Classifying leukemia types with chromatin conformation data

Genome Biology

Volumn 15, Issue 4, 2014, Pages

  Rousseau, Mathieu ^a,b   Ferraiuolo, Maria A ^a   Crutchley, Jennifer L ^a   Wang, Xue Qing D ^a   Miura, Hisashi ^a   Blanchette, Mathieu ^b   Dostie, Josée ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MIXED LINEAGE LEUKEMIA PROTEIN; CHROMATIN; HOMEODOMAIN PROTEIN; HOXA PROTEIN;

ARTICLE; CANCER CLASSIFICATION; CHROMATIN CONFORMATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; GENE; GENE CLUSTER; GENE LOCUS; HOXA GENE; LEUKEMIA; PROTEIN EXPRESSION; SUPPORT VECTOR MACHINE; CHEMISTRY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETICS; HUMAN; TUMOR CELL LINE;

CELL LINE, TUMOR; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; HOMEODOMAIN PROTEINS; HUMANS; LEUKEMIA;

EID: 84899652185     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-4-r60     Document Type: Article

References (73)

1. Dostie J, Bickmore WA. Chromosome organization in the nucleus - charting new territory across the Hi-Cs. Curr Opin Genet Dev 2012, 22:125-131. 10.1016/j.gde.2011.12.006, 22265226.
2. Fraser P, Bickmore W. Nuclear organization of the genome and the potential for gene regulation. Nature 2007, 447:413-417. 10.1038/nature05916, 17522674.
3. Babu MM, Janga SC, de Santiago I, Pombo A. Eukaryotic gene regulation in three dimensions and its impact on genome evolution. Curr Opin Genet Dev 2008, 18:571-582. 10.1016/j.gde.2008.10.002, 19007886.
4. Cook PR. A model for all genomes: the role of transcription factories. J Mol Biol 2009, 395:1-10.
5. Pombo A, Branco MR. Functional organisation of the genome during interphase. Curr Opin Genet Dev 2007, 17:451-455. 10.1016/j.gde.2007.08.008, 17920259.
6. Cremer T, Cremer M. Chromosome territories. Cold Spring Harb Perspect Biol 2010, 2:a003889. 2829961, 20300217.
7. Eskiw CH, Cope NF, Clay I, Schoenfelder S, Nagano T, Fraser P. Transcription factories and nuclear organization of the genome. Cold Spring Harb Symp Quant Biol 2010, 75:501-506. 10.1101/sqb.2010.75.046, 21467135.
8. Razin SV, Gavrilov AA, Pichugin A, Lipinski M, Iarovaia OV, Vassetzky YS. Transcription factories in the context of the nuclear and genome organization. Nucleic Acids Res 2011, doi:10.1093/nar/gkr683.
9. Li G, Reinberg D. Chromatin higher-order structures and gene regulation. Curr Opin Genet Dev 2011, 21:175-186. 10.1016/j.gde.2011.01.022, 3124554, 21342762.
10. West AG, Fraser P. Remote control of gene transcription. Hum Mol Genet 2005, 14:R101-R111. 10.1093/hmg/ddi104, 15809261.
11. Woodcock CL. Chromatin architecture. Curr Opin Struct Biol 2006, 16:213-220. 10.1016/j.sbi.2006.02.005, 16540311.
12. Gondor A, Ohlsson R. Chromosome crosstalk in three dimensions. Nature 2009, 461:212-217. 10.1038/nature08453, 19741702.
13. Tolhuis B, Palstra RJ, Splinter E-G, Grosveld F, de Laat W. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 2002, 10:1453-1465. 10.1016/S1097-2765(02)00781-5, 12504019.
14. Mishiro T, Ishihara K, Hino S, Tsutsumi S, Aburatani H, Shirahige K, Kinoshita Y, Nakao M. Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J 2009, 28:1234-1245. 10.1038/emboj.2009.81, 2683055, 19322193.
15. Morey C, Avner P. The demoiselle of X-inactivation: 50 years old and as trendy and mesmerising as ever. PLoS Genet 2011, 7:e1002212. 10.1371/journal.pgen.1002212, 3141017, 21811421.
16. Chaumeil J, Le Baccon P, Wutz A, Heard E. A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev 2006, 20:2223-2237. 10.1101/gad.380906, 1553206, 16912274.
17. Mattout A, Pike BL, Towbin BD, Bank EM, Gonzalez-Sandoval A, Stadler MB, Meister P, Gruenbaum Y, Gasser SM. An EDMD mutation in C. elegans lamin blocks muscle-specific gene relocation and compromises muscle integrity. Curr Biol 2011, 21:1603-1614. 10.1016/j.cub.2011.08.030, 21962710.
