Discovery of structural alterations in solid tumor oligodendroglioma by single molecule analysis

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Ray, Mohana ^a   Goldstein, Steve ^a   Zhou, Shiguo ^a   Potamousis, Konstantinos ^a   Sarkar, Deepayan ^b   Newton, Michael A ^c,d   Esterberg, Elizabeth ^c   Kendziorski, Christina ^c   Bogler, Oliver ^e   Schwartz, David C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b INDIAN STATISTICAL INSTITUTE   (India)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d University of Wisconsin Madison   (United States)

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

Author keywords

Cancer genomics; Mutation; Oligodendroglioma; Optical mapping; Single molecule; Structural variation

Indexed keywords

GENOMIC DNA;

ARTICLE; CHROMOSOME 19Q; CHROMOSOME 1P; CONTROLLED STUDY; COPY NUMBER VARIATION; DNA STRUCTURE; GENE INSERTION; GENE LOCUS; GENE STRUCTURE; GENETIC HETEROGENEITY; HUMAN; MICROARRAY ANALYSIS; OLIGODENDROGLIOMA; POLYMERASE CHAIN REACTION; SCORING SYSTEM; SINGLE NUCLEOTIDE POLYMORPHISM; STRUCTURE ANALYSIS;

ADULT; AGED; BASE SEQUENCE; CHROMOSOMES, HUMAN, PAIR 1; CHROMOSOMES, HUMAN, PAIR 19; DNA COPY NUMBER VARIATIONS; FEMALE; GENOMICS; HUMANS; MUTATION; OLIGODENDROGLIOMA; PHYSICAL CHROMOSOME MAPPING; POLYMERASE CHAIN REACTION; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCIBILITY OF RESULTS;

EID: 84880907747     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-505     Document Type: Article

References (157)

1. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987, 235(4785):177-182. 10.1126/science.3798106, 3798106.
2. Bos JL. Ras oncogenes in human cancer: a review. Cancer Res 1989, 49(17):4682-4689.
3. Murphree AL, Benedict WF. Retinoblastoma: clues to human oncogenesis. Science 1984, 223(4640):1028-1033. 10.1126/science.6320372, 6320372.
4. Orlow I, Lacombe L, Hannon GJ, Serrano M, Pellicer I, Dalbagni G, Reuter VE, Zhang ZF, Beach D, Cordon-Cardo C. Deletion of the p16 and p15 genes in human bladder tumors. J Natl Cancer Inst 1995, 87(20):1524-1529. 10.1093/jnci/87.20.1524, 7563186.
5. ar-Rushdi A, Nishikura K, Erikson J, Watt R, Rovera G, Croce CM. Differential expression of the translocated and the untranslocated c-myc oncogene in Burkitt lymphoma. Science 1983, 222(4622):390-393. 10.1126/science.6414084, 6414084.
6. Shtivelman E, Lifshitz B, Gale RP, Canaani E. Fused transcript of abl and bcr genes in chronic myelogenous leukaemia. Nature 1985, 315(6020):550-554. 10.1038/315550a0, 2989692.
7. Albertson DG, Collins C, McCormick F, Gray JW. Chromosome aberrations in solid tumors. Nat Genet 2003, 34(4):369-376. 10.1038/ng1215, 12923544.
8. Farabegoli F, Santini D, Ceccarelli C, Taffurelli M, Marrano D, Baldini N. Clone heterogeneity in diploid and aneuploid breast carcinomas as detected by FISH. Cytometry 2001, 46(1):50-56. 10.1002/1097-0320(20010215)46:1<50::AID-CYTO1037>3.0.CO;2-T, 11241507.
9. Marusyk A, Polyak K. Tumor heterogeneity: causes and consequences. Biochim Biophys Acta 1805, 1:105-117.
10. Navin N, Krasnitz A, Rodgers L, Cook K, Meth J, Kendall J, Riggs M, Eberling Y, Troge J, Grubor V, et al. Inferring tumor progression from genomic heterogeneity. Genome Res 2010, 20(1):68-80. 10.1101/gr.099622.109, 2798832, 19903760.
11. Zhang FF, Murata-Collins JL, Gaytan P, Forman SJ, Kopecky KJ, Willman CL, Appelbaum FR, Slovak ML. Twenty-four-color spectral karyotyping reveals chromosome aberrations in cytogenetically normal acute myeloid leukemia. Genes Chromosomes Cancer 2000, 28(3):318-328. 10.1002/1098-2264(200007)28:3<318::AID-GCC10>3.0.CO;2-M, 10862038.
12. Hicks DG, Tubbs RR. Assessment of the HER2 status in breast cancer by fluorescence in situ hybridization: a technical review with interpretive guidelines. Hum Pathol 2005, 36(3):250-261. 10.1016/j.humpath.2004.11.010, 15791569.
13. Pinkel D, Segraves R, Sudar D, Clark S, Poole I, Kowbel D, Collins C, Kuo WL, Chen C, Zhai Y, et al. High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nat Genet 1998, 20(2):207-211. 10.1038/2524, 9771718.
14. Ishkanian AS, Malloff CA, Watson SK, DeLeeuw RJ, Chi B, Coe BP, Snijders A, Albertson DG, Pinkel D, Marra MA, et al. A tiling resolution DNA microarray with complete coverage of the human genome. Nat Genet 2004, 36(3):299-303. 10.1038/ng1307, 14981516.
15. Kallioniemi A, Kallioniemi OP, Sudar D, Rutovitz D, Gray JW, Waldman F, Pinkel D. Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors. Science 1992, 258(5083):818-821. 10.1126/science.1359641, 1359641.
