ^a   Haight, Jillian ^a   Gorrini, Chiara ^a   Bassi, Christian ^a   Thu, Kelsie L ^a   Murakami, Kiichi ^a   Elford, Alisha R ^a   Ueda, Takeshi ^a,i   Straley, Kimberly ^j   Yen, Katharine E ^j   Melino, Gerry ^k,l   Cimmino, Luisa ^m   Aifantis, Iannis ^m   Levine, Ross L ^g   De Carvalho, Daniel D ^a,b   Lupien, Mathieu ^a,b   Rossi, Derrick J ^c   Nolan, Garry P ^e   Cairns, Rob A ^a   Mak, Tak W ^a,b   more..

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d Harvard University   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF CAMPINAS   (Brazil)

^g MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^h Mbed Pathology   (Canada)

ⁱ HIROSHIMA UNIVERSITY   (Japan)

^j AGIOS PHARMACEUTICALS   (United States)

^k MEDICAL RESEARCH COUNCIL   (United Kingdom)

^l UNIVERSITY OF ROME TOR VERGATA   (Italy)

^m NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DNA; ISOCITRATE DEHYDROGENASE 1; ATM PROTEIN, HUMAN; ATM PROTEIN, MOUSE; DNA BINDING PROTEIN; IDH1 PROTEIN, HUMAN; ISOCITRATE DEHYDROGENASE; ONCOPROTEIN; TET2 PROTEIN, HUMAN; TET2 PROTEIN, MOUSE;

AGED; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOWN REGULATION; HEMATOPOIETIC STEM CELL; HISTONE METHYLATION; HUMAN; KNOCKOUT MOUSE; LEUKEMIA; MOUSE; MUTATOR GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL SELF-RENEWAL; TET2 GENE; ANIMAL; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; DOWN-REGULATION; HEMATOPOIETIC STEM CELLS; HUMANS; ISOCITRATE DEHYDROGENASE; MICE; MUTATION; PROTO-ONCOGENE PROTEINS;

EID: 84978828293     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2016.05.018     Document Type: Article

References (49)

