The impact of translocations and gene fusions on cancer causation

Nature Reviews Cancer

Volumn 7, Issue 4, 2007, Pages 233-245

  Mitelman, Felix ^a   Johansson, Bertil ^a   Mertens, Fredrik ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGENESIS; CARCINOGENIC ACTIVITY; CARCINOMA; CHILDHOOD CANCER; CHROMOSOME ABERRATION; CHROMOSOME ANALYSIS; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; CYTOGENETICS; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; GENE FUSION; HEMATOLOGIC DISEASE; HUMAN; MALIGNANT TRANSFORMATION; MOLECULAR MECHANICS; MORBIDITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SARCOMA; SOLID TUMOR;

CHROMOSOME ABERRATIONS; GENE FUSION; HUMANS; MODELS, GENETIC; NEOPLASMS; TERMINOLOGY; TRANSLOCATION, GENETIC;

EID: 33947581390     PISSN: 1474175X     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrc2091     Document Type: Review

References (144)

1. Boveri, T. Zur Frage der Entstehung maligner Tumoren. Gustav Fisher Verlag, Jena (1914).
2. Tjio, J. H. & Levan, A. The chromosome number of man. Hereditas 42, 1-6 (1956).
3. Nowell, P. C. & Hungerford, D. A. A minute chromosome in human chronic granulocytic leukemia. Science 132, 1497 (1960). The first description of a specific cancer-associated chromosome abnormality.
4. Caspersson, T., Zech, L. & Johansson, C. Differential binding of alkylating fluorochromes in human chromosomes. Exp. Cell. Res. 60, 315-319 (1970).
5. Vogelstein, B. & Kinzler, K. W. Cancer genes and the pathways they control. Nature Med. 10, 789-799 (2004).
6. Rowley, J. D. A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 243, 290-293 (1973). The first report of a specific translocation in a human malignancy.
7. Rabbitts, T. H. Chromosomal translocations in human cancer. Nature 372, 143-149 (1994).
8. Look, A. T. Oncogenic transcription factors in human acute leukemias. Science 278, 1059-1064 (1997).
9. Rowley, J. D. Chromosomal translocations: dangerous liaisons revisited. Nature Rev. Cancer 1, 245-250 (2001).
10. Mitelman, F., Johansson, B. & Mertens, F. Mitelman Database of Chromosome Aberrations in Cancer [online], http://cgap.nci.nih.gov/Chromosomes/ Mitelman (2006). A comprehensive resource of all published neoplasia-associated karyotypes and their corresponding gene fusions.
11. Kearney, L. & Horsley, S. W. Molecular cytogenetics in haematological malignancy: current technology and future prospects. Chromosoma 114, 286-294 (2005).
12. Pinkel, D. & Albertson, D. G. Array comparative genomic hybridization and its applications in cancer. Nature Genet. 37, S11-S17 (2005).
13. Speicher, M. R. & Carter, N. P. The new cytogenetics: blurring the boundaries with molecular biology. Nature Rev. Genet. 6, 782-792 (2005).
14. Futreal, P. A. et al. A census of human cancer genes. Nature Rev. Cancer 4, 177-183 (2004).
15. Sjöblom, T. et al. The consensus coding sequences of human breast and colorectal cancers. Science 314, 268-274 (2006). A recent large-scale study showing an unexpectedly large number of mutations in breast and colon cancer.
16. Mandahl, N. Cytogenetics and molecular genetics of bone and soft tissue tumors. Adv. Cancer Res. 69, 63-99 (1996).
17. Harrison, C. J. & Foroni, L. Cytogenetics and molecular genetics of acute lymphoblastic leukemia. Rev. Clin. Exp. Hematol. 6, 91-113 (2002).
18. Borden, E. C. et al. Soft tissue sarcomas of adults: state of the translational science. Clin. Cancer Res. 9, 1941-1956 (2003).
19. Johansson, B., Mertens, F. & Mitelman, F. Clinical and biological importance of cytogenetic abnormalities in childhood and adult acute lymphoblastic leukemia. Ann. Med. 36, 492-503 (2004).