16. Pierotti MA, Santoro M, Jenkins RB, Sozzi G, Bongarzone I, Grieco M, Monzini N, Miozzo M, Herrmann MA, Fusco 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 1992, 89(5):1616-1620. 10.1073/pnas.89.5.1616, 48503, 1542652.
17. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, Fujiwara S, Watanabe H, Kurashina K, Hatanaka H, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007, 448(7153):561-566. 10.1038/nature05945, 17625570.
18. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005, 310(5748):644-648. 10.1126/science.1117679, 16254181.
19. Hajirasouliha I, Hormozdiari F, Alkan C, Kidd JM, Birol I, Eichler EE, Sahinalp SC. Detection and characterization of novel sequence insertions using paired-end next-generation sequencing. Bioinformatics 2010, 26(10):1277-1283. 10.1093/bioinformatics/btq152, 2865866, 20385726.
20. Liu G, Gramling S, Munoz D, Cheng D, Azad AK, Mirshams M, Chen Z, Xu W, Roberts H, Shepherd FA, et al. Two novel BRM insertion promoter sequence variants are associated with loss of BRM expression and lung cancer risk. Oncogene 2011, 30(29):3295-3304. 10.1038/onc.2011.81, 3400140, 21478907.
21. Bailey JA, Eichler EE. Primate segmental duplications: crucibles of evolution, diversity and disease. Nat Rev Genet 2006, 7(7):552-564. 10.1038/nrg1895, 16770338.
22. Mefford HC, Eichler EE. Duplication hotspots, rare genomic disorders, and common disease. Curr Opin Genet Dev 2009, 19(3):196-204. 10.1016/j.gde.2009.04.003, 2746670, 19477115.
23. Alkan C, Coe BP, Eichler EE. Genome structural variation discovery and genotyping. Nat Rev Genet 2011, 12(5):363-376. 10.1038/nrg2958, 21358748.
24. Wood LD, Parsons DW, Jones S, Lin J, Sjoblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, et al. The genomic landscapes of human breast and colorectal cancers. Science 2007, 318(5853):1108-1113. 10.1126/science.1145720, 17932254.
25. Stephens P, Edkins S, Davies H, Greenman C, Cox C, Hunter C, Bignell G, Teague J, Smith R, Stevens C, et al. A screen of the complete protein kinase gene family identifies diverse patterns of somatic mutations in human breast cancer. Nat Genet 2005, 37(6):590-592. 10.1038/ng1571, 15908952.
26. Bardelli A, Parsons DW, Silliman N, Ptak J, Szabo S, Saha S, Markowitz S, Willson JK, Parmigiani G, Kinzler KW, et al. Mutational analysis of the tyrosine kinome in colorectal cancers. Science 2003, 300(5621):949. 10.1126/science.1082596, 12738854.
27. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, Herman P, Kaye FJ, Lindeman N, Boggon TJ, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004, 304(5676):1497-1500. 10.1126/science.1099314, 15118125.
28. Shah SP, Roth A, Goya R, Oloumi A, Ha G, Zhao Y, Turashvili G, Ding J, Tse K, Haffari G, et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012, 486(7403):395-399.
29. Sjoblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, et al. The consensus coding sequences of human breast and colorectal cancers. Science 2006, 314(5797):268-274. 10.1126/science.1133427, 16959974.
30. Bettegowda C, Agrawal N, Jiao Y, Sausen M, Wood LD, Hruban RH, Rodriguez FJ, Cahill DP, McLendon R, Riggins G, et al. Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 2011, 333(6048):1453-1455. 10.1126/science.1210557, 3170506, 21817013.
31. Agrawal N, Frederick MJ, Pickering CR, Bettegowda C, Chang K, Li RJ, Fakhry C, Xie TX, Zhang J, Wang J, et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 2011, 333(6046):1154-1157. 10.1126/science.1206923, 3162986, 21798897.
32. Network CGAR. Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474(7353):609-615. 10.1038/nature10166, 3163504, 21720365.
33. Chapman MA, Lawrence MS, Keats JJ, Cibulskis K, Sougnez C, Schinzel AC, Harview CL, Brunet JP, Ahmann GJ, Adli M, et al. Initial genome sequencing and analysis of multiple myeloma. Nature 2011, 471(7339):467-472. 10.1038/nature09837, 3560292, 21430775.
34. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS, Ritchey JK, Young MA, Lamprecht T, McLellan MD, et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012, 481(7382):506-510. 10.1038/nature10738, 3267864, 22237025.
35. Ding L, Ellis MJ, Li S, Larson DE, Chen K, Wallis JW, Harris CC, McLellan MD, Fulton RS, Fulton LL, et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010, 464(7291):999-1005. 10.1038/nature08989, 2872544, 20393555.
36. Lee W, Jiang Z, Liu J, Haverty PM, Guan Y, Stinson J, Yue P, Zhang Y, Pant KP, Bhatt D, et al. The mutation spectrum revealed by paired genome sequences from a lung cancer patient. Nature 2010, 465(7297):473-477. 10.1038/nature09004, 20505728.
37. Ley TJ, Mardis ER, Ding L, Fulton B, McLellan MD, Chen K, Dooling D, Dunford-Shore BH, McGrath S, Hickenbotham M, et al. DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature 2008, 456(7218):66-72. 10.1038/nature07485, 2603574, 18987736.