18. Pomerantz MM, Ahmadiyeh N, Jia L, Herman P, Verzi MP, Doddapaneni H, Beckwith CA, Chan JA, Hills A, Davis M, Yao K, Kehoe SM, Lenz HJ, Haiman CA, Yan C, Henderson BE, Frenkel B, Barretina J, Bass A, Tabernero J, Baselga J, Regan MM, Manak JR, Shivdasani R, Coetzee GA, Freedman ML. The 8q24 cancer risk variant rs6983267 shows long-range interaction with MYC in colorectal cancer. Nat Genet 2009, 41:882-884. 10.1038/ng.403, 2763485, 19561607.
19. Pittman AM, Naranjo S, Jalava SE, Twiss P, Ma Y, Olver B, Lloyd A, Vijayakrishnan J, Qureshi M, Broderick P, van Wezel T, Morreau H, Tuupanen S, Aaltonen LA, Alonso ME, Manzanares M, Gavilan A, Visakorpi T, Gomez-Skarmeta JL, Houlston RS. Allelic variation at the 8q23.3 colorectal cancer risk locus functions as a cis-acting regulator of EIF3H. PLoS Genet 2010, 6:e1001126. 10.1371/journal.pgen.1001126, 2940760, 20862326.
20. Meyer KB, Maia AT, O'Reilly M, Ghoussaini M, Prathalingam R, Porter-Gill P, Ambs S, Prokunina-Olsson L, Carroll J, Ponder BA. A functional variant at a prostate cancer predisposition locus at 8q24 is associated with PVT1 expression. PLoS Genet 2011, 7:e1002165. 10.1371/journal.pgen.1002165, 3140991, 21814516.
21. Tiwari VK, Cope L, McGarvey KM, Ohm JE, Baylin SB. A novel 6C assay uncovers polycomb-mediated higher order chromatin conformations. Genome Res 2008, 18:1171-1179. 10.1101/gr.073452.107, 2493406, 18502945.
22. Erfurth F, Hemenway CS, de Erkenez AC, Domer PH. MLL fusion partners AF4 and AF9 interact at subnuclear foci. Leukemia 2004, 18:92-102. 10.1038/sj.leu.2403200, 14603337.
23. Tolhuis B, Blom M, Kerkhoven RM, Pagie L, Teunissen H, Nieuwland M, Simonis M, de Laat W, van Lohuizen M, van Steensel B. Interactions among polycomb domains Are guided by chromosome architecture. PLoS Genet 2011, 7:e1001343. 10.1371/journal.pgen.1001343, 3063757, 21455484.
24. Smith E, Lin C, Shilatifard A. The super elongation complex (SEC) and MLL in development and disease. Genes Dev 2011, 25:661-672. 10.1101/gad.2015411, 3070929, 21460034.
25. Balgobind BV, Zwaan CM, Pieters R, Van den Heuvel-Eibrink MM. The heterogeneity of pediatric MLL-rearranged acute myeloid leukemia. Leukemia 2011, 25:1239-1248. 10.1038/leu.2011.90, 21566656.
26. Tkachuk DC, Kohler S, Cleary ML. Involvement of a homolog of drosophila trithorax by 11q23 chromosomal translocations in acute leukemias. Cell 1992, 71:691-700. 10.1016/0092-8674(92)90602-9, 1423624.
27. Thirman MJ, Gill HJ, Burnett RC, Mbangkollo D, McCabe NR, Kobayashi H, Ziemin-van Der Peol S, Kaneko Y, Morgan R, Sandberg AA, Chaganti RSK, Larson RA, Le Beau MM, Diaz MO, Rowley JD. Rearrangement of the MLL gene in acute lymphoblastic and acute myeloid leukemias with 11q23 chromosomal translocations. N Engl J Med 1993, 329:909-914. 10.1056/NEJM199309233291302, 8361504.
28. Daser A, Rabbitts TH. Extending the repertoire of the mixed-lineage leukemia gene MLL in leukemogenesis. Genes Dev 2004, 18:965-974. 10.1101/gad.1195504, 15132992.
29. Ferrando AA, Armstrong SA, Neuberg DS, Sallan SE, Silverman LB, Korsmeyer SJ, Look AT. Gene expression signatures in MLL-rearranged T-lineage and B-precursor acute leukemias: dominance of HOX dysregulation. Blood 2003, 102:262-268. 10.1182/blood-2002-10-3221, 12637319.
30. Lin C, Smith ER, Takahashi H, Lai KC, Martin-Brown S, Florens L, Washburn MP, Conaway JW, Conaway RC, Shilatifard A. AFF4, a component of the ELL/P-TEFb elongation complex and a shared subunit of MLL chimeras, can link transcription elongation to leukemia. Mol Cell 2010, 37:429-437. 10.1016/j.molcel.2010.01.026, 2872029, 20159561.