20. Mrózek, K., Heerema, N. A. & Bloomfield, C. D. Cytogenetics in acute leukemia. Blood Rev. 18, 115-136 (2004).
21. Mitelman, F., Mertens, F. & Johansson B. Prevalence estimates of recurrent balanced cytogenetic aberrations and gene fusions in unselected patients with neoplastic disorders. Genes Chromosomes Cancer 43, 350-366 (2005).
22. Yeoh, E. J. et al. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell 1, 133-143 (2002).
23. Andersson, A. et al. Molecular signatures in childhood acute leukemia and their correlations to expression patterns in normal hematopoietic subpopulations. Proc. Natl Acad. Sci. USA 102, 19069-19074 (2005).
24. Davicioni, E. et al. Identification of a PAX-FKHR gene expression signature that defines molecular classes and determines the prognosis of alveolar rhabdomyosarcomas. Cancer Res. 66, 6936-6946 (2006).
25. Nowell, P. C. The clonal evolution of tumor cell populations. Science 194, 23-28 (1976).
26. Heim, S., Mandahl, N. & Mitelman, F. Genetic convergence and divergence in tumor progression. Cancer Res. 48, 5911-5916 (1988).
27. Johansson, B., Mertens, F. & Mitelman, F. Primary vs. secondary neoplasia-associated chromosomal abnormalities - balanced rearrangements vs. genomic imbalances? Genes Chromosomes Cancer 16, 155-163 (1996).
28. Nowell, P. C. Tumor progression: a brief historical perspective. Semin. Cancer Biol. 12, 261-266 (2002).
29. Hauschka, T. S. Cell population studies on mouse ascites tumors. Ann. NY Acad. Sci. 16, 64-73 (1953).
30. Levan, A. Chromosomal studies on some human tumors and tissues of normal origin, grown in vivo and in vitro at the Sloan-Kettering Institute. Cancer 9, 648-663 (1956).
31. Makino, S. Further evidence favoring the concept of the stem cell in ascites tumors of rats. Ann. NY Acad. Sci. 63, 818-830 (1956).
32. Heim, S. & Mitelman, F. Primary chromosome abnormalities in human neoplasia. Adv. Cancer Res. 52, 1-43 (1989).
33. Sinclair, P. B. et al. Large deletions at the t(9;22) breakpoint are common and may identify a poorprognosis subgroup of patients with chronic myeloid leukemia. Blood 95, 738-743 (2000).
34. Kolomietz, E. et al. Primary chromosomal rearrangements of leukemia are frequently accompanied by extensive submicroscopic deletions and may lead to altered prognosis. Blood 97, 3581-3588 (2001).
35. Aplan, P. D. Causes of oncogenic chromosomal translocation. Trends Genet. 22, 46-55 (2006). A recent review of mechanisms behind the origin of neoplasia-associated translocations and gene fusions.
36. Rego, E. M. & Pandolfi, P. P. Reciprocal products of chromosomal translocations in human cancer pathogenesis: key players or innocent bystanders? Trends Mol. Med. 8, 396-405 (2002).
37. Xia S. J. & Barr, F. G. Chromosome translocations in sarcomas and the emergence of oncogenic transcription factors. Eur. J. Cancer 41, 2513-2527 (2005).
38. Antonescu, C. R. The role of genetic testing in soft tissue sarcoma. Histopathology 48, 13-21 (2006).
39. Oehler, V. G. & Radich, J. P. Monitoring bcr-abl by polymerase chain reaction in the treatment of chronic myeloid leukemia. Curr. Oncol. Rep. 5, 426-435 (2003).
40. Avigad, S. et al. The predictive potential of molecular detection in the nonmetastatic Ewing family of tumors. Cancer 100, 1053-1058 (2004).
41. Deininger, M., Buchdunger, E. & Druker, B. J. The development of imatinib as a therapeutic agent for chronic myeloid leukemia. Blood 105, 2640-2653 (2005). Provides an up-to-date review of targeted therapy in BCR-ABL1-positive leukaemia.