38. Pleasance ED, Cheetham RK, Stephens PJ, McBride DJ, Humphray SJ, Greenman CD, Varela I, Lin ML, Ordonez GR, Bignell GR, et al. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 2010, 463(7278):191. 10.1038/nature08658, 3145108, 20016485.
39. Pleasance ED, Stephens PJ, O'Meara S, McBride DJ, Meynert A, Jones D, Lin ML, Beare D, Lau KW, Greenman C, et al. A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 2010, 463(7278):184-190. 10.1038/nature08629, 2880489, 20016488.
40. Shah SP, Morin RD, Khattra J, Prentice L, Pugh T, Burleigh A, Delaney A, Gelmon K, Guliany R, Senz J, et al. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 2009, 461(7265):809-813. 10.1038/nature08489, 19812674.
41. Mills RE, Walter K, Stewart C, Handsaker RE, Chen K, Alkan C, Abyzov A, Yoon SC, Ye K, Cheetham RK, et al. Mapping copy number variation by population-scale genome sequencing. Nature 2011, 470(7332):59-65. 10.1038/nature09708, 3077050, 21293372.
42. Alkan C, Sajjadian S, Eichler EE. Limitations of next-generation genome sequence assembly. Nat Methods 2011, 8(1):61-65. 10.1038/nmeth.1527, 3115693, 21102452.
43. Consortium GP. A map of human genome variation from population-scale sequencing. Nature 2010, 467(7319):1061-1073. 10.1038/nature09534, 3042601, 20981092.
44. Medvedev P, Stanciu M, Brudno M. Computational methods for discovering structural variation with next-generation sequencing. Nat Methods 2009, 6(11 Suppl):S13-S20.
45. Reslewic S, Zhou S, Place M, Zhang Y, Briska A, Goldstein S, Churas C, Runnheim R, Forrest D, Lim A, et al. Whole-genome shotgun Optical Mapping of Rhodospirillum rubrum. Appl Environ Microbiol 2005, 71(9):5511-5522. 10.1128/AEM.71.9.5511-5522.2005, 1214604, 16151144.
46. Lai Z, Jing J, Aston C, Clarke V, Apodaca J, Dimalanta ET, Carucci DJ, Gardner MJ, Mishra B, Anantharaman TS, et al. A shotgun optical map of the entire Plasmodium falciparum genome. Nat Genet 1999, 23(3):309-313. 10.1038/15484, 10610179.
47. Lin J, Qi R, Aston C, Jing J, Anantharaman TS, Mishra B, White O, Daly MJ, Minton KW, Venter JC, et al. Whole-genome shotgun Optical Mapping of Deinococcus radiodurans. Science 1999, 285(5433):1558-1562. 10.1126/science.285.5433.1558, 10477518.
48. Schwartz DC, Li X, Hernandez LI, Ramnarain SP, Huff EJ, Wang YK. Ordered restriction maps of Saccharomyces cerevisiae chromosomes constructed by Optical Mapping. Science 1993, 262(5130):110-114. 10.1126/science.8211116, 8211116.
49. Young ND, Debelle F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H, et al. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 2011, 480(7378):520-524. 3272368, 22089132.
50. Zhou S, Wei F, Nguyen J, Bechner M, Potamousis K, Goldstein S, Pape L, Mehan MR, Churas C, Pasternak S, et al. A single molecule scaffold for the maize genome. PLoS Genet 2009, 5(11):e1000711. 10.1371/journal.pgen.1000711, 2774507, 19936062.
51. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, et al. The B73 maize genome: complexity, diversity, and dynamics. Science 2009, 326(5956):1112-1115. 10.1126/science.1178534, 19965430.
52. Zhou S, Bechner MC, Place M, Churas CP, Pape L, Leong SA, Runnheim R, Forrest DK, Goldstein S, Livny M, et al. Validation of rice genome sequence by Optical Mapping. BMC Genomics 2007, 8:278. 10.1186/1471-2164-8-278, 2048515, 17697381.
53. Kidd JM, Cooper GM, Donahue WF, Hayden HS, Sampas N, Graves T, Hansen N, Teague B, Alkan C, Antonacci F, et al. Mapping and sequencing of structural variation from eight human genomes. Nature 2008, 453(7191):56-64. 10.1038/nature06862, 2424287, 18451855.
54. Zody MC, Garber M, Adams DJ, Sharpe T, Harrow J, Lupski JR, Nicholson C, Searle SM, Wilming L, Young SK, et al. DNA sequence of human chromosome 17 and analysis of rearrangement in the human lineage. Nature 2006, 440(7087):1045-1049. 10.1038/nature04689, 2610434, 16625196.
55. Ananiev GE, Goldstein S, Runnheim R, Forrest DK, Zhou S, Potamousis K, Churas CP, Bergendahl V, Thomson JA, Schwartz DC. Optical Mapping discerns genome wide DNA methylation profiles. BMC Mol Biol 2008, 9:68. 10.1186/1471-2199-9-68, 2516518, 18667073.
56. Teague B, Waterman MS, Goldstein S, Potamousis K, Zhou S, Reslewic S, Sarkar D, Valouev A, Churas C, Kidd JM, et al. High-resolution human genome structure by single-molecule analysis. Proc Natl Acad Sci USA 2010, 107(24):10848-10853. 10.1073/pnas.0914638107, 2890719, 20534489.
57. Church DM, Goodstadt L, Hillier LW, Zody MC, Goldstein S, She X, Bult CJ, Agarwala R, Cherry JL, DiCuccio M, et al. Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol 2009, 7(5):e1000112. 10.1371/journal.pbio.1000112, 2680341, 19468303.
