Acute myeloid leukaemia: A paradigm for the clonal evolution of cancer?

DMM Disease Models and Mechanisms

Volumn 7, Issue 8, 2014, Pages 941-951

  Grove, Carolyn S ^a   Vassiliou, George S ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Acute myeloid leukaemia; Cancer; Clonal evolution; In vivo models of leukaemia; Mutation

Indexed keywords

ANIMAL; CANCER STEM CELL; CLONAL EVOLUTION; GENETIC ASSOCIATION STUDY; GENETICS; HUMAN; HUMAN GENOME; LEUKEMIA, MYELOID, ACUTE; MUTATION; PATHOLOGY;

ANIMALS; CLONAL EVOLUTION; GENETIC ASSOCIATION STUDIES; GENOME, HUMAN; HUMANS; LEUKEMIA, MYELOID, ACUTE; MUTATION; NEOPLASTIC STEM CELLS;

EID: 84905826038     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.015974     Document Type: Review

References (92)

1. AIHW (2013). Cancer survival and prevalence in Australia: period estimates from 1982 to 2010. Asia Pac. J. Clin. Oncol. 9, 29-39.
2. Aktipis, C. A. and Nesse, R. M. (2013). Evolutionary foundations for cancer biology. Evol. Appl. 6, 144-159.
3. Alexandrov, L. B., Nik-Zainal, S., Wedge, D. C., Aparicio, S. A. J. R., Behjati, S., Biankin, A. V., Bignell, G. R., Bolli, N., Borg, A., Børresen-Dale, A.-L. et al.; Australian Pancreatic Cancer Genome Initiative; ICGC Breast Cancer Consortium; ICGC MMML-Seq Consortium; ICGC PedBrain (2013). Signatures of mutational processes in human cancer. Nature 500, 415-421.
4. Anderson, K., Lutz, C., van Delft, F. W., Bateman, C. M., Guo, Y., Colman, S. M., Kempski, H., Moorman, A. V., Titley, I., Swansbury, J. et al. (2011). Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 469, 356-361.
5. Arai, F., Hirao, A., Ohmura, M., Sato, H., Matsuoka, S., Takubo, K., Ito, K., Koh, G. Y. and Suda, T. (2004). Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118, 149-161. (Pubitemid 38962572)
6. Beekman, R., Valkhof, M. G., Sanders, M. A., van Strien, P. M. H., Haanstra, J. R., Broeders, L., Geertsma-Kleinekoort, W. M., Veerman, A. J. P., Valk, P. J. M., Verhaak, R. G. et al. (2012). Sequential gain of mutations in severe congenital neutropenia progressing to acute myeloid leukemia. Blood 119, 5071-5077.
7. Beerman, I., Maloney, W. J., Weissmann, I. L. and Rossi, D. J. (2010). Stem cells and the aging hematopoietic system. Curr. Opin. Immunol . 22, 500-506.
8. Ben-Batalla, I., Schultze, A., Wroblewski, M., Erdmann, R., Heuser, M., Waizenegger, J. S., Riecken, K., Binder, M., Schewe, D., Sawall, S. et al. (2013). Axl, a prognostic and therapeutic target in acute myeloid leukemia mediates paracrine crosstalk of leukemia cells with bone marrow stroma. Blood 122, 2443-2452.
9. Bhayat, F., Das-Gupta, E., Smith, C., McKeever, T. and Hubbard, R. (2009). The incidence of and mortality from leukaemias in the UK: a general population-based study. BMC Cancer 9, 252.
10. Busque, L., Patel, J. P., Figueroa, M. E., Vasanthakumar, A., Provost, S., Hamilou, Z., Mollica, L., Li, J., Viale, A., Heguy, A. et al. (2012). Recurrent somatic TET2 mutations in normal elderly individuals with clonal hematopoiesis. Nat. Genet. 44, 1179-1181.
11. Campbell, P. J., Pleasance, E. D., Stephens, P. J., Dicks, E., Rance, R., Goodhead, I., Follows, G. A., Green, A. R., Futreal, P. A. and Stratton, M. R. (2008). Subclonal phylogenetic structures in cancer revealed by ultra-deep sequencing. Proc. Natl. Acad. Sci. USA 105, 13081-13086.
12. Campbell, P. J., Yachida, S., Mudie, L. J., Stephens, P. J., Pleasance, E. D., Stebbings, L. A., Morsberger, L. A., Latimer, C., McLaren, S., Lin, M.-L. et al. (2010). The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 467, 1109-1113.