42. Kern, W., Schoch, C., Haferlach, T. & Schnittger, S. Monitoring of minimal residual disease in acute myeloid leukemia. Crit. Rev. Oncol. Hematol. 56, 283-309 (2005).
43. Adams, J. M. et al. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318, 533-538 (1985).
44. Daley, G. Q., Van Etten, R. A. & Baltimore, D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science 247, 824-830 (1990).
45. Elefanty, A. G., Hariharan, I. K. & Cory, S. bcr-abl, the hallmark of chronic myeloid leukaemia in man, induces multiple haemopoietic neoplasms in mice. EMBO J. 9, 1069-1078 (1990).
46. Heisterkamp, N. et al. Acute leukaemia in bcr/abl transgenic mice. Nature 344, 251-253 (1990).
47. Kamps, M. P. & Baltimore, D. E2A-Pbx1, the t(1;19) translocation protein of human pre-B-cell acute lymphocytic leukemia, causes acute myeloid leukemia in mice. Mol. Cell Biol. 13, 351-357 (1993).
48. Corral, J. et al. An Mll-AF9 fusion gene made by homologous recombination causes acute leukemia in chimeric mice: a method to create fusion oncogenes. Cell 85, 853-861 (1996).
49. Pérez-Losada, J. et al. The chimeric FUS/TLS-CHOP fusion protein specifically induces liposarcomas in transgenic mice. Oncogene 19, 2413-2422 (2000).
50. Rego, E. M. et al. Leukemia with distinct phenotypes in transgenic mice expressing PML/RARα, PLZF/RAR α or NPM/RAR α. Oncogene 25, 1974-1979 (2006).
51. Rodriguez-Garcia, A. et al. Selective destruction of tumor cells through specific inhibition of products resulting from chromosomal translocations. Curr. Cancer Drug Targets 1, 109-119 (2001).
52. Thomas, M., Greil, J. & Heidenreich, O. Targeting leukemic fusion proteins with small interfering RNAs: recent advances and therapeutic potentials. Acta Pharmacol. Sin. 27, 273-281 (2006).
53. Küppers, R. Mechanisms of B-cell lymphoma pathogenesis. Nature Rev. Cancer 5, 251-262 (2005).
54. Sirvent, N., Maire, G. & Pedeutour, F. Genetics of dermatofibrosarcoma protuberans family of tumors: from ring chromosomes to tyrosine kinase inhibitor treatment. Genes Chromosomes Cancer 37, 1-19 (2003).
55. Kas, K. et al. Promoter swapping between the genes for a novel zinc finger protein and beta-catenin in pleiomorphic adenomas with t(3;8)(p21;q12) translocations. Nature Genet. 15, 170-174 (1997). First example of a translocation resulting in gene deregulation through promoter exchange in a solid tumour.
56. Dahlén, A. et al. Activation of the GLI oncogene through fusion with the β-actin gene (ACTB) in a group of distinctive pericytic neoplasms: pericytoma with t(7;12). Am. J. Pathol. 164, 1645-1653 (2004).
57. Oliveira, A. M. et al. Aneurysmal bone cyst variant translocations upregulate USP6 transcription by promoter swapping with the ZNF9, COL1A1, TRAP150, and OMD genes. Oncogene 24, 3419-3426 (2005).
58. West, R. B. et al. A landscape effect in tenosynovial giant-cell tumor from activation of CSF1 expression by a translocation in a minority of tumor cells. Proc. Natl Acad. Sci. USA 103, 690-695 (2006).
59. Popovici, C. et al. Reciprocal translocations in breast tumor cell lines: cloning of a t(3;20) that targets the FHIT gene. Genes Chromosomes Cancer 35, 204-218 (2002).
60. Belloni, E. et al. A new complex rearrangement involving the ETV6, LOC115548, and MN1 genes in a case of acute myeloid leukemia. Genes Chromosomes Cancer 41, 272-277 (2004).