58. DeAngelis LM. Brain tumors. N Engl J Med 2001, 344(2):114-123. 10.1056/NEJM200101113440207, 11150363.
59. Reifenberger G, Louis DN. Oligodendroglioma: toward molecular definitions in diagnostic neuro-oncology. J Neuropathol Exp Neurol 2003, 62(2):111-126.
60. Cairncross G, Jenkins R. Gliomas with 1p/19q codeletion: a.k.a. oligodendroglioma. Cancer J 2008, 14(6):352-357. 10.1097/PPO.0b013e31818d8178, 19060598.
61. Cairncross JG, Ueki K, Zlatescu MC, Lisle DK, Finkelstein DM, Hammond RR, Silver JS, Stark PC, Macdonald DR, Ino Y, et al. Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst 1998, 90(19):1473-1479. 10.1093/jnci/90.19.1473, 9776413.
62. Walker C, du Plessis DG, Joyce KA, Fildes D, Gee A, Haylock B, Husband D, Smith T, Broome J, Warnke PC. Molecular pathology and clinical characteristics of oligodendroglial neoplasms. Ann Neurol 2005, 57(6):855-865. 10.1002/ana.20496, 15929038.
63. Bromberg JE, van den Bent MJ. Oligodendrogliomas: molecular biology and treatment. Oncologist 2009, 14(2):155-163. 10.1634/theoncologist.2008-0248, 19182242.
64. Wharton SB, Maltby E, Jellinek DA, Levy D, Atkey N, Hibberd S, Crimmins D, Stoeber K, Williams GH. Subtypes of oligodendroglioma defined by 1p,19q deletions, differ in the proportion of apoptotic cells but not in replication-licensed non-proliferating cells. Acta Neuropathol 2007, 113(2):119-127. 10.1007/s00401-006-0177-2, 1781098, 17160531.
65. van den Bent MJ, Looijenga LH, Langenberg K, Dinjens W, Graveland W, Uytdewilligen L, Sillevis Smitt PA, Jenkins RB, Kros JM. Chromosomal anomalies in oligodendroglial tumors are correlated with clinical features. Cancer 2003, 97(5):1276-1284. 10.1002/cncr.11187, 12599236.
66. Dimalanta ET, Lim A, Runnheim R, Lamers C, Churas C, Forrest DK, de Pablo JJ, Graham MD, Coppersmith SN, Goldstein S, et al. A microfluidic system for large DNA molecule arrays. Anal Chem 2004, 76(18):5293-5301. 10.1021/ac0496401, 15362885.
67. Valouev A, Li L, Liu YC, Schwartz DC, Yang Y, Zhang Y, Waterman MS. Alignment of optical maps. J Comput Biol 2006, 13(2):442-462. 10.1089/cmb.2006.13.442, 16597251.
68. Sarkar D. On the analysis of Optical Mapping data 2006, Madison, WI: University of Wisconsin.
69. Sarkar D, Goldstein S, Schwartz DC, Newton MA. Statistical significance of optical map alignments. J Comput Biol 2012, 19(5):478-492. 10.1089/cmb.2011.0221, 3342520, 22506568.
70. Griffin CA, Burger P, Morsberger L, Yonescu R, Swierczynski S, Weingart JD, Murphy KM. Identification of der(1;19)(q10;p10) in five oligodendrogliomas suggests mechanism of concurrent 1p and 19q loss. J Neuropathol Exp Neurol 2006, 65(10):988-994. 10.1097/01.jnen.0000235122.98052.8f, 17021403.
71. Jenkins RB, Blair H, Ballman KV, Giannini C, Arusell RM, Law M, Flynn H, Passe S, Felten S, Brown PD, et al. A t(1;19)(q10;p10) mediates the combined deletions of 1p and 19q and predicts a better prognosis of patients with oligodendroglioma. Cancer Res 2006, 66(20):9852-9861. 10.1158/0008-5472.CAN-06-1796, 17047046.
72. Anderson K, Lutz C, van Delft FW, Bateman CM, Guo Y, Colman SM, Kempski H, Moorman AV, Titley I, Swansbury J, et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 2011, 469(7330):356-361. 10.1038/nature09650, 21160474.
73. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, Stewart A, Tarpey P, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012, 366(10):883-892. 10.1056/NEJMoa1113205, 22397650.
74. Yap TA, Gerlinger M, Futreal PA, Pusztai L, Swanton C. Intratumor heterogeneity: seeing the wood for the trees. Sci Transl Med 2012, 4(127):127-110.
75. Wicks SR, Yeh RT, Gish WR, Waterston RH, Plasterk RH. Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 2001, 28(2):160-164. 10.1038/88878, 11381264.
76. Macintyre G, Alford T, Xiong L, Rouleau GA, Tibbo PG, Cox DW. Association of NPAS3 exonic variation with schizophrenia. Schizophr Res 2010, 120(1-3):143-149.
77. Pickard BS, Christoforou A, Thomson PA, Fawkes A, Evans KL, Morris SW, Porteous DJ, Blackwood DH, Muir WJ. Interacting haplotypes at the NPAS3 locus alter risk of schizophrenia and bipolar disorder. Mol Psychiatry 2009, 14(9):874-884. 10.1038/mp.2008.24, 18317462.
78. Moreira F, Kiehl TR, So K, Ajeawung NF, Honculada C, Gould P, Pieper RO, Kamnasaran D. NPAS3 demonstrates features of a tumor suppressive role in driving the progression of Astrocytomas. Am J Pathol 2011, 179(1):462-476. 10.1016/j.ajpath.2011.03.044, 3123785, 21703424.