31. Biswas D, Milne TA, Basrur V, Kim J, Elenitoba-Johnson KS, Allis CD, Roeder RG. Function of leukemogenic mixed lineage leukemia 1 (MLL) fusion proteins through distinct partner protein complexes. Proc Natl Acad Sci U S A 2011, 108:15751-15756. 10.1073/pnas.1111498108, 3179097, 21896721.
32. Marschalek R. Mechanisms of leukemogenesis by MLL fusion proteins. Br J Haematol 2011, 152:141-154. 10.1111/j.1365-2141.2010.08459.x, 21118195.
33. Cavalli G, Misteli T. Functional implications of genome topology. Nat Struct Mol Biol 2013, 20:290-299. 10.1038/nsmb.2474, 23463314.
34. Look AT. Oncogenic transcription factors in the human acute leukemias. Science 1997, 278:1059-1064. 10.1126/science.278.5340.1059, 9353180.
35. Liu H, Cheng EH, Hsieh JJ. MLL fusions: pathways to leukemia. Cancer Biol Ther 2009, 8:1204-1211. 10.4161/cbt.8.13.8924, 3289713, 19729989.
36. Cowell IG, Sondka Z, Smith K, Lee KC, Manville CM, Sidorczuk-Lesthuruge M, Rance HA, Padget K, Jackson GH, Adachi N, Austin CA. Model for MLL translocations in therapy-related leukemia involving topoisomerase IIbeta-mediated DNA strand breaks and gene proximity. Proc Natl Acad Sci U S A 2012, 109:8989-8994. 10.1073/pnas.1204406109, 3384169, 22615413.
37. Eguchi M, Eguchi-Ishimae M, Greaves M. Molecular pathogenesis of MLL-associated leukemias. Int J Hematol 2005, 82:9-20. 10.1532/IJH97.05042, 16105754.
38. Fraser J, Rousseau M, Shenker S, Ferraiuolo MA, Hayashizaki Y, Blanchette M, Dostie J. Chromatin conformation signatures of cellular differentiation. Genome Biol 2009, 10:R37. 10.1186/gb-2009-10-4-r37, 2688928, 19374771.
39. Sauvageau G, Lansdorp PM, Eaves CJ, Hogge DE, Dragowska WH, Reid DS, Largman C, Lawrence HJ, Humphries RK. Differential expression of homeobox genes in functionally distinct CD34+ subpopulations of human bone marrow cells. Proc Natl Acad Sci U S A 1994, 91:12223-12227. 10.1073/pnas.91.25.12223, 45409, 7527557.
40. Pineault N, Helgason CD, Lawrence HJ, Humphries RK. Differential expression of Hox, Meis1, and Pbx1 genes in primitive cells throughout murine hematopoietic ontogeny. Exp Hematol 2002, 30:49-57. 10.1016/S0301-472X(01)00757-3, 11823037.
41. Calvo R, West J, Franklin W, Erickson P, Bemis L, Li E, Helfrich B, Bunn P, Roche J, Brambilla E, Rosell R, Gemmill RM, Drabkin HA. Altered HOX and WNT7A expression in human lung cancer. Proc Natl Acad Sci U S A 2000, 97:12776-12781. 10.1073/pnas.97.23.12776, 18840, 11070089.
42. Makiyama K, Hamada J, Takada M, Murakawa K, Takahashi Y, Tada M, Tamoto E, Shindo G, Matsunaga A, Teramoto K, Komuro K, Kondo S, Katoh H, Koike T, Moriuchi T. Aberrant expression of HOX genes in human invasive breast carcinoma. Oncol Rep 2005, 13:673-679.
43. Maeda K, Hamada J, Takahashi Y, Tada M, Yamamoto Y, Sugihara T, Moriuchi T. Altered expressions of HOX genes in human cutaneous malignant melanoma. Int J Cancer 2005, 114:436-441. 10.1002/ijc.20706, 15551325.
44. Eklund EA. The role of HOX genes in malignant myeloid disease. Curr Opin Hematol 2007, 14:85-89. 10.1097/MOH.0b013e32801684b6, 17255784.
45. Thorsteinsdottir U, Sauvageau G, Hough MR, Dragowska W, Lansdorp PM, Lawrence HJ, Largman C, Humphries RK. Overexpression of HOXA10 in murine hematopoietic cells perturbs both myeloid and lymphoid differentiation and leads to acute myeloid leukemia. Mol Cell Biol 1997, 17:495-505. 231774, 8972230.
46. Kroon E, Krosl J, Thorsteinsdottir U, Baban S, Buchberg AM, Sauvageau G. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. Embo J 1998, 17:3714-3725. 10.1093/emboj/17.13.3714, 1170707, 9649441.
47. Ayton PM, Cleary ML. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev 2003, 17:2298-2307. 10.1101/gad.1111603, 196466, 12952893.
