A Sleeping Beauty mutagenesis screen reveals a tumor suppressor role for Ncoa2/Src-2 in liver cancer

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 21, 2012, Pages

  O'Donnell, Kathryn A ^a,g   Keng, Vincent W ^b,c,d   York, Brian ^e   Reineke, Erin L ^e   Seo, Daekwan ^f   Fan, Danhua ^b,c   Silverstein, Kevin A T ^b,c   Schrum, Christina T ^a   Xie, Wei Rose ^a,e   Mularoni, Loris ^a   Wheelan, Sarah J ^a   Torbenson, Michael S ^a   O'Malley, Bert W ^e   Largaespada, David A ^b,c,d   Boeke, Jef D ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

^g UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Cancer gene identification; Hepatocellular carcinoma; Mouse models of cancer; Myc oncogene

Indexed keywords

DIETHYLNITROSAMINE; MESSENGER RNA; MYC PROTEIN; NUCLEAR RECEPTOR COACTIVATOR 2; ZINC FINGER PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DTNB GENE; FEMALE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE INSERTION; GENE MUTATION; HUMAN; HUMAN CELL; LIVER CANCER; LIVER CARCINOGENESIS; MALE; MOUSE; NCOA2 GENE; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SEQUENCE ANALYSIS; TRANSPOSON; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; ZFX GENE;

ALKYLATING AGENTS; ANIMALS; CARCINOMA, HEPATOCELLULAR; DIETHYLNITROSAMINE; DISEASE MODELS, ANIMAL; DNA MUTATIONAL ANALYSIS; FEMALE; GENES, MYC; GENES, TUMOR SUPPRESSOR; HEK293 CELLS; HUMANS; LIVER NEOPLASMS; MALE; MICE; MICE, NUDE; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; NUCLEAR RECEPTOR COACTIVATOR 2; TRANSPLANTATION, HETEROLOGOUS; TRANSPOSASES;

MUS;

EID: 84861432291     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1115433109     Document Type: Article

References (59)