61. Karenko, L. et al. Primary cutaneous T-cell lymphomas show a deletion or translocation affecting NAV3, the human UNC-53 homologue. Cancer Res. 65, 8101-8110 (2005).
62. Berger, R. et al. Loss of the NPM1 gene in myeloid disorders with chromosome 5 rearrangements. Leukemia 20, 319-321 (2006).
63. Panagopoulos, I. et al. Fusion of ETV6 with an intronic sequence of the BAZ2A gene in a paediatric pre-B acute lymphoblastic leukaemia with a cryptic chromosome 12 rearrangement. Br. J. Haematol. 133, 270-275 (2006).
64. Deininger, M. W. N., Goldman, J. M. & Melo, J. V. The molecular biology of chronic myeloid leukemia. Blood 96, 3343-3356 (2000).
65. Mitelman, F., Johansson, B. & Mertens, F. Fusion genes and rearranged genes as a linear function of chromosome aberrations in cancer. Nature Genet. 36, 331-334 (2004). An analysis of the impact of cytogenetic analyses on the detection of new gene fusions.
66. Lannon, C. L. & Sorensen, P. H. B. ETV6-NTRK3: a chimeric protein tyrosine kinase with transformation activity in multiple cell lineages. Semin. Cancer Biol. 15, 215-223 (2005). A review of the pathogenetic implications of a gene fusion involved in histogenetically distinct tumour types.
67. Meyer, C. et al. The MLL recombinome of acute leukemias. Leukemia 20, 777-784 (2006). A recent summary of partner genes involved in fusions with the MLL gene.
68. Bohlander, S. K. ETV6: a versatile player in leukemogenesis. Semin. Cancer Biol. 15, 162-174 (2005).
69. Janknecht, R. EWS-ETS oncoproteins: the linchpin of Ewing tumors. Gene 363, 1-14 (2005).
70. Höglund, M., Frigyesi, A. & Mitelman, F. A gene fusion network in human neoplasia. Oncogene 25, 2674-2678 (2006).
71. Barabási, A.-L. & Oltvai, Z. N. Network biology: understanding the cell's functional organization. Nature Rev. Genet. 5, 101-113 (2004).
72. Ladanyi, M. et al. The der(17)t(X;17)(p11;q25) of human alveolar soft part sarcoma fuses the TFE3 transcription factor gene to ASPL, a novel gene at 17q25. Oncogene 20, 48-57 (2001).
73. Graux, C. et al. Fusion of NUP214 to ABL1 on amplified episomes in T-cell acute lymphoblastic leukemia. Nature Genet. 36, 1084-1089 (2004).
74. Bernard, O. et al. Two site-specific deletions and t(1;14) translocation restricted to human T-cell acute leukemias disrupt the 5′ part of the tal-1 gene. Oncogene 6, 1477-1488 (1991).
75. Kourlas, P. J. et al. Identification of a gene at 11q23 encoding a guanine nucleotide exchange factor: evidence for its fusion with MLL in acute myeloid leukemia. Proc. Natl Acad. Sci. USA 97, 2145-2150 (2000).
76. Fu J.-F., Hsu J.-J., Tang T.-C. & Shih L.-Y. Identification of CBL, a proto-oncogene at 11q23. 3, as a novel MLL fusion partner in a patient with de novo acute myeloid leukemia. Genes Chromosomes Cancer 37, 214-219 (2003).
77. Meyer, C. et al. Diagnostic tool for the identification of MLL rearrangements including unknown partner genes. Proc. Natl Acad. Sci. USA 102, 449-454 (2005).
78. Pardanani, A. et al. CHIC2 deletion, a surrogate for FIP1L1-PDGFRA fusion, occurs in systemic mastocytosis associated with eosinophilia and predicts response to imatinib mesylate therapy. Blood 102, 3093-3096 (2003).
79. Hibbard, M. K. et al. PLAG1 fusion oncogenes in lipoblastoma. Cancer Res. 60, 4869-4872 (2000).
80. Charest, A. et al. Fusion of FIG to the receptor tyrosine kinase ROS in a glioblastoma with an interstitial del(6)(q21q21). Genes Chromosomes Cancer 37, 58-71 (2003).