13. Casas, S., Aventín, A., Fuentes, F., Vallespí, T., Granada, I., Carrió, A., Angel Martínez-Climent, J., Solé, F., Teixidó, M., Bernués, M. et al. (2004). Genetic diagnosis by comparative genomic hybridization in adult de novo acute myelocytic leukemia. Cancer Genet. Cytogenet. 153, 16-25. (Pubitemid 39592124)
14. Catlin, S. N., Busque, L., Gale, R. E., Guttorp, P. and Abkowitz, J. L. (2011). The replication rate of human hematopoietic stem cells in vivo. Blood 117, 4460-4466.
15. Challen, G. A., Sun, D., Jeong, M., Luo, M., Jelinek, J., Berg, J. S., Bock, C., Vasanthakumar, A., Gu, H., Xi, Y. et al. (2012). Dnmt3a is essential for hematopoietic stem cell differentiation. Nat. Genet. 44, 23-31.
16. Chen, C.-L., Rappailles, A., Duquenne, L., Huvet, M., Guilbaud, G., Farinelli, L., Audit, B., d'Aubenton-Carafa, Y., Arneodo, A., Hyrien, O. et al. (2010). Impact of replication timing on non-CpG and CpG substitution rates in mammalian genomes. Genome Res. 20, 447-457.
17. Cozzio, A., Passegué, E., Ayton, P. M., Karsunky, H., Cleary, M. L. and Weissman, I. L. (2003). Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 17, 3029-3035. (Pubitemid 38040767)
18. Craddock, C., Tauro, S., Moss, P. and Grimwade, D. (2005). Biology and management of relapsed acute myeloid leukaemia. Br. J. Haematol. 129, 18-34. (Pubitemid 40524048)
19. Delhommeau, F., Dupont, S., Della Valle, V., James, C., Trannoy, S., Massé, A., Kosmider, O., Le Couedic, J.-P., Robert, F., Alberdi, A. et al. (2009). Mutation in TET2 in myeloid cancers. N. Engl. J. Med. 360, 2289-2301.
20. Ding, L., Ley, T. J., Larson, D. E., Miller, C. A., Koboldt, D. C., Welch, J. S., Ritchey, J. K., Young, M. A., Lamprecht, T., McLellan, M. D. et al. (2012). Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 481, 506-510.
21. Diwan, B. A., Rice, J. M., Ohshima, M. and Ward, J. M. (1986). Interstrain differences in susceptibility to liver carcinogenesis initiated by N-nitrosodiethylamine and its promotion by phenobarbital in C57BL/6NCr, C3H/HeNCrMTV- and DBA/2NCr mice. Carcinogenesis 7, 215-220. (Pubitemid 17130535)
22. Dores, G. M., Devesa, S. S., Curtis, R. E., Linet, M. S. and Morton, L. M. (2012). Acute leukemia incidence and patient survival among children and adults in the United States, 2001-2007. Blood 119, 34-43.
23. Ford, A. M., Ridge, S. A., Cabrera, M. E., Mahmoud, H., Steel, C. M., Chan, L. C. and Greaves, M. (1993). In utero rearrangements in the trithorax-related oncogene in infant leukaemias. Nature 363, 358-360. (Pubitemid 23161533)
24. Forsberg, L. A., Rasi, C., Razzaghian, H. R., Pakalapati, G., Waite, L., Thilbeault, K. S., Ronowicz, A., Wineinger, N. E., Tiwari, H. K., Boomsma, D. et al. (2012). Age-related somatic structural changes in the nuclear genome of human blood cells. Am. J. Hum. Genet. 90, 217-228.
25. Gatenby, R. A., Silva, A. S., Gillies, R. J. and Frieden, B. R. (2009). Adaptive therapy. Cancer Res. 69, 4894-4903.
26. Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P. et al. (2012). Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883-892.