1. An, J., Gonzalez-Avalos, E., Chawla, A., Jeong, M., Lopez-Moyado, I.F., Li, W., Goodell, M.A., Chavez, L., Ko, M., Rao, A., Acute loss of TET function results in aggressive myeloid cancer in mice. Nat. Commun., 6, 2015, 10071.
2. Beerman, I., Seita, J., Inlay, M.A., Weissman, I.L., Rossi, D.J., Quiescent hematopoietic stem cells accumulate DNA damage during aging that is repaired upon entry into cell cycle. Cell Stem Cell 15 (2014), 37–50.
3. Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y., Greenleaf, W.J., Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10 (2013), 1213–1218.
4. Busque, L., Patel, J.P., Figueroa, M.E., Vasanthakumar, A., Provost, S., Hamilou, Z., Mollica, L., Li, J., Viale, A., Heguy, A., et al. Recurrent somatic TET2 mutations in normal elderly individuals with clonal hematopoiesis. Nat. Genet. 44 (2012), 1179–1181.
5. Cairns, R.A., Mak, T.W., Oncogenic isocitrate dehydrogenase mutations: mechanisms, models, and clinical opportunities. Cancer Discov. 3 (2013), 730–741.
6. Cancer Genome Atlas Research Network, Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N. Engl. J. Med. 368 (2013), 2059–2074.
7. Cellot, S., Hope, K.J., Chagraoui, J., Sauvageau, M., Deneault, E., MacRae, T., Mayotte, N., Wilhelm, B.T., Landry, J.R., Ting, S.B., et al. RNAi screen identifies Jarid1b as a major regulator of mouse HSC activity. Blood 122 (2013), 1545–1555.
8. Chen, C., Liu, Y., Lu, C., Cross, J.R., Morris, J.P., Shroff, A.S., Ward, P.S., Bradner, J.E., Thompson, C., Lowe, S.W., Cancer-associated IDH2 mutants drive an acute myeloid leukemia that is susceptible to Brd4 inhibition. Genes Dev. 27 (2013), 1974–1985.
9. Chen, Y., Yang, R., Guo, P., Ju, Z., Gadd45a deletion aggravates hematopoietic stem cell dysfunction in ATM-deficient mice. Protein Cell 5 (2014), 80–89.
10. Chowdhury, R., Yeoh, K.K., Tian, Y.M., Hillringhaus, L., Bagg, E.A., Rose, N.R., Leung, I.K., Li, X.S., Woon, E.C., Yang, M., et al. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep. 12 (2011), 463–469.
11. Cimmino, L., Dawlaty, M.M., Ndiaye-Lobry, D., Yap, Y.S., Bakogianni, S., Yu, Y., Bhattacharyya, S., Shaknovich, R., Geng, H., Lobry, C., et al. TET1 is a tumor suppressor of hematopoietic malignancy. Nat. Immunol. 16 (2015), 653–662.
12. Corces-Zimmerman, M.R., Hong, W.J., Weissman, I.L., Medeiros, B.C., Majeti, R., Preleukemic mutations in human acute myeloid leukemia affect epigenetic regulators and persist in remission. Proc. Natl. Acad. Sci. USA 111 (2014), 2548–2553.
13. Figueroa, M.E., Abdel-Wahab, O., Lu, C., Ward, P.S., Patel, J., Shih, A., Li, Y., Bhagwat, N., Vasanthakumar, A., Fernandez, H.F., et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 18 (2010), 553–567.
14. Garaycoechea, J.I., Crossan, G.P., Langevin, F., Daly, M., Arends, M.J., Patel, K.J., Genotoxic consequences of endogenous aldehydes on mouse haematopoietic stem cell function. Nature 489 (2012), 571–575.
15. Grove, C.S., Vassiliou, G.S., Acute myeloid leukaemia: a paradigm for the clonal evolution of cancer?. Dis. Model Mech. 7 (2014), 941–951.
16. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674.
17. Hirata, M., Sasaki, M., Cairns, R.A., Inoue, S., Puviindran, V., Li, W.Y., Snow, B.E., Jones, L.D., Wei, Q., Sato, S., et al. Mutant IDH is sufficient to initiate enchondromatosis in mice. Proc. Natl. Acad. Sci. USA 112 (2015), 2829–2834.
18. Im, A.P., Sehgal, A.R., Carroll, M.P., Smith, B.D., Tefferi, A., Johnson, D.E., Boyiadzis, M., DNMT3A and IDH mutations in acute myeloid leukemia and other myeloid malignancies: associations with prognosis and potential treatment strategies. Leukemia 28 (2014), 1774–1783.