81. Perner, S. et al. TMPRSS2:ERG fusion-associated deletions provide insight into the heterogeneity of prostate cancer. Cancer Res. 66, 8337-8341 (2006).
82. Yoshimoto, M. et al. Three-color FISH analysis of TMPRSS2/ERG fusions in prostate cancer indicates that genomic microdeletion of chromosome 21 is associated with rearrangement. Neoplasia 8, 465-469 (2006).
83. Mitelman, F., Mertens, F. & Johansson, B. A breakpoint map of recurrent chromosomal rearrangements in human neoplasia. Nature Genet. 15, 417-474 (1997).
84. Pinkel, D. et al. High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nature Genet. 20, 207-211 (1998).
85. Pollack, J. R. et al. Genome-wide analysis of DNA copy-number changes using cDNA microarrays. Natrue Genet. 23, 41-46 (1999).
86. Cowell, J. K. & Nowak, N. J. High-resolution analysis of genetic events in cancer cells using bacterial artificial chromosome arrays and comparative genome hybridization. Adv. Cancer Res. 90, 91-125 (2003).
87. Bacher, U. et al. Population-based age-specific incidences of cytogenetic subgroups of acute myeloid leukemia. Haematologica 90, 1502-1510 (2005).
88. Sanderson R. N. et al. Population-based demographic study of karyotypes in 1709 patients with adult acute myeloid leukemia. Leukemia 20, 444-450 (2006).
89. Gorunova, L. et al. Cytogenetic analysis of pancreatic carcinomas: intratumor heterogeneity and nonrandom pattern of chromosome aberrations. Genes Chromosomes Cancer 23, 81-99 (1998).
90. Johansson, B. et al. Cytogenetic polyclonality in hematologic malignancies. Genes Chromosomes Cancer 24, 222-229 (1999).
91. Han, J. Y., Theil, K. S. & Hoeltge, G. Frequencies and characterization of cytogenetically unrelated clones in various hematologic malignancies: seven years of experiences in a single institution. Cancer Genet. Cytogenet. 164, 128-132 (2006).
92. Pierotti, M. A. et al. Characterization of an inversion on the long arm of chromosome 10 juxtaposing D10S170 and RET and creating the oncogenic sequence RET/PTC. Proc. Natl Acad. Sci. USA 89, 1616-1620 (1992). The first description of a gene fusion in a solid tumour.
93. Pierotti, M. A. Chromosomal rearrangements in thyroid carcinomas: a recombination or death dilemma. Cancer Lett. 166, 1-7 (2001).
94. Behboudi, A. et al. Molecular classification of mucoepidermoid carcinomas- prognostic significance of the MECT1-MAML2 fusion oncogene. Genes Chromosomes Cancer 45, 470-481 (2006).
95. French, C. A. et al. Midline carcinoma of children and young adults with NUT rearrangement. J. Clin. Oncol. 22, 4135-4139 (2004).
96. Tomlins, S. A. et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310, 644-648 (2005). The first study to show a fusion gene that occurs in a large proportion of a common malignant solid tumour.
97. Cerveira, N. et al. TMPRSS2-ERG gene fusion causing ERG overexpression precedes chromosome copy number changes in prostate carcinomas and paired HGPIN lesions. Neoplasia 8, 826-832 (2006).
98. Hermans, K. G. et al. TMPRSS2:ERG fusion by translocation or interstitial deletion is highly relevant in androgen-dependent prostate cancer, but is bypassed in late-stage androgen receptor-negative prostate cancer. Cancer Res. 66, 10658-10663 (2006).
99. Iljin, K. et al. TMPRSS2 fusions with oncogenic ETS factors in prostate cancer involve unbalanced genomic rearrangements and are associated with HDAC1 and epigenetic reprogramming. Cancer Res. 66, 10242-10246 (2006).
100. Soller, M. J. et al. Confirmation of the high frequency of the TMPRSS2/ERG fusion gene in prostate cancer. Genes Chromosomes Cancer 45, 717-719 (2006).