79. Lehto M, Olkkonen VM. The OSBP-related proteins: a novel protein family involved in vesicle transport, cellular lipid metabolism, and cell signalling. Biochim Biophys Acta 2003, 1631(1):1-11. 10.1016/S1388-1981(02)00364-5, 12573443.
80. Lehto M, Tienari J, Lehtonen S, Lehtonen E, Olkkonen VM. Subfamily III of mammalian oxysterol-binding protein (OSBP) homologues: the expression and intracellular localization of ORP3, ORP6, and ORP7. Cell Tissue Res 2004, 315(1):39-57. 10.1007/s00441-003-0817-y, 14593528.
81. Lehto M, Mayranpaa MI, Pellinen T, Ihalmo P, Lehtonen S, Kovanen PT, Groop PH, Ivaska J, Olkkonen VM. The R-Ras interaction partner ORP3 regulates cell adhesion. J Cell Sci 2008, 121(Pt 5):695-705.
82. Sander B, Flygare J, Porwit-Macdonald A, Smith CI, Emanuelsson E, Kimby E, Liden J, Christensson B. Mantle cell lymphomas with low levels of cyclin D1 long mRNA transcripts are highly proliferative and can be discriminated by elevated cyclin A2 and cyclin B1. Int J Cancer 2005, 117(3):418-430. 10.1002/ijc.21166, 15900590.
83. Ek S, Andreasson U, Hober S, Kampf C, Ponten F, Uhlen M, Merz H, Borrebaeck CA. From gene expression analysis to tissue microarrays: a rational approach to identify therapeutic and diagnostic targets in lymphoid malignancies. Mol Cell Proteomics 2006, 5(6):1072-1081. 10.1074/mcp.M600077-MCP200, 16524965.
84. Bijl J, Sauvageau M, Thompson A, Sauvageau G. High incidence of proviral integrations in the Hoxa locus in a new model of E2a-PBX1-induced B-cell leukemia. Genes Dev 2005, 19(2):224-233. 10.1101/gad.1268505, 545883, 15655112.
85. Abbas N, Lucking CB, Ricard S, Durr A, Bonifati V, De Michele G, Bouley S, Vaughan JR, Gasser T, Marconi R, et al. A wide variety of mutations in the parkin gene are responsible for autosomal recessive parkinsonism in Europe. French Parkinson's Disease Genetics Study Group and the European Consortium on Genetic Susceptibility in Parkinson's Disease. Hum Mol Genet 1999, 8(4):567-574. 10.1093/hmg/8.4.567, 10072423.
86. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998, 392(6676):605-608. 10.1038/33416, 9560156.
87. Lucking CB, Durr A, Bonifati V, Vaughan J, De Michele G, Gasser T, Harhangi BS, Meco G, Denefle P, Wood NW, et al. Association between early-onset Parkinson's disease and mutations in the parkin gene. N Engl J Med 2000, 342(21):1560-1567. 10.1056/NEJM200005253422103, 10824074.
88. Veeriah S, Taylor BS, Meng S, Fang F, Yilmaz E, Vivanco I, Janakiraman M, Schultz N, Hanrahan AJ, Pao W, et al. Somatic mutations of the Parkinson's disease-associated gene PARK2 in glioblastoma and other human malignancies. Nat Genet 2010, 42(1):77-82. 10.1038/ng.491, 19946270.
89. Cesari R, Martin ES, Calin GA, Pentimalli F, Bichi R, McAdams H, Trapasso F, Drusco A, Shimizu M, Masciullo V, et al. Parkin, a gene implicated in autosomal recessive juvenile parkinsonism, is a candidate tumor suppressor gene on chromosome 6q25-q27. Proc Natl Acad Sci USA 2003, 100(10):5956-5961. 10.1073/pnas.0931262100, 156308, 12719539.
90. Denison SR, Wang F, Becker NA, Schule B, Kock N, Phillips LA, Klein C, Smith DI. Alterations in the common fragile site gene Parkin in ovarian and other cancers. Oncogene 2003, 22(51):8370-8378. 10.1038/sj.onc.1207072, 14614460.
91. Fujiwara M, Marusawa H, Wang HQ, Iwai A, Ikeuchi K, Imai Y, Kataoka A, Nukina N, Takahashi R, Chiba T. Parkin as a tumor suppressor gene for hepatocellular carcinoma. Oncogene 2008, 27(46):6002-6011. 10.1038/onc.2008.199, 18574468.
92. Poulogiannis G, McIntyre RE, Dimitriadi M, Apps JR, Wilson CH, Ichimura K, Luo F, Cantley LC, Wyllie AH, Adams DJ, et al. PARK2 deletions occur frequently in sporadic colorectal cancer and accelerate adenoma development in Apc mutant mice. Proc Natl Acad Sci USA 2010, 107(34):15145-15150. 10.1073/pnas.1009941107, 2930574, 20696900.
93. Wang F, Denison S, Lai JP, Philips LA, Montoya D, Kock N, Schule B, Klein C, Shridhar V, Roberts LR, et al. Parkin gene alterations in hepatocellular carcinoma. Genes Chromosomes Cancer 2004, 40(2):85-96. 10.1002/gcc.20020, 15101042.
94. Picchio MC, Martin ES, Cesari R, Calin GA, Yendamuri S, Kuroki T, Pentimalli F, Sarti M, Yoder K, Kaiser LR, et al. Alterations of the tumor suppressor gene Parkin in non-small cell lung cancer. Clin Cancer Res 2004, 10(8):2720-2724. 10.1158/1078-0432.CCR-03-0086, 15102676.
