Analyzing tumor heterogeneity and driver genes in single myeloid leukemia cells with SBCapSeq

Nature Biotechnology

Volumn 34, Issue 9, 2016, Pages 962-972

  Mann, Karen M ^a,b,g   Newberg, Justin Y ^a   Black, Michael A ^c   Jones, Devin J ^a   Amaya Manzanares, Felipe ^a   Guzman Rojas, Liliana ^a   Kodama, Takahiro ^a   Ward, Jerrold M ^b,f   Rust, Alistair G ^d,f,g   Van Der Weyden, Louise ^d   Yew, Christopher Chin Kuan ^b,f,h   Waters, Jill L ^e,f,i   Leung, Marco L ^e   Rogers, Keith ^b   Rogers, Susan M ^b   Mcnoe, Leslie A ^c   Selvanesan, Luxmanan ^c,f,j   Navin, Nicholas ^b   Jenkins, Nancy A ^a,b   Copeland, Neal G ^a,b   Mann, Michael B ^a,b,g   more..

^a HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^f Global VetPathology   (United States)

^g INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^h National Heart Research Institute Singapore   (Singapore)

ⁱ ILLUMINA INC   (United States)

^j Pacific Edge Limited   (New Zealand)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BIOINFORMATICS; CELL CULTURE; CELL PROLIFERATION; CELLS; CYTOLOGY; DISEASES; GENE EXPRESSION; GENES; TUMORS;

CELL POPULATIONS; COST PROHIBITIVE; INTERACTING GENES; MYELOID LEUKEMIA; SEQUENCING METHOD; SINGLECELL ANALYSIS; TRANSPOSON INSERTION SITE; TUMOR HETEROGENEITY;

CLONE CELLS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOINFORMATICS; CELL HETEROGENEITY; CLONE; CONTROLLED STUDY; EXPERIMENTAL MODEL; GENE; GENE SEQUENCE; HUMAN; HYBRIDIZATION; MOUSE; MYELOID LEUKEMIA; MYELOID LEUKEMIA CELL LINE; NONHUMAN; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; TRANSPOSON; TUMOR GENE; ALGORITHM; ANIMAL; DNA SEQUENCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SEQUENCING; IN SITU HYBRIDIZATION; MALE; PATHOLOGY; PROCEDURES; SOFTWARE;

DNA; SLEEPING BEAUTY TRANSPOSASE, HUMAN; TRANSPOSASE; TRANSPOSON; TUMOR MARKER; TUMOR PROTEIN;

ALGORITHMS; ANIMALS; BIOMARKERS, TUMOR; DNA TRANSPOSABLE ELEMENTS; DNA, NEOPLASM; FEMALE; GENES, NEOPLASM; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; IN SITU HYBRIDIZATION; LEUKEMIA, MYELOID; MALE; MICE; MUTAGENESIS, INSERTIONAL; NEOPLASM PROTEINS; SEQUENCE ANALYSIS, DNA; SOFTWARE; TRANSPOSASES;

EID: 84987657154     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.3637     Document Type: Article

References (62)