1. Ivics Z, Hackett PB, Plasterk RH, Izsvák Z (1997) Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91:501-510. (Pubitemid 27508239)
2. Collier LS, Carlson CM, Ravimohan S, Dupuy AJ, Largaespada DA (2005) Cancer gene discovery in solid tumours using transposon-based somatic mutagenesis in the mouse. Nature 436:272-276. (Pubitemid 41021279)
3. Dupuy AJ, Akagi K, Largaespada DA, Copeland NG, Jenkins NA (2005) Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 436:221-226. (Pubitemid 41021267)
4. Collier LS, et al. (2009) Whole-body sleeping beauty mutagenesis can cause penetrant leukemia/lymphoma and rare high-grade glioma without associated embryonic lethality. Cancer Res 69:8429-8437.
5. Keng VW, et al. (2009) A conditional transposon-based insertional mutagenesis screen for genes associated with mouse hepatocellular carcinoma. Nat Biotechnol 27:264-274.
6. Starr TK, et al. (2009) A transposon-based genetic screen in mice identifies genes altered in colorectal cancer. Science 323:1747-1750.
7. Roberts LR (2008) Sorafenib in liver cancer - just the beginning. N Engl J Med 359:420-422.
8. Thorgeirsson SS, Grisham JW (2002) Molecular pathogenesis of human hepatocellular carcinoma. Nat Genet 31:339-346. (Pubitemid 35154440)
9. Buendia MA (2000) Genetics of hepatocellular carcinoma. Semin Cancer Biol 10:185-200. (Pubitemid 30614220)
10. Beer S, et al. (2004) Developmental context determines latency of MYC-induced tumorigenesis. PLoS Biol 2:e332.
11. Felsher DW, Bishop JM (1999) Reversible tumorigenesis by MYC in hematopoietic lineages. Mol Cell 4:199-207. (Pubitemid 29456888)
12. Shachaf CM, et al. (2004) MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer. Nature 431:1112-1117. (Pubitemid 39472236)
13. Zender L, et al. (2006) Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125:1253-1267. (Pubitemid 43929093)
14. Zender L, et al. (2005) Generation and analysis of genetically defined liver carcinomas derived from bipotential liver progenitors. Cold Spring Harb Symp Quant Biol 70:251-261. (Pubitemid 44124879)
15. Zender L, et al. (2008) An oncogenomics-based in vivo RNAi screen identifies tumor suppressors in liver cancer. Cell 135:852-864.
16. Keng VW, et al. (2005) Region-specific saturation germline mutagenesis in mice using the Sleeping Beauty transposon system. Nat Methods 2:763-769. (Pubitemid 41486208)
17. Carlson CM, et al. (2003) Transposon mutagenesis of the mouse germline. Genetics 165:243-256. (Pubitemid 37204070)
18. Horie K, et al. (2003) Characterization of Sleeping Beauty transposition and its application to genetic screening in mice. Mol Cell Biol 23:9189-9207. (Pubitemid 37499807)
19. Vigdal TJ, Kaufman CD, Izsvák Z, Voytas DF, Ivics Z (2002) Common physical properties of DNA affecting target site selection of sleeping beauty and other Tc1/mariner transposable elements. J Mol Biol 323:441-452. (Pubitemid 35283672)
20. García-Caballero T, et al. (2000) Increased expression of growth hormone and prolactin receptors in hepatocellular carcinomas. Endocrine 12:265-271. (Pubitemid 30432243)
21. Chopra AR, et al. (2008) Absence of the SRC-2 coactivator results in a glycogenopathy resembling Von Gierke's disease. Science 322:1395-1399. (Pubitemid 352775254)
22. Jeong JW, et al. (2006) The genomic analysis of the impact of steroid receptor coactivators ablation on hepatic metabolism. Mol Endocrinol 20:1138-1152.
23. Lee JS, et al. (2006) A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 12:410-416.
24. Gehin M, et al. (2002) The function of TIF2/GRIP1 in mouse reproduction is distinct from those of SRC-1 and p/CIP. Mol Cell Biol 22:5923-5937. (Pubitemid 34815840)
25. Fausto N, Campbell JS (2010) Mouse models of hepatocellular carcinoma. Semin Liver Dis 30:87-98.
26. Maeda S, Kamata H, Luo JL, Leffert H, Karin M (2005) IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 121:977-990. (Pubitemid 40884391)
27. Rad R, et al. (2010) PiggyBac transposon mutagenesis: A tool for cancer gene discovery in mice. Science 330:1104-1107.
28. Starr TK, et al. (2011) A Sleeping Beauty transposon-mediated screen identifies murine susceptibility genes for adenomatous polyposis coli (Apc)-dependent intestinal tumorigenesis. Proc Natl Acad Sci USA 108:5765-5770.
29. Loh NY, Nebenius-Oosthuizen D, Blake DJ, Smith AJ, Davies KE (2001) Role of beta-dystrobrevin in nonmuscle dystrophin-associated protein complex-like complexes in kidney and liver. Mol Cell Biol 21:7442-7448. (Pubitemid 32953494)