19. Inoue, S., Hao, Z., Elia, A.J., Cescon, D., Zhou, L., Silvester, J., Snow, B., Harris, I.S., Sasaki, M., Li, W.Y., et al. Mule/Huwe1/Arf-BP1 suppresses Ras-driven tumorigenesis by preventing c-Myc/Miz1-mediated down-regulation of p21 and p15. Genes Dev. 27 (2013), 1101–1114.
20. Ito, K., Hirao, A., Arai, F., Matsuoka, S., Takubo, K., Hamaguchi, I., Nomiyama, K., Hosokawa, K., Sakurada, K., Nakagata, N., et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431 (2004), 997–1002.
21. Ito, K., Takubo, K., Arai, F., Satoh, H., Matsuoka, S., Ohmura, M., Naka, K., Azuma, M., Miyamoto, K., Hosokawa, K., et al. Regulation of reactive oxygen species by Atm is essential for proper response to DNA double-strand breaks in lymphocytes. J. Immunol. 178 (2007), 103–110.
22. Jan, M., Snyder, T.M., Corces-Zimmerman, M.R., Vyas, P., Weissman, I.L., Quake, S.R., Majeti, R., Clonal evolution of preleukemic hematopoietic stem cells precedes human acute myeloid leukemia. Sci. Transl. Med., 4, 2012, 149ra118.
23. Karnitz, L.M., Flatten, K.S., Wagner, J.M., Loegering, D., Hackbarth, J.S., Arlander, S.J., Vroman, B.T., Thomas, M.B., Baek, Y.U., Hopkins, K.M., et al. Gemcitabine-induced activation of checkpoint signaling pathways that affect tumor cell survival. Mol. Pharmacol. 68 (2005), 1636–1644.
24. Ko, M., Bandukwala, H.S., An, J., Lamperti, E.D., Thompson, E.C., Hastie, R., Tsangaratou, A., Rajewsky, K., Koralov, S.B., Rao, A., Ten-Eleven-Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proc. Natl. Acad. Sci. USA 108 (2011), 14566–14571.
25. Kunimoto, H., Fukuchi, Y., Sakurai, M., Sadahira, K., Ikeda, Y., Okamoto, S., Nakajima, H., Tet2 disruption leads to enhanced self-renewal and altered differentiation of fetal liver hematopoietic stem cells. Sci. Rep., 2, 2012, 273.
26. Lehnertz, B., Pabst, C., Su, L., Miller, M., Liu, F., Yi, L., Zhang, R., Krosl, J., Yung, E., Kirschner, J., et al. The methyltransferase G9a regulates HoxA9-dependent transcription in AML. Genes Dev. 28 (2014), 317–327.
27. Lu, C., Ward, P.S., Kapoor, G.S., Rohle, D., Turcan, S., Abdel-Wahab, O., Edwards, C.R., Khanin, R., Figueroa, M.E., Melnick, A., et al. IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 483 (2012), 474–478.
28. Mohrin, M., Bourke, E., Alexander, D., Warr, M.R., Barry-Holson, K., Le Beau, M.M., Morrison, C.G., Passegue, E., Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell 7 (2010), 174–185.
29. Moran-Crusio, K., Reavie, L., Shih, A., Abdel-Wahab, O., Ndiaye-Lobry, D., Lobry, C., Figueroa, M.E., Vasanthakumar, A., Patel, J., Zhao, X., et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 20 (2011), 11–24.
30. Niedernhofer, L.J., DNA repair is crucial for maintaining hematopoietic stem cell function. DNA Repair 7 (2008), 523–529.
31. Nijnik, A., Woodbine, L., Marchetti, C., Dawson, S., Lambe, T., Liu, C., Rodrigues, N.P., Crockford, T.L., Cabuy, E., Vindigni, A., et al. DNA repair is limiting for haematopoietic stem cells during ageing. Nature 447 (2007), 686–690.
32. Nitta, E., Yamashita, M., Hosokawa, K., Xian, M., Takubo, K., Arai, F., Nakada, S., Suda, T., Telomerase reverse transcriptase protects ATM-deficient hematopoietic stem cells from ROS-induced apoptosis through a telomere-independent mechanism. Blood 117 (2011), 4169–4180.
33. Patel, J.P., Gonen, M., Figueroa, M.E., Fernandez, H., Sun, Z., Racevskis, J., Van Vlierberghe, P., Dolgalev, I., Thomas, S., Aminova, O., et al. Prognostic relevance of integrated genetic profiling in acute myeloid leukemia. N. Engl. J. Med. 366 (2012), 1079–1089.