1. Mann, M. B., Jenkins, N. A., Copeland, N. G. & Mann, K. M. Sleeping Beauty mutagenesis: exploiting forward genetic screens for cancer gene discovery. Curr. Opin. Genet. Dev. 24, 16-22 (2014).
2. Mann, K. M., Jenkins, N. A., Copeland, N. G. & Mann, M. B. Transposon insertional mutagenesis models of cancer. Cold Spring Harb. Protoc. 2014, 235-247 (2014).
3. Mann, M. B. et al. Transposon mutagenesis identifies genetic drivers of BrafV600E melanoma. Nat. Genet. 47, 486-495 (2015).
4. Takeda, H. et al. Transposon mutagenesis identifies genes and evolutionary forces driving gastrointestinal tract tumor progression. Nat. Genet. 47, 142-150 (2015).
5. Genovesi, L. A. et al. Sleeping Beauty mutagenesis in a mouse medulloblastoma model defines networks that discriminate between human molecular subgroups. Proc. Natl. Acad. Sci. USA 110, E4325-E4334 (2013).
6. Pérez-Mancera, P. A. et al. The deubiquitinase USP9X suppresses pancreatic ductal adenocarcinoma. Nature 486, 266-270 (2012).
7. Dupuy, A. J. et al. A modified Sleeping Beauty transposon system that can be used to model a wide variety of human cancers in mice. Cancer Res. 69, 8150-8156 (2009).
8. Lewandoski, M., Meyers, E. N. & Martin, G. R. Analysis of Fgf8 gene function in vertebrate development. Cold Spring Harb. Symp. Quant. Biol. 62, 159-168 (1997).
9. Jonkers, J. et al. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29, 418-425 (2001).
10. Olive, K. P. et al. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 119, 847-860 (2004).
11. Doyle, B. et al. p53 mutation and loss have different effects on tumourigenesis in a novel mouse model of pleomorphic rhabdomyosarcoma. J. Pathol. 222, 129-137 (2010).
12. Hanel, W. et al. Two hot spot mutant p53 mouse models display differential gain of function in tumorigenesis. Cell Death Differ. 20, 898-909 (2013).
13. Lang, G. A. et al. Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 119, 861-872 (2004).
14. Morton, J. P. et al. Mutant p53 drives metastasis and overcomes growth arrest/senescence in pancreatic cancer. Proc. Natl. Acad. Sci. USA 107, 246-251 (2010).
15. Cesta, M. F. Normal structure, function, and histology of the spleen. Toxicol. Pathol. 34, 455-465 (2006).
16. Anderson, K. et al. Ectopic expression of PAX5 promotes maintenance of biphenotypic myeloid progenitors coexpressing myeloid and B-cell lineage-associated genes. Blood 109, 3697-3705 (2007).
17. Swerdlow, S. H. et al. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues, 4th edn., Vol. 2 (The International Agency for Research on Cancer of the World Health Organization, 2008).
18. Futreal, P. A. et al. A census of human cancer genes. Nat. Rev. Cancer 4, 177-183 (2004).
19. Cancer Genome Atlas Research Network. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N. Engl. J. Med. 368, 2059-2074 (2013).
20. Tang, J. Z. et al. Transposon mutagenesis reveals cooperation of ETS family transcription factors with signaling pathways in erythro-megakaryocytic leukemia. Proc. Natl. Acad. Sci. USA 110, 6091-6096 (2013).
21. Vassiliou, G. S. et al. Mutant nucleophosmin and cooperating pathways drive leukemia initiation and progression in mice. Nat. Genet. 43, 470-475 (2011).
22. Milella, M. et al. Therapeutic targeting of the MEK/MAPK signal transduction module in acute myeloid leukemia. J. Clin. Invest. 108, 851-859 (2001).
23. Ricciardi, M. R. et al. Quantitative single cell determination of ERK phosphorylation and regulation in relapsed and refractory primary acute myeloid leukemia. Leukemia 19, 1543-1549 (2005).
24. Friedel, R. H. et al. Clonal expansion analysis of transposon insertions by high-throughput sequencing identifies candidate cancer genes in a PiggyBac mutagenesis screen. PLoS One 8, e72338 (2013).
25. Koudijs, M. J. et al. High-throughput semiquantitative analysis of insertional mutations in heterogeneous tumors. Genome Res. 21, 2181-2189 (2011).
26. Brett, B. T. et al. Novel molecular and computational methods improve the accuracy of insertion site analysis in Sleeping Beauty-induced tumors. PLoS One 6, e24668 (2011).
27. Kircher, M., Sawyer, S. & Meyer, M. Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res. 40, e3 (2012).
28. Lou, D. I. et al. High-throughput DNA sequencing errors are reduced by orders of magnitude using circle sequencing. Proc. Natl. Acad. Sci. USA 110, 19872-19877 (2013).
29. Liu, G. et al. Target-site preferences of Sleeping Beauty transposons. J. Mol. Biol. 346, 161-173 (2005).