95. Kahkonen M. Population cytogenetics of folate-sensitive fragile sites. I. Common fragile sites. Hum Genet 1988, 80(4):344-348. 10.1007/BF00273649, 3198111.
96. Ren Y, Jiang H, Yang F, Nakaso K, Feng J. Parkin protects dopaminergic neurons against microtubule-depolymerizing toxins by attenuating microtubule-associated protein kinase activation. J Biol Chem 2009, 284(6):4009-4017. 2635057, 19074146.
97. Wang H, Liu B, Zhang C, Peng G, Liu M, Li D, Gu F, Chen Q, Dong JT, Fu L, et al. Parkin regulates paclitaxel sensitivity in breast cancer via a microtubule-dependent mechanism. J Pathol 2009, 218(1):76-85. 10.1002/path.2512, 19214989.
98. Yang F, Jiang Q, Zhao J, Ren Y, Sutton MD, Feng J. Parkin stabilizes microtubules through strong binding mediated by three independent domains. J Biol Chem 2005, 280(17):17154-17162. 10.1074/jbc.M500843200, 15737990.
99. Manna T, Grenningloh G, Miller HP, Wilson L. Stathmin family protein SCG10 differentially regulates the plus and minus end dynamics of microtubules at steady state in vitro: implications for its role in neurite outgrowth. Biochemistry 2007, 46(11):3543-3552. 10.1021/bi061819d, 17311410.
100. Lee HS, Lee DC, Park MH, Yang SJ, Lee JJ, Kim DM, Jang Y, Lee JH, Choi JY, Kang YK, et al. STMN2 is a novel target of beta-catenin/TCF-mediated transcription in human hepatoma cells. Biochem Biophys Res Commun 2006, 345(3):1059-1067. 10.1016/j.bbrc.2006.05.017, 16712787.
101. Riederer BM, Pellier V, Antonsson B, Di Paolo G, Stimpson SA, Lutjens R, Catsicas S, Grenningloh G. Regulation of microtubule dynamics by the neuronal growth-associated protein SCG10. Proc Natl Acad Sci USA 1997, 94(2):741-745. 10.1073/pnas.94.2.741, 19584, 9012855.
102. Ngo TT, Peng T, Liang XJ, Akeju O, Pastorino S, Zhang W, Kotliarov Y, Zenklusen JC, Fine HA, Maric D, et al. The 1p-encoded protein stathmin and resistance of malignant gliomas to nitrosoureas. J Natl Cancer Inst 2007, 99(8):639-652. 10.1093/jnci/djk135, 17440165.
103. Liang XJ, Choi Y, Sackett DL, Park JK. Nitrosoureas inhibit the stathmin-mediated migration and invasion of malignant glioma cells. Cancer Res 2008, 68(13):5267-5272. 10.1158/0008-5472.CAN-07-6482, 2493613, 18593927.
104. Alli E, Bash-Babula J, Yang JM, Hait WN. Effect of stathmin on the sensitivity to antimicrotubule drugs in human breast cancer. Cancer Res 2002, 62(23):6864-6869.
105. Alli E, Yang JM, Hait WN. Silencing of stathmin induces tumor-suppressor function in breast cancer cell lines harboring mutant p53. Oncogene 2007, 26(7):1003-1012. 10.1038/sj.onc.1209864, 16909102.
106. Mistry SJ, Atweh GF. Therapeutic interactions between stathmin inhibition and chemotherapeutic agents in prostate cancer. Mol Cancer Ther 2006, 5(12):3248-3257. 10.1158/1535-7163.MCT-06-0227, 17172428.
107. Muller FL, Colla S, Aquilanti E, Manzo VE, Genovese G, Lee J, Eisenson D, Narurkar R, Deng P, Nezi L, et al. Passenger deletions generate therapeutic vulnerabilities in cancer. Nature 2012, 488(7411):337-342. 10.1038/nature11331, 3712624, 22895339.
108. Nijhawan D, Zack TI, Ren Y, Strickland MR, Lamothe R, Schumacher SE, Tsherniak A, Besche HC, Rosenbluh J, Shehata S, et al. Cancer vulnerabilities unveiled by genomic loss. Cell 2012, 150(4):842-854. 10.1016/j.cell.2012.07.023, 22901813.
109. Hanein S, Martin E, Boukhris A, Byrne P, Goizet C, Hamri A, Benomar A, Lossos A, Denora P, Fernandez J, et al. Identification of the SPG15 gene, encoding spastizin, as a frequent cause of complicated autosomal-recessive spastic paraplegia, including Kjellin syndrome. Am J Hum Genet 2008, 82(4):992-1002. 10.1016/j.ajhg.2008.03.004, 2427184, 18394578.
110. Sagona AP, Nezis IP, Bache KG, Haglund K, Bakken AC, Skotheim RI, Stenmark H. A tumor-associated mutation of FYVE-CENT prevents its interaction with Beclin 1 and interferes with cytokinesis. PLoS One 2011, 6(3):e17086. 10.1371/journal.pone.0017086, 3063775, 21455500.
111. Sagona AP, Nezis IP, Pedersen NM, Liestol K, Poulton J, Rusten TE, Skotheim RI, Raiborg C, Stenmark H. PtdIns(3)P controls cytokinesis through KIF13A-mediated recruitment of FYVE-CENT to the midbody. Nat Cell Biol 2010, 12(4):362-371. 10.1038/ncb2036, 20208530.