101. Wang, J., Cai, Y., Ren, C. & Ittmann, M. Expression of variant TMPRSS2/ERG fusion messenger RNAs is associated with aggressive prostate cancer. Cancer Res. 66, 8347-8351 (2006).
102. Tomlins, S. A. et al. TMPRSS2:ETV4 gene fusions define a third molecular subtype of prostate cancer. Cancer Res. 66, 3396-3400 (2006).
103. Parkin, D. M., Bray, F., Ferlay, J. & Pisani, P. Global cancer statistics, 2002. CA. Cancer J. Clin. 55, 74-108 (2005).
104. Kamanger, F., Dores, G. M. & Anderson, W. F. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J. Clin. Oncol. 24, 2137-2150 (2006).
105. Cancer Incidence in Sweden 2004. The National Board of Health and Welfare, Stockholm (2004).
106. Novo, F. J. & Vizmanos, J. L. Chromosome translocations in cancer: computational evidence for the random generation of double-strand breaks. Trends Genet. 22, 193-196 (2006).
107. Povirk, L. F. Biochemical mechanisms of chromosomal translocations resulting from DNA double-strand breaks. DNA Repair 5, 1199-1212 (2006).
108. Obe, G. et al. Chromosomal aberrations: formation, identification and distribution. Mutat. Res. 504, 17-36 (2002).
109. Mitelman, F., Mark, J., Levan, G. &Levan, A. Tumor etiology and chromosome pattern. Science 176, 1340-1341 (1972).
110. Mitelman, F., Brandt, L. & Nilsson, P. G. Relation among occupational exposure to potential mutagenic/carcinogenic agents, clinical findings, and bone marrow chromosomes in acute nonlymphocytic leukemia. Blood 52, 1229-1237 (1978).
111. Mauritzson, N. et al. Pooled analysis of clinical and cytogenetic features in treatment-related and de novo adult acute myeloid leukemia and myelodysplastic syndromes based on a consecutive series of 761 patients analyzed 1976-1993 and on 5098 unselected cases reported in the literature 1974-2001. Leukemia 16, 2366-2378 (2002).
112. Pedersen-Bjergaard, J., Andersen, M. K., Christiansen, D. H. & Nerlov, C. Genetic pathways in therapy-related myelodysplasia and acute myeloid leukemia. Blood 99, 1909-1912 (2002).
113. Mistry, A. R. et al. DNA topoisomerase II in therapy-related acute promyelocytic leukemia. N. Engl. J. Med. 352, 1529-1538 (2005).
114. Zhang, Y. & Rowley, J. D. Chromatin structural elements and chromosomal translocations in leukemia. DNA Repair 5, 1282-1297 (2006).
115. Fugazzola, L. et al. Oncogenic rearrangements of the RET proto-oncogene in papillary thyroid carcinomas from children exposed to the Chernobyl nuclear accident. Cancer Res. 55, 5617-5620 (1995).
116. Rabes, H. M. et al. Pattern of radiation-induced RET and NTRK1 rearrangements in 191 post-chernobyl papillary thyroid carcinomas: biological, phenotypic, and clinical implications. Clin. Cancer Res. 6, 1093-1103 (2000).
117. Taylor, A. M. Chromosome instability syndromes. Best Pract. Res. Clin. Haematol. 14, 631-644 (2001).
118. Misteli, T. Concepts in nuclear architecture. BioEssays 27, 477-487 (2005).
119. Cremer, T. et al. Chromosome territories - a functional nuclear landscape. Curr. Opin. Cell Biol. 18, 307-316 (2006). References 118-119 provide comprehensive reviews of chromosome territories in interphase nuclei.
120. Kozubek, S. et al. The topological organization of chromosomes 9 and 22 in cell nuclei has a determinative role in the induction of t(9,22) translocations and in the pathogenesis of t(9,22) leukemias. Chromosoma 108, 426-435 (1999).