34. Peng, G., Chun-Jen Lin, C., Mo, W., Dai, H., Park, Y.Y., Kim, S.M., Peng, Y., Mo, Q., Siwko, S., Hu, R., et al. Genome-wide transcriptome profiling of homologous recombination DNA repair. Nat. Commun., 5, 2014, 3361.
35. Quivoron, C., Couronne, L., Della Valle, V., Lopez, C.K., Plo, I., Wagner-Ballon, O., Do Cruzeiro, M., Delhommeau, F., Arnulf, B., Stern, M.H., 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.
36. Rossi, D.J., Bryder, D., Seita, J., Nussenzweig, A., Hoeijmakers, J., Weissman, I.L., Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447 (2007), 725–729.
37. Santos, M.A., Faryabi, R.B., Ergen, A.V., Day, A.M., Malhowski, A., Canela, A., Onozawa, M., Lee, J.E., Callen, E., Gutierrez-Martinez, P., et al. DNA-damage-induced differentiation of leukaemic cells as an anti-cancer barrier. Nature 514 (2014), 107–111.
38. Sasaki, M., Knobbe, C.B., Itsumi, M., Elia, A.J., Harris, I.S., Chio, I.I., Cairns, R.A., McCracken, S., Wakeham, A., Haight, J., et al. D-2-hydroxyglutarate produced by mutant IDH1 perturbs collagen maturation and basement membrane function. Genes Dev. 26 (2012), 2038–2049.
39. Sasaki, M., Knobbe, C.B., Munger, J.C., Lind, E.F., Brenner, D., Brustle, A., Harris, I.S., Holmes, R., Wakeham, A., Haight, J., et al. IDH1(R132H) mutation increases murine haematopoietic progenitors and alters epigenetics. Nature 488 (2012), 656–659.
40. Shih, A.H., Abdel-Wahab, O., Patel, J.P., Levine, R.L., The role of mutations in epigenetic regulators in myeloid malignancies. Nat. Rev. Cancer 12 (2012), 599–612.
41. Shlush, L.I., Zandi, S., Mitchell, A., Chen, W.C., Brandwein, J.M., Gupta, V., Kennedy, J.A., Schimmer, A.D., Schuh, A.C., Yee, K.W., et al. Identification of pre-leukaemic haematopoietic stem cells in acute leukaemia. Nature 506 (2014), 328–333.
42. Spring, K., Ahangari, F., Scott, S.P., Waring, P., Purdie, D.M., Chen, P.C., Hourigan, K., Ramsay, J., McKinnon, P.J., Swift, M., Lavin, M.F., Mice heterozygous for mutation in Atm, the gene involved in ataxia-telangiectasia, have heightened susceptibility to cancer. Nat. Genet. 32 (2002), 185–190.
43. Stracker, T.H., Roig, I., Knobel, P.A., Marjanovic, M., The ATM signaling network in development and disease. Front. Genet., 4, 2013, 37.
44. Taiwo, O., Wilson, G.A., Morris, T., Seisenberger, S., Reik, W., Pearce, D., Beck, S., Butcher, L.M., Methylome analysis using MeDIP-seq with low DNA concentrations. Nat. Protoc. 7 (2012), 617–636.
45. Takagi, M., Sato, M., Piao, J., Miyamoto, S., Isoda, T., Kitagawa, M., Honda, H., Mizutani, S., ATM-dependent DNA damage-response pathway as a determinant in chronic myelogenous leukemia. DNA Repair 12 (2013), 500–507.
46. Welch, J.S., Ley, T.J., Link, D.C., Miller, C.A., Larson, D.E., Koboldt, D.C., Wartman, L.D., Lamprecht, T.L., Liu, F., Xia, J., et al. The origin and evolution of mutations in acute myeloid leukemia. Cell 150 (2012), 264–278.
47. Xie, M., Lu, C., Wang, J., McLellan, M.D., Johnson, K.J., Wendl, M.C., McMichael, J.F., Schmidt, H.K., Yellapantula, V., Miller, C.A., et al. Age-related mutations associated with clonal hematopoietic expansion and malignancies. Nat. Med. 20 (2014), 1472–1478.
48. Zhan, H., Suzuki, T., Aizawa, K., Miyagawa, K., Nagai, R., Ataxia telangiectasia mutated (ATM)-mediated DNA damage response in oxidative stress-induced vascular endothelial cell senescence. J. Biol. Chem. 285 (2010), 29662–29670.
49. Zhao, Z., Chen, L., Dawlaty, M.M., Pan, F., Weeks, O., Zhou, Y., Cao, Z., Shi, H., Wang, J., Lin, L., et al. Combined loss of Tet1 and Tet2 promotes B cell, but not myeloid malignancies, in mice. Cell Rep. 13 (2015), 1692–1704.