112. Pober BR. Williams-Beuren syndrome. N Engl J Med 2010, 362(3):239-252. 10.1056/NEJMra0903074, 20089974.
113. Hobart HH, Morris CA, Mervis CB, Pani AM, Kistler DJ, Rios CM, Kimberley KW, Gregg RG, Bray-Ward P. Inversion of the Williams syndrome region is a common polymorphism found more frequently in parents of children with Williams syndrome. Am J Med Genet C Semin Med Genet 2010, 154C(2):220-228. 10.1002/ajmg.c.30258, 2946898, 20425783.
114. Osborne LR, Li M, Pober B, Chitayat D, Bodurtha J, Mandel A, Costa T, Grebe T, Cox S, Tsui LC, et al. A 1.5 million-base pair inversion polymorphism in families with Williams-Beuren syndrome. Nat Genet 2001, 29(3):321-325. 10.1038/ng753, 2889916, 11685205.
115. Tam E, Young EJ, Morris CA, Marshall CR, Loo W, Scherer SW, Mervis CB, Osborne LR. The common inversion of the Williams-Beuren syndrome region at 7q11.23 does not cause clinical symptoms. Am J Med Genet A 2008, 146A(14):1797-1806. 10.1002/ajmg.a.32360, 2886033, 18553513.
116. Aso T, Lane WS, Conaway JW, Conaway RC. Elongin (SIII): a multisubunit regulator of elongation by RNA polymerase II. Science 1995, 269(5229):1439-1443. 10.1126/science.7660129, 7660129.
117. Conaway JW, Bradsher JN, Tan S, Conaway RC. Transcription factor SIII: a novel component of the RNA polymerase II elongation complex. Cell Mol Biol Res 1993, 39(4):323-329.
118. Bradsher JN, Jackson KW, Conaway RC, Conaway JW. RNA polymerase II transcription factor SIII. I. Identification, purification, and properties. J Biol Chem 1993, 268(34):25587-25593.
119. Kamura T, Burian D, Yan Q, Schmidt SL, Lane WS, Querido E, Branton PE, Shilatifard A, Conaway RC, Conaway JW. Muf1, a novel Elongin BC-interacting leucine-rich repeat protein that can assemble with Cul5 and Rbx1 to reconstitute a ubiquitin ligase. J Biol Chem 2001, 276(32):29748-29753. 10.1074/jbc.M103093200, 11384984.
120. Yasukawa T, Kamura T, Kitajima S, Conaway RC, Conaway JW, Aso T. Mammalian Elongin A complex mediates DNA-damage-induced ubiquitylation and degradation of Rpb1. EMBO J 2008, 27(24):3256-3266. 10.1038/emboj.2008.249, 2609743, 19037258.
121. Barr FG. Chromosomal translocations involving paired box transcription factors in human cancer. Int J Biochem Cell Biol 1997, 29(12):1449-1461. 10.1016/S1357-2725(97)00095-2, 9570138.
122. Buckingham M, Relaix F. The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu Rev Cell Dev Biol 2007, 23:645-673. 10.1146/annurev.cellbio.23.090506.123438, 17506689.
123. Murdoch B, Delconte C, Garcia-Castro MI. Pax7 lineage contributions to the Mammalian neural crest. PLoS One 2012, 7(7):e41089. 10.1371/journal.pone.0041089, 3407174, 22848431.
124. Davis RJ, D'Cruz CM, Lovell MA, Biegel JA, Barr FG. Fusion of PAX7 to FKHR by the variant t(1;13)(p36;q14) translocation in alveolar rhabdomyosarcoma. Cancer Res 1994, 54(11):2869-2872.
125. Bennicelli JL, Advani S, Schafer BW, Barr FG. PAX3 and PAX7 exhibit conserved cis-acting transcription repression domains and utilize a common gain of function mechanism in alveolar rhabdomyosarcoma. Oncogene 1999, 18(30):4348-4356. 10.1038/sj.onc.1202812, 10439042.
126. Matsuda M, Kobayashi Y, Masuda S, Adachi M, Watanabe T, Yamashita JK, Nishi E, Tsukita S, Furuse M. Identification of adherens junction-associated GTPase activating proteins by the fluorescence localization-based expression cloning. Exp Cell Res 2008, 314(5):939-949. 10.1016/j.yexcr.2007.11.009, 18241859.
127. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321(5897):1807-1812. 10.1126/science.1164382, 2820389, 18772396.
128. Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, et al. The genetic landscape of the childhood cancer medulloblastoma. Science 2011, 331(6016):435-439. 10.1126/science.1198056, 3110744, 21163964.
129. Grasso CS, Wu YM, Robinson DR, Cao X, Dhanasekaran SM, Khan AP, Quist MJ, Jing X, Lonigro RJ, Brenner JC, et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012, 487(7406):239-243. 10.1038/nature11125, 3396711, 22722839.
130. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321(5897):1801-1806. 10.1126/science.1164368, 2848990, 18772397.
131. Berger MF, Hodis E, Heffernan TP, Deribe YL, Lawrence MS, Protopopov A, Ivanova E, Watson IR, Nickerson E, Ghosh P, et al. Melanoma genome sequencing reveals frequent PREX2 mutations. Nature 2012, 485(7399):502-506. 3367798, 22622578.
132. Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489(7414):57-74. 10.1038/nature11247, 3439153, 22955616.
133. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 2011, 473(7345):43-49. 10.1038/nature09906, 3088773, 21441907.