121. Neves, H., Ramos, C., da Silva, M. G., Parreira, A. & Parreira, L. The nuclear topography of ABL, BCR, PML, and RARalpha genes: evidence for gene proximity in specific phases of the cell cycle and stages of hematopoietic differentiation. Blood 93, 1197-1207 (1999).
122. Nikiforova, M. N. et al. Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 290, 138-141 (2000).
123. Roix, J. J., McQueen, P. G., Munson, P. J., Parada, L. A. & Misteli, T. Spatial proximity of translocation-prone gene loci in human lymphomas. Nature Genet. 34, 287-291 (2003).
124. Raghavan, S. C. & Lieber, M. R. DNA structures at chromosomal translocation sites. BioEssays 28, 480-494 (2006).
125. Greaves, M. F. & Wiemels, J. Origins of chromosome translocations in childhood leukaemia. Nature Rev. Cancer 3, 639-649 (2003). Discusses the prenatal origin of gene fusions and the latency period in the development of leukaemia.
126. Huntly, B. J. P. & Gilliland, D. G. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nature Rev. Cancer 5, 311-321 (2005).
127. Wang, J. C. Y. & Dick, J. E. Cancer stem cells: lessons from leukemia. Trends Cell Biol. 15, 494-501 (2005). References 126-127 provide comprehensive reviews of the role of stem cells in oncogenesis.
128. Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J. & Clarke, M. F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100, 3983-3988 (2003).
129. Singh, S. K. et al. Identification of human brain tumour initiating cells. Nature 432, 396-401 (2004).
130. Bender Kim, C. F. et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121, 823-835 (2005).
131. O'Brien, C. A., Pollett, A., Gallinger, S. & Dick, J. E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445, 106-110 (2007).
132. Ricci-Vitiani, L. et al. Identification and expansion of human colon-cancer-initiating cells. Nature 445, 111-115 (2007).
133. Johansson, B., Fioretos, T. & Mitelman, F. Cytogenetic and molecular genetic evolution of chronic myeloid leukemia. Acta Haematol. 107, 76-94 (2002).
134. Turhan, A. G. et al. Highly purified primitive hematopoietic stem cells are PML-RARA negative and generate nonclonal progenitors in acute promyelocytic leukemia. Blood 85, 2154-2161 (1995).
135. Castor, A. et al. Distinct patterns of hematopoietic stem cell involvement in acute lymphoblastic leukemia. Nature Med. 11, 630-637 (2005).
136. Hotfilder, M. et al. Leukemic stem cells in childhood high-risk ALL/t(9;22) and t(4;11) are present in primitive lymphoid-restricted CD34+CD19- cells. Cancer Res. 65, 1442-1449 (2005).
137. Riggi, N. et al. Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells. Cancer Res. 65, 11459-11468 (2005).
138. Riggi, N. et al. Expression of the FUS-CHOP fusion protein in primary mesenchymal progenitor cells gives rise to a model of myxoid liposarcoma. Cancer Res. 66, 7016-7023 (2006).
139. Janz, S., Potter, M. & Rabkin, C. S. Lymphoma- and leukemia-associated chromosomal translocations in healthy individuals. Genes Chromosomes Cancer 36, 211-223 (2003).
140. Nucifora, G., Larson, R. A. & Rowley, J. D. Persistence of the 8;21 translocation in patients with acute myeloid leukemia type M2 in long-term remission. Blood 82, 712-715 (1993).
141. Jurlander, J. et al. Persistence of the AML1/ETO fusion transcript in patients treated with allogeneic bone marrow transplantation for t(8;21) leukemia. Blood 88, 2183-2191 (1996).
142. Castilla, L. H. et al. The fusion gene Cbfb-MYH11 blocks myeloid differentiation and predisposes mice to acute myelomonocytic leukaemia. Nature Genet. 23, 144-146 (1999).
143. Higuchi, M. et al. Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. Cancer Cell 1, 63-74 (2002).
144. Kelly, L. M., Gilliland, D. G. Genetics of myeloid leukemias. Annu. Rev. Genomics Hum. Genet. 3, 179-198 (2002).