48. Garcia-Fernandez J. The genesis and evolution of homeobox gene clusters. Nat Rev Genet 2005, 6:881-892. 10.1038/nrg1723, 16341069.
49. Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH. Zebrafish hox clusters and vertebrate genome evolution. Science 1998, 282:1711-1714.
50. Ethier SD, Miura H, Dostie J. Discovering genome regulation with 3C and 3C-related technologies. Biochim Biophys Acta 1819, 2012:401-410.
51. Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL, Honan TA, Rubio ED, Krumm A, Lamb J, Nusbaum C, Green RD, Dekker J. Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res 2006, 16:1299-1309. 10.1101/gr.5571506, 1581439, 16954542.
52. Ferraiuolo MA, Rousseau M, Miyamoto C, Shenker S, Wang XQ, Nadler M, Blanchette M, Dostie J. The three-dimensional architecture of Hox cluster silencing. Nucleic Acids Res 2010, 38:7472-7484. 10.1093/nar/gkq644, 2995065, 20660483.
53. Cortes C, Vapnik V. Support-vector networks. Mach Learn 1995, 20:273-297.
54. Noble WS. What is a support vector machine?. Nat Biotechnol 2006, 24:1565-1567. 10.1038/nbt1206-1565, 17160063.
55. Rousseau M, Crutchley JL, Miura H, Suderman M, Blanchette M, Dostie J. Hox in motion: tracking HoxA cluster conformation during differentiation. Nucleic Acids Res 2014, 42:1524-1540. 10.1093/nar/gkt998, 3919592, 24174538.
56. Phillips JE, Corces VG. CTCF: master weaver of the genome. Cell 2009, 137:1194-1211. 10.1016/j.cell.2009.06.001, 3040116, 19563753.
57. Fraser J, Ethier SD, Miura H, Dostie J. A Torrent of data: mapping chromatin organization using 5C and high-throughput sequencing. Methods Enzymol 2012, 513:113-141.
58. Ferraiuolo MA, Sanyal A, Naumova N, Dekker J, Dostie J. From cells to chromatin: capturing snapshots of genome organization with 5C technology. Methods 2012, 58:255-267. 10.1016/j.ymeth.2012.10.011, 3874844, 23137922.
59. Ludwig JA, Weinstein JN. Biomarkers in cancer staging, prognosis and treatment selection. Nat Rev Cancer 2005, 5:845-856. 10.1038/nrc1739, 16239904.
60. Dr Josee Dostie Laboratory. [http://Dostielab.biochem.mcgill.ca].
61. Weka 3: Data Mining Software in Java, version 3.7.5. [http://www.cs.waikato.ac.nz/ml/weka/].
62. Hall M, Frank E, Holmes G, Pfahringer B, Reutemann P, Witten IH. The WEKA data mining software: an update. SIGKDD Explorations 2009, 11:10-18.
63. Keerthi SS, Shevade SK, Bhattacharyya C, Murthy KRK. Improvements to Platt's SMO algorithm for SVM classifier design. Neural Computation 2001, 13:13.
64. Hastie T, Tibshirani R. Classification by pairwise coupling. Ann Statist 1998, 26:451-800.
65. R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. [http://www.R-project.org/].
66. Lefrancois P, Euskirchen GM, Auerbach RK, Rozowsky J, Gibson T, Yellman CM, Gerstein M, Snyder M. Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC Genomics 2009, 10:37. 10.1186/1471-2164-10-37, 2656530, 19159457.
67. The McGill University and Génome Québec Innovation Centre. [http://gqinnovationcenter.com/].
68. Collection of command line tools for Short-Reads FASTA/FASTQ files preprocessing. http://hannonlab.cshl.edu/fastx_toolkit/.
69. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
70. Software for motif discovery and ChIP-Seq analysis. http://homer.salk.edu/homer/chipseq/.
71. Dr. Josee Dostie Laboratory. http://dostielab.biochem.mcgill.ca/research.html.
72. 5C and ChIP-seq datasets generated for this study downloadable from the Gene Expression Omnibus. http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE55408.
73. Lajoie BR, van Berkum NL, Sanyal A, Dekker J. My5C: web tools for chromosome conformation capture studies. Nat Methods 2009, 6:690-691. 10.1038/nmeth1009-690, 2859197, 19789528.