134. Kalyana-Sundaram S, Kumar-Sinha C, Shankar S, Robinson DR, Wu YM, Cao X, Asangani IA, Kothari V, Prensner JR, Lonigro RJ, et al. Expressed pseudogenes in the transcriptional landscape of human cancers. Cell 2012, 149(7):1622-1634. 10.1016/j.cell.2012.04.041, 3597446, 22726445.
135. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129(7):1311-1323. 10.1016/j.cell.2007.05.022, 2084369, 17604720.
136. Forbes SA, Bhamra G, Bamford S, Dawson E, Kok C, Clements J, Menzies A, Teague JW, Futreal PA, Stratton MR. The Catalogue of Somatic Mutations in Cancer (COSMIC). Curr Protoc Hum Genet 2008, 10:10-11.
137. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, Jia M, Shepherd R, Leung K, Menzies A, et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 2011, 39:945-950.
138. Sun L, Hui AM, Su Q, Vortmeyer A, Kotliarov Y, Pastorino S, Passaniti A, Menon J, Walling J, Bailey R, et al. Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell 2006, 9(4):287-300. 10.1016/j.ccr.2006.03.003, 16616334.
139. Edgar R, Domrachev M, Lash AE. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30(1):207-210. 10.1093/nar/30.1.207, 99122, 11752295.
140. Yuan M, Kendziorski C. A unified approach for simultaneous gene clustering and differential expression identification. Biometrics 2006, 62(4):1089-1098. 10.1111/j.1541-0420.2006.00611.x, 17156283.
141. Bauer S, Grossmann S, Vingron M, Robinson PN. Ontologizer 2.0-a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics 2008, 24(14):1650-1651. 10.1093/bioinformatics/btn250, 18511468.
142. Zhang B, Kirov S, Snoddy J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res 2005, 33:W741-W748. 10.1093/nar/gki475, 1160236, 15980575.
143. Wuchty S, Arjona D, Bozdag S, Bauer PO. Involvement of microRNA families in cancer. Nucleic Acids Res 2012, 40(17):8219-8226. 10.1093/nar/gks627, 3458565, 22743268.
144. Coons SW, Johnson PC, Scheithauer BW, Yates AJ, Pearl DK. Improving diagnostic accuracy and interobserver concordance in the classification and grading of primary gliomas. Cancer 1997, 79(7):1381-1393. 10.1002/(SICI)1097-0142(19970401)79:7<1381::AID-CNCR16>3.0.CO;2-W, 9083161.
145. Reis-Filho JS, Faoro LN, Carrilho C, Bleggi-Torres LF, Schmitt FC. Evaluation of cell proliferation, epidermal growth factor receptor, and bcl-2 immunoexpression as prognostic factors for patients with World Health Organization grade 2 oligodendroglioma. Cancer 2000, 88(4):862-869. 10.1002/(SICI)1097-0142(20000215)88:4<862::AID-CNCR17>3.0.CO;2-G, 10679656.
146. VanDevanter DR, Yirdaw G, Do C, Tysseling KA, Drescher CA, Forseth BJ, Von Hoff DD, McNutt MA. Preparation of uniform, intact DNA samples from resected tumor tissues for pulsed-field gel electrophoretic analyses. Biotechniques 1992, 13(6):884-887.
147. Lim A, Dimalanta ET, Potamousis KD, Yen G, Apodoca J, Tao C, Lin J, Qi R, Skiadas J, Ramanathan A, et al. Shotgun optical maps of the whole Escherichia coli O157:H7 genome. Genome Res 2001, 11(9):1584-1593. 10.1101/gr.172101, 311123, 11544203.
148. Lim A. Single molecule systems: Advancements and applications to microbial and human genome analysis 2004, PhD Thesis. University of Wisconsin-Madison.
149. Reslewic S. The Optical Mapping of genomes: Gaining new insights on genomic structure and variation by single DNA molecule analysis 2005, PhD Thesis. University of Wisconsin-Madison.
150. Zhou S, Herschleb J, Schwartz DC. Optical Mapping: a single molecule system for genome analysis. New methods for DNA sequencing 2007, 265-300.
151. Schwartz DC, Cantor CR. Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell 1984, 37(1):67-75. 10.1016/0092-8674(84)90301-5, 6373014.
152. Zhou S, Deng W, Anantharaman TS, Lim A, Dimalanta ET, Wang J, Wu T, Chunhong T, Creighton R, Kile A, et al. A whole-genome shotgun optical map of Yersinia pestis strain KIM. Appl Environ Microbiol 2002, 68(12):6321-6331. 10.1128/AEM.68.12.6321-6331.2002, 134435, 12450857.
153. Anantharaman T, Mishra B, Schwartz D. Genomics via Optical Mapping: III: Contiging genomic DNA. Proc Int Conf Intell Syst Mol Biol 1999, 1999:18-27.
154. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. The human genome browser at UCSC. Genome Res 2002, 12(6):996-1006. 186604, 12045153.
155. Lai W, Choudhary V, Park PJ. CGHweb: a tool for comparing DNA copy number segmentations from multiple algorithms. Bioinformatics 2008, 24(7):1014-1015. 10.1093/bioinformatics/btn067, 2516369, 18296463.
156. Iafrate AJ, Feuk L, Rivera MN, Listewnik ML, Donahoe PK, Qi Y, Scherer SW, Lee C. Detection of large-scale variation in the human genome. Nat Genet 2004, 36(9):949-951. 10.1038/ng1416, 15286789.
157. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 2007, 35:W71-W74. 10.1093/nar/gkm306, 1933133, 17485472.