30. Ceccarini M, et al. (2007) Association of dystrobrevin and regulatory subunit of protein kinase A: A new role for dystrobrevin as a scaffold for signaling proteins. J Mol Biol 371:1174-1187. (Pubitemid 47198261)
31. Yasuda H, Mizuno A, Tamaoki T, Morinaga T (1994) ATBF1, a multiple-homeodomain zinc finger protein, selectively down-regulates AT-rich elements of the human alpha-fetoprotein gene. Mol Cell Biol 14:1395-1401.
32. Kim CJ, et al. (2008) Down-regulation of ATBF1 is a major inactivating mechanism in hepatocellular carcinoma. Histopathology 52:552-559. (Pubitemid 351442655)
33. Galan-Caridad JM, et al. (2007) Zfx controls the self-renewal of embryonic and hematopoietic stem cells. Cell 129:345-357. (Pubitemid 46574969)
34. Arenzana TL, Smith-Raska MR, Reizis B (2009) Transcription factor Zfx controls BCR-induced proliferation and survival of B lymphocytes. Blood 113:5857-5867.
35. Hu G, et al. (2009) A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Genes Dev 23:837-848.
36. Lee HC, Kim M, Wands JR (2006) Wnt/Frizzled signaling in hepatocellular carcinoma. Front Biosci 11:1901-1915. (Pubitemid 43253403)
37. Merle P, et al. (2005) Oncogenic role of the frizzled-7/beta-catenin pathway in hepatocellular carcinoma. J Hepatol 43:854-862. (Pubitemid 41414512)
38. Satoh S, et al. (2000) AXIN1 mutations in hepatocellular carcinomas, and growth suppression in cancer cells by virus-mediated transfer of AXIN1. Nat Genet 24:245-250.
39. de la Roche M, Worm J, Bienz M (2008) The function of BCL9 in Wnt/beta-catenin signaling and colorectal cancer cells. BMC Cancer 8:199.
40. Mani M, et al. (2009) BCL9 promotes tumor progression by conferring enhanced proliferative, metastatic, and angiogenic properties to cancer cells. Cancer Res 69:7577-7586.
41. Busby V, et al. (2004) Alpha-T-catenin is expressed in human brain and interacts with the Wnt signaling pathway but is not responsible for linkage to chromosome 10 in Alzheimer's disease. Neuromolecular Med 5:133-146. (Pubitemid 38596547)
42. Quinlan AR, et al. (2010) Genome-wide mapping and assembly of structural variant breakpoints in the mouse genome. Genome Res 20:623-635.
43. Martinez-Sanz J, et al. (2006) Binding of human centrin 2 to the centrosomal protein hSfi1. FEBS J 273:4504-4515. (Pubitemid 44401601)
44. Downward J (2003) Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3:11-22.
45. Soucek L, et al. (2008) Modelling Myc inhibition as a cancer therapy. Nature 455:679-683.
46. Chou JY, Matern D, Mansfield BC, Chen YT (2002) Type I glycogen storage diseases: Disorders of the glucose-6-phosphatase complex. Curr Mol Med 2:121-143. (Pubitemid 34649836)
47. Mutel E, et al. (2011) Targeted deletion of liver glucose-6 phosphatase mimics glycogen storage disease type 1a including development of multiple adenomas. J Hepatol 54:529-537.
48. Tsubouchi H, Kamibeppu A, Fujisaki K, Nagahama J, Hashimoto S (1980) Hepatic gluconeogenic key enzymes in patients with hepatic cancer. Gastroenterol Jpn 15:564-569. (Pubitemid 11137920)
49. Weber G, Cantero A (1955) Glucose-6-phosphatase activity in normal, pre-cancerous, and neoplastic tissues. Cancer Res 15:105-108.
50. Lee PJ (2002) Glycogen storage disease type I: Pathophysiology of liver adenomas. Eur J Pediatr 161(Suppl 1):S46-S49.
51. Kim W, et al. (2007) Apoptosis-inducing antitumor efficacy of hexokinase II inhibitor in hepatocellular carcinoma. Mol Cancer Ther 6:2554-2562. (Pubitemid 47480421)
52. Pelicano H, Martin DS, Xu RH, Huang P (2006) Glycolysis inhibition for anticancer treatment. Oncogene 25:4633-4646. (Pubitemid 44187614)
53. Kim JW, et al. (2004) Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitation assays. Mol Cell Biol 24:5923-5936.
54. Shim H, et al. (1997) c-Myc transactivation of LDH-A: Implications for tumor metabolism and growth. Proc Natl Acad Sci USA 94:6658-6663. (Pubitemid 27281920)
55. Osthus RC, et al. (2000) Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 275:21797-21800. (Pubitemid 30621745)
56. Rice P, Longden I, Bleasby A (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet 16:276-277.
57. Stabenau A, et al. (2004) The Ensembl core software libraries. Genome Res 14:929-933. (Pubitemid 38660512)
58. Sakurai T, Maeda S, Chang L, Karin M (2006) Loss of hepatic NF-kappa B activity enhances chemical hepatocarcinogenesis through sustained c-Jun N-terminal kinase 1 activation. Proc Natl Acad Sci USA 103:10544-10551. (Pubitemid 44078014)
59. York B, et al. (2010) Reprogramming the posttranslational code of SRC-3 confers a switch in mammalian systems biology. Proc Natl Acad Sci USA 107:11122-11127.