Transposon activation mutagenesis as a screening tool for identifying resistance to cancer therapeutics

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Chen, Li ^a   Stuart, Lynda ^a   Ohsumi, Toshiro K ^a   Burgess, Shawn ^b   Varshney, Gaurav K ^b   Dastur, Anahita ^a   Borowsky, Mark ^a   Benes, Cyril ^a   Lacy Hulbert, Adam ^a   Schmidt, Emmett V ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

Chemotherapy; Gene activation; Resistance; Transposon mutagenesis

Indexed keywords

MULTIDRUG RESISTANCE PROTEIN 1; PACLITAXEL;

ABCB1 GENE; ARTICLE; CANCER CELL; CANCER RESISTANCE; CELL CLONE; CONTROLLED STUDY; DNA LIBRARY; GENE ACTIVATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE INTERACTION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; MUTAGENESIS; OPEN READING FRAME; RNA INTERFERENCE; TRANSPOSON;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; BLOTTING, WESTERN; CELL LINE, TUMOR; DNA BARCODING, TAXONOMIC; DNA MUTATIONAL ANALYSIS; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, NEOPLASM; HUMANS; MUTAGENESIS, INSERTIONAL; NEOPLASMS; PACLITAXEL; RNA, MESSENGER;

EID: 84874245525     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-93     Document Type: Article

References (50)

1. Meijer D, van Agthoven T, Bosma PT, Nooter K, Dorssers LC. Functional screen for genes responsible for tamoxifen resistance in human breast cancer cells. Mol Cancer Res 2006, 4(6):379-386.
2. Johannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, Johnson LA, Emery CM, Stransky N, Cogdill AP, Barretina J. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 2010, 468(7326):968-972.
3. Gaither LA. Chemogenomics approaches to novel target discovery. Expert Rev Proteomics 2007, 4(3):411-419.
4. Kool J, Berns A. High-throughput insertional mutagenesis screens in mice to identify oncogenic networks. Nat Rev Cancer 2009, 9(6):389-399.
5. Dorssers LC, van Agthoven T, Dekker A, van Agthoven TL, Kok EM. Induction of antiestrogen resistance in human breast cancer cells by random insertional mutagenesis using defective retroviruses: identification of bcar-1, a common integration site. Mol Endocrinol 1993, 7(7):870-878.
6. Miething C, Grundler R, Mugler C, Brero S, Hoepfl J, Geigl J, Speicher MR, Ottmann O, Peschel C, Duyster J. Retroviral insertional mutagenesis identifies RUNX genes involved in chronic myeloid leukemia disease persistence under imatinib treatment. Proc Natl Acad Sci U S A 2007, 104(11):4594-4599.
7. Singhal R, Deng X, Chenchik AA, Kandel ES. Long-distance effects of insertional mutagenesis. PLoS One 2011, 6(1):e15832.
8. Carette JE, Raaben M, Wong AC, Herbert AS, Obernosterer G, Mulherkar N, Kuehne AI, Kranzusch PJ, Griffin AM, Ruthel G. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 2011, 477(7364):340-343.
9. McClintock B. The origin and behavior of mutable loci in maize. Proc Natl Acad Sci U S A 1950, 36(6):344-355.
10. Ivics Z, Hackett PB, Plasterk RH, Izsvak Z. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 1997, 91(4):501-510.
11. Elick TA, Bauser CA, Fraser MJ. Excision of the piggyBac transposable element in vitro is a precise event that is enhanced by the expression of its encoded transposase. Genetica 1996, 98(1):33-41.
12. Fraser MJ, Ciszczon T, Elick T, Bauser C. Precise excision of TTAA-specific lepidopteran transposons piggyBac (IFP2) and tagalong (TFP3) from the baculovirus genome in cell lines from two species of Lepidoptera. Insect Mol Biol 1996, 5(2):141-151.
13. Ding S, Wu X, Li G, Han M, Zhuang Y, Xu T. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 2005, 122(3):473-483.
14. Chew SK, Rad R, Futreal PA, Bradley A, Liu P. Genetic screens using the piggyBac transposon. Methods 2011, 53(4):366-371.
15. Ivics Z, Li MA, Mates L, Boeke JD, Nagy A, Bradley A, Izsvak Z. Transposon-mediated genome manipulation in vertebrates. Nat Methods 2009, 6(6):415-422.
16. Wang W, Bradley A, Huang Y. A piggyBac transposon-based genome-wide library of insertionally mutated Blm-deficient murine ES cells. Genome Res 2009, 19(4):667-673.
17. Horie K, Yusa K, Yae K, Odajima J, Fischer SE, Keng VW, Hayakawa T, Mizuno S, Kondoh G, Ijiri T. Characterization of Sleeping Beauty transposition and its application to genetic screening in mice. Mol Cell Biol 2003, 23(24):9189-9207.
18. Mates L, Izsvak Z, Ivics Z. Technology transfer from worms and flies to vertebrates: transposition-based genome manipulations and their future perspectives. Genome Biol 2007, 8 Suppl 1:S1.
19. Walden R, Fritze K, Hayashi H, Miklashevichs E, Harling H, Schell J. Activation tagging: a means of isolating genes implicated as playing a role in plant growth and development. Plant Mol Biol 1994, 26(5):1521-1528.
20. Collier LS, Carlson CM, Ravimohan S, Dupuy AJ, Largaespada DA. Cancer gene discovery in solid tumours using transposon-based somatic mutagenesis in the mouse. Nature 2005, 436(7048):272-276.
21. Vassiliou GS, Cooper JL, Rad R, Li J, Rice S, Uren A, Rad L, Ellis P, Andrews R, Banerjee R. Mutant nucleophosmin and cooperating pathways drive leukemia initiation and progression in mice. Nat Genet 2011, 43(5):470-475.
22. Boshart M, Weber F, Jahn G, Dorsch-Hasler K, Fleckenstein B, Schaffner W. A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell 1985, 41(2):521-530.
23. Koh J, Enders GH, Dynlacht BD, Harlow E. Tumour-derived p16 alleles encoding proteins defective in cell-cycle inhibition. Nature 1995, 375(6531):506-510.
24. Jao LE, Maddison L, Chen W, Burgess SM. Using retroviruses as a mutagenesis tool to explore