27. Gilliland, D. G. and Griffin, J. D. (2002). The roles of FLT3 in hematopoiesis and leukemia. Blood 100, 1532-1542.
28. Goldie J. H. and Coldman A. J. (1984). The genetic origin of drug resistance in neoplasms: implications for systemic therapy. Cancer Res. 44, 3643-3653. (Pubitemid 14041569)
29. Greaves, M. and Maley, C. C. (2012). Clonal evolution in cancer. Nature 481, 306-313.
30. Hanahan, D. and Weinberg, R. A. (2000). The hallmarks of cancer. Cell 100, 57-70. (Pubitemid 30046295)
31. Huntly, B. J. P., Shigematsu, H., Deguchi, K., Lee, B. H., Mizuno, S., Duclos, N., Rowan, R., Amaral, S., Curley, D., Williams, I. R. et al. (2004). MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell 6, 587-596
32. Itzhar, N., Dessen, P., Toujani, S., Auger, N., Preudhomme, C., Richon, C., Lazar, V., Saada, V., Bennaceur, A., Bourhis, J. H. et al. (2011). Chromosomal minimal critical regions in therapy-related leukemia appear different from those of de novo leukemia by high-resolution aCGH. PLoS ONE 6, e16623.
33. Itzykson, R., Kosmider, O., Renneville, A., Morabito, M., Preudhomme, C., Berthon, C., Adès, L., Fenaux, P., Platzbecker, U., Gagey, O. et al. (2013). Clonal architecture of chronic myelomonocytic leukemias. Blood 121, 2186-2198.
34. Jacobs, K. B., Yeager, M., Zhou, W., Wacholder, S., Wang, Z., Rodriguez-Santiago, B., Hutchinson, A., Deng, X., Liu, C., Horner, M.-J. et al. (2012). Detectable clonal mosaicism and its relationship to aging and cancer. Nat. Genet. 44, 651-658.
35. Jan, M., Snyder, T. M., Corces-Zimmerman, M. R., Vyas, P., Weissman, I. L., Quake, S. R. and Majeti, R. (2012). Clonal evolution of preleukemic hematopoietic stem cells precedes human acute myeloid leukemia. Sci. Transl. Med. 4, 149ra118.
36. Jones, A. V., Chase, A., Silver, R. T., Oscier, D., Zoi, K., Wang, Y. L., Cario, H., Pahl, H. L., Collins, A., Reiter, A. et al. (2009). JAK2 haplotype is a major risk factor for the development of myeloproliferative neoplasms. Nat. Genet. 41, 446-449.
37. Kelly, L. M., Kutok, J. L., Williams, I. R., Boulton, C. L., Amaral, S. M., Curley, D. P., Ley, T. J. and Gilliland, D. G. (2002). PML/RARalpha and FLT3-ITD induce an APL-like disease in a mouse model. Proc. Natl. Acad. Sci. USA 99, 8283-8288. (Pubitemid 34651044)
38. Kim, S.-H., Elango, N., Warden, C., Vigoda, E. and Yi, S. V. (2006). Heterogeneous genomic molecular clocks in primates. PLoS Genet. 2, e163.
39. Kreso, A., O'Brien, C. A., van Galen, P., Gan, O. I., Notta, F., Brown, A. M. K., Ng, K., Ma, J., Wienholds, E., Dunant, C. et al. (2013). Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer. Science 339, 543-548.
40. Krönke, J., Bullinger, L., Teleanu, V., Tschürtz, F., Gaidzik, V. I., Kühn, M. W. M., Rücker, F. G., Holzmann, K., Paschka, P., Kapp-Schwörer, S. et al. (2013). Clonal evolution in relapsed NPM1-mutated acute myeloid leukemia. Blood 122, 100-108.
41. Kusec, R., Laczika, K., Knöbl, P., Friedl, J., Greinix, H., Kahls, P., Linkesch, W., Schwarzinger, I., Mitterbauer, G., Purtscher, B. et al. (1994). AML1/ETO fusion mRNA can be detected in remission blood samples of all patients with t(8;21) acute myeloid leukemia after chemotherapy or autologous bone marrow transplantation. Leukemia 8, 735-739. (Pubitemid 24161076)
42. Lapidot, T., Sirard, C., Vormoor, J., Murdoch, B., Hoang, T., Caceres-Cortes, J., Minden, M., Paterson, B., Caligiuri, M. A. and Dick, J. E. (1994). A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645-648. (Pubitemid 24067706)
43. Laurie, C. C., Laurie, C. A., Rice, K., Doheny, K. F., Zelnick, L. R., McHugh, C. P., Ling, H., Hetrick, K. N., Pugh, E. W., Amos, C. et al. (2012). Detectable clonal mosaicism from birth to old age and its relationship to cancer. Nat. Genet. 44, 642-650.
44. Lawrence, M. S., Stojanov, P., Polak, P., Kryukov, G. V., Cibulskis, K., Sivachenko, A., Carter, S. L., Stewart, C., Mermel, C. H., Roberts, S. A. et al. (2013). Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499, 214-218.
45. Li, L. and Clevers, H. (2010). Coexistence of quiescent and active adult stem cells in mammals. Science 327, 542-545.
46. Lynch, M. (2010). Rate, molecular spectrum, and consequences of human mutation. Proc. Natl. Acad. Sci. USA 107, 961-968.
47. McFarland, C. D., Korolev, K. S., Kryukov, G. V., Sunyaev, S. R. and Mirny, L. A. (2013). Impact of deleterious passenger mutations on cancer progression. Proc. Natl. Acad. Sci. 110, 2910-2915.
48. Miyamoto, T., Nagafuji, K., Akashi, K., Harada, M., Kyo, T., Akashi, T., Takenaka, K., Mizuno, S., Gondo, H., Okamura, T. et al. (1996). Persistence of multipotent progenitors expressing AML1/ETO transcripts in long-term remission patients with t(8;21) acute myelogenous leukemia. Blood 87, 4789-4796. (Pubitemid 26162380)
49. 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. (2011). Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 20, 11-24.
50. Mori, H., Colman, S. M., Xiao, Z., Ford, A. M., Healy, L. E., Donaldson, C., Hows, J. M., Navarrete, C. and Greaves, M. (2002). Chromosome translocations and covert leukemic clones are generated during normal fetal development. Proc. Natl. Acad. Sci. USA 99, 8242-8247. (Pubitemid 34651037)
51. Mullighan, C. G., Phillips, L. A., Su, X., Ma, J., Miller, C. B., Shurtleff, S. A. and Downing, J. R. (2008). Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 322, 1377-1380. (Pubitemid 352775249)
52. Mupo, A., Celani, L., Dovey, O., Cooper, J. L., Grove, C., Rad, R., Sportoletti, P., Falini, B., Bradley, A. and Vassiliou, G. S. (2013). A powerful molecular synergy between mutant Nucleophosmin and Flt3-ITD drives acute myeloid leukemia in mice. Leukemia 27, 1917-1920.
53. Nik-Zainal, S., Alexandrov, L. B., Wedge, D. C., Van Loo, P., Greenman, C. D., Raine, K., Jones, D., Hinton, J., Marshall, J., Stebbings, L. A. et al.; Breast Cancer Working Group of the International Cancer Genome Consortium (2012a). Mutational processes molding the genomes of 21 breast cancers. Cell 149, 979-993.
54. Nik-Zainal, S., Van Loo, P., Wedge, D. C., Alexandrov, L. B., Greenman, C. D., Lau, K. W., Raine, K., Jones, D., Marshall, J., Ramakrishna, M. et al.; Breast Cancer Working Group of the International Cancer Genome Consortium (2012b). The life history of 21 breast cancers. Cell 149, 994-1007.
55. Notta, F., Mullighan, C. G., Wang, J. C. Y., Poeppl, A., Doulatov, S., Phillips, L. A., Ma, J., Minden, M. D., Downing, J. R. and Dick, J. E. (2011). Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature 469, 362-367.
56. Nowell, P. C. (1976). The clonal evolution of tumor cell populations. Science 194, 23-28.
57. Olcaydu, D., Harutyunyan, A., Jäger, R., Berg, T., Gisslinger, B., Pabinger, I., Gisslinger, H. and Kralovics, R. (2009). A common JAK2 haplotype confers susceptibility to myeloproliferative neoplasms. Nat. Genet. 41, 450-454.
58. Østgård, L. S. G., Kjeldsen, E., Holm, M. S., Brown, P. N., Pedersen, B. B., Bendix, K., Johansen, P., Kristensen, J. S. and Nørgaard, J. M. (2010). Reasons for treating secondary AML as de novo AML. Eur. J. Haematol. 85, 217-226.
59. Owen, C. J., Toze, C. L., Koochin, A., Forrest, D. L., Smith, C. A., Stevens, J. M., Jackson, S. C., Poon, M.-C., Sinclair, G. D., Leber, B. et al. (2008). Five new pedigrees with inherited RUNX1 mutations causing familial platelet disorder with propensity to myeloid malignancy. Blood 112, 4639-4645.
60. Parkin, B., Ouillette, P., Li, Y., Keller, J., Lam, C., Roulston, D., Li, C., Shedden, K. and Malek, S. N. (2013). Clonal evolution and devolution after chemotherapy in adult acute myelogenous leukemia. Blood 121, 369-377.
61. Pina, C. and Enver, T. (2007). Differential contributions of haematopoietic stem cells to foetal and adult haematopoiesis: insights from functional analysis of transcriptional regulators. Oncogene 26, 6750-6765. (Pubitemid 47585100)
62. Pleasance, E. D., Stephens, P. J., O'Meara, S., McBride, D. J., Meynert, A., Jones, D., Lin, M.-L., Beare, D., Lau, K. W., Greenman, C. et al. (2010). A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 463, 184-190.
63. Potter, M. and Wiener, F. (1992). Plasmacytomagenesis in mice: model of neoplastic development dependent upon chromosomal translocations. Carcinogenesis 13, 1681-1697.
64. Prchal, J. T., Prchal, J. F., Belickova, M., Chen, S., Guan, Y., Gartland, G. L. and Cooper, M. D. (1996). Clonal stability of blood cell lineages indicated by X-chromosomal transcriptional polymorphism. J. Exp. Med. 183, 561-567. (Pubitemid 26059519)
65. Quivoron, C., Couronné, L., Della Valle, V., Lopez, C. K., Plo, I., Wagner-Ballon, O., Do Cruzeiro, M., Delhommeau, F., Arnulf, B., Stern, M.-H. et al. (2011). TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 20, 25-38.
66. Rhoades, K. L., Hetherington, C. J., Harakawa, N., Yergeau, D. A., Zhou, L., Liu, L.-Q., Little, M.-T., Tenen, D. G. and Zhang, D.-E. (2000). Analysis of the role of AML1-ETO in leukemogenesis, using an inducible transgenic mouse model. Blood 96, 2108-2115.
67. Datta, R. S., Gutteridge, A., Swanton, C., Maley, C. C. and Graham, T. A. (2013). Modelling the evolution of genetic instability during tumour progression. Evol. Appl. 6, 20-33.
68. Schick, U. M., McDavid, A., Crane, P. K., Weston, N., Ehrlich, K., Newton, K. M., Wallace, R., Bookman, E., Harrison, T., Aragaki, A. et al. (2013). Confirmation of the reported association of clonal chromosomal mosaicism with an increased risk of incident hematologic cancer. PLoS ONE 8, e59823.
69. Schlenk, R. F. and Döhner, H. (2013). Genomic applications in the clinic: use in treatment paradigm of acute myeloid leukemia. Hematology Am. Soc. Hematol. Educ. Program 2013, 324-330.
70. Schuster-Böckler, B. and Lehner, B. (2012). Chromatin organization is a major influence on regional mutation rates in human cancer cells. Nature 488, 504-507.
71. Shah, A., Andersson, T. M. L., Rachet, B., Björkholm, M. and Lambert, P. C. (2013). Survival and cure of acute myeloid leukaemia in England, 1971-2006: a population-based study. Br. J. Haematol. 162, 509-516.
72. 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.; HALT Pan-Leukemia Gene Panel Consortium (2014). Identification of pre-leukaemic haematopoietic stem cells in acute leukaemia. Nature 506, 328-333.
73. Skaggs, B. J., Gorre, M. E., Ryvkin, A., Burgess, M. R., Xie, Y., Han, Y., Komisopoulou, E., Brown, L. M., Loo, J. A., Landaw, E. M. et al. (2006). Phosphorylation of the ATP-binding loop directs oncogenicity of drug-resistant BCRABL mutants. Proc. Natl. Acad. Sci. USA 103, 19466-19471. (Pubitemid 46026054)
74. Sprouffske, K., Athena Aktipis, C., Radich, J. P., Carroll, M., Nedelcu, A. M. and Maley, C. C. (2013). An evolutionary explanation for the presence of cancer nonstem cells in neoplasms. Evol. Appl. 6, 92-101.
75. Stephens, P. J., Greenman, C. D., Fu, B., Yang, F., Bignell, G. R., Mudie, L. J., Pleasance, E. D., Lau, K. W., Beare, D., Stebbings, L. A. et al. (2011). Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144, 27-40.
76. Stratton, M. R., Campbell, P. J. and Futreal, P. A. (2009). The cancer genome. Nature 458, 719-724.
77. Swierczek, S. I., Agarwal, N., Nussenzveig, R. H., Rothstein, G., Wilson, A., Artz, A. and Prchal, J. T. (2008). Hematopoiesis is not clonal in healthy elderly women. Blood 112, 3186-3193.
78. Tanaka, M., Yujiri, T., Ito, S., Okayama, N., Takahashi, T., Shinohara, K., Azuno, Y., Nawata, R., Hinoda, Y. and Tanizawa, Y. (2013). JAK2 46/1 haplotype is associated with JAK2 V617F-positive myeloproliferative neoplasms in Japanese patients. Int. J. Hematol. 97, 409-413.
79. The Cancer Genome Atlas Research Network (2013). Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N. Engl. J. Med. 368, 2059-2074.
80. Tutt, A., Robson, M., Garber, J. E., Domchek, S. M., Audeh, M. W., Weitzel, J. N., Friedlander, M., Arun, B., Loman, N., Schmutzler, R. K. et al. (2010). Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet 376, 235-244.
81. Vassiliou, G. S., Cooper, J. L., Rad, R., Li, J., Rice, S., Uren, A., Rad, L., Ellis, P., Andrews, R., Banerjee, R. et al. (2011). Mutant nucleophosmin and cooperating pathways drive leukemia initiation and progression in mice. Nat. Genet. 43, 470-475.
82. Voisin, V., Barat, C., Hoang, T. and Rassart, E. (2006). Novel insights into the pathogenesis of the Graffi murine leukemia retrovirus. J. Virol. 80, 4026-4037.
83. Walter, M. J., Shen, D., Ding, L., Shao, J., Koboldt, D. C., Chen, K., Larson, D. E., McLellan, M. D., Dooling, D., Abbott, R. et al. (2012). Clonal architecture of secondary acute myeloid leukemia. N. Engl. J. Med. 366, 1090-1098.
84. Wang, J., Xu, Z., Liu, L., Gale, R. P., Cross, N. C. P., Jones, A. V., Qin, T., Ai, X., Xu, J., Zhang, T. et al. (2013). JAK2V617F allele burden, JAK2 46/1 haplotype and clinical features of Chinese with myeloproliferative neoplasms. Leukemia 27, 1763-1767.
85. Wartman, L. D., Larson, D. E., Xiang, Z., Ding, L., Chen, K., Lin, L., Cahan, P., Klco, J. M., Welch, J. S., Li, C. et al. (2011). Sequencing a mouse acute promyelocytic leukemia genome reveals genetic events relevant for disease progression. J. Clin. Invest. 121, 1445-1455.
86. Weaver, B. A. A., Silk, A. D., Montagna, C., Verdier-Pinard, P. and Cleveland, D. W. (2007). Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell 11, 25-36. (Pubitemid 46070223)
87. 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. (2012). The origin and evolution of mutations in acute myeloid leukemia. Cell 150, 264-278.
88. Whitman, S. P., Archer, K. J., Feng, L., Baldus, C., Becknell, B., Carlson, B. D., Carroll, A. J., Mrózek, K., Vardiman, J. W., George, S. L. et al. (2001). Absence of the wild-type allele predicts poor prognosis in adult de novo acute myeloid leukemia with normal cytogenetics and the internal tandem duplication of FLT3: a cancer and leukemia group B study. Cancer Res. 61, 7233-7239. (Pubitemid 32946520)
89. Wiemels, J. L., Ford, A. M., Van Wering, E. R., Postma, A. and Greaves, M. (1999). Protracted and variable latency of acute lymphoblastic leukemia after tel-aml1 gene fusion in utero. Blood 94, 1057-1062. (Pubitemid 29361838)
90. Wiemels, J. L., Xiao, Z., Buffler, P. A., Maia, A. T., Ma, X., Dicks, B. M., Smith, M. T., Zhang, L., Feusner, J., Wiencke, J. et al. (2002). In utero origin of t(8;21) AML1-ETO translocations in childhood acute myeloid leukemia. Blood 99, 3801-3805. (Pubitemid 34534554)
91. Woo, Y. H. and Li, W.-H. (2012). DNA replication timing and selection shape the landscape of nucleotide variation in cancer genomes. Nat. Commun. 3, 1004.
92. Yamada, Y., Matsushiro, H., Ogawa, M. S., Okamoto, K., Nakakuki, Y., Toyokuni, S., Fukumoto, M. and Hiai, H. (1994). Genetic predisposition to pre-B lymphomas in SL/Kh strain mice. Cancer Res. 54, 403-407. (Pubitemid 24053177)