30. Vogelstein, B. et al. Cancer genome landscapes. Science 339, 1546-1558 (2013).
31. Wang, Y. et al. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 512, 155-160 (2014).
32. Tanaka, Y. et al. The transcriptional programme controlled by Runx1 during early embryonic blood development. Dev. Biol. 366, 404-419 (2012).
33. Taoudi, S. et al. ERG dependence distinguishes developmental control of hematopoietic stem cell maintenance from hematopoietic specification. Genes Dev. 25, 251-262 (2011).
34. Thoms, J. A. et al. ERG promotes T-acute lymphoblastic leukemia and is transcriptionally regulated in leukemic cells by a stem cell enhancer. Blood 117, 7079-7089 (2011).
35. Marcucci, G. et al. Cancer and Leukemia Group B Study. High expression levels of the ETS-related gene, ERG, predict adverse outcome and improve molecular risk-based classification of cytogenetically normal acute myeloid leukemia: A Cancer and Leukemia Group B Study. J. Clin. Oncol. 25, 3337-3343 (2007).
36. Hayashi, A. A. & Proud, C. G. The rapid activation of protein synthesis by growth hormone requires signaling through mTOR. Am. J. Physiol. Endocrinol. Metab. 292, E1647-E1655 (2007).
37. Sliwa, T. et al. Hyperexpression of NOTCH-1 is found in immature acute myeloid leukemia. Int. J. Clin. Exp. Pathol. 7, 882-889 (2014).
38. Wu, Y. et al. Therapeutic antibody targeting of individual Notch receptors. Nature 464, 1052-1057 (2010).
39. Marziali, G. et al. Role of Ets-1 in erythroid differentiation. Blood Cells Mol. Dis. 29, 553-561 (2002).
40. Sottoriva, A. et al. A Big Bang model of human colorectal tumor growth. Nat. Genet. 47, 209-216 (2015).
41. Busch, K. et al. Fundamental properties of unperturbed haematopoiesis from stem cells in vivo. Nature 518, 542-546 (2015).
42. Sun, J. et al. Clonal dynamics of native haematopoiesis. Nature 514, 322-327 (2014).
43. Dupuy, A. J., Akagi, K., Largaespada, D. A., Copeland, N. G. & Jenkins, N. A. Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 436, 221-226 (2005).
44. Starr, T. K. et al. A transposon-based genetic screen in mice identifies genes altered in colorectal cancer. Science 323, 1747-1750 (2009).
45. Rehg, J. E., Bush, D. & Ward, J. M. The utility of immunohistochemistry for the identification of hematopoietic and lymphoid cells in normal tissues and interpretation of proliferative and inflammatory lesions of mice and rats. Toxicol. Pathol. 40, 345-374 (2012).
46. Leung, M. L., Wang, Y., Waters, J. & Navin, N. E. SNES: single nucleus exome sequencing. Genome Biol. 16, 55 (2015).
47. Mann, K. M. et al. Australian Pancreatic Cancer Genome Initiative. Sleeping Beauty mutagenesis reveals cooperating mutations and pathways in pancreatic adenocarcinoma. Proc. Natl. Acad. Sci. USA 109, 5934-5941 (2012).
48. March, H. N. et al. Insertional mutagenesis identifies multiple networks of cooperating genes driving intestinal tumorigenesis. Nat. Genet. 43, 1202-1209 (2011).
49. de Ridder, J., Uren, A., Kool, J., Reinders, M. & Wessels, L. Detecting statistically significant common insertion sites in retroviral insertional mutagenesis screens. PLoS Comput. Biol. 2, e166 (2006).
50. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
51. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-seq. Bioinformatics 25, 1105-1111 (2009).
52. R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2013).
53. Gautier, L., Cope, L., Bolstad, B. M. & Irizarry, R. A. Affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307-315 (2004).
54. Koboldt, D. C. et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22, 568-576 (2012).
55. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
56. Wang, K., Li, M. & Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164 (2010).
57. Venkatraman, E. S. & Olshen, A. B. A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23, 657-663 (2007).
58. Kim, D. et al. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
59. Trapnell, C. et al. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31, 46-53 (2013).
60. Gu, Z., Gu, L., Eils, R., Schlesner, M. & Brors, B. circlize implements and enhances circular visualization in R. Bioinformatics 30, 2811-2812 (2014).
61. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).
62. Henare, K. et al. Dissection of stromal and cancer cell-derived signals in melanoma xenografts before and after treatment with DMXAA. Br. J. Cancer 106, 1134-1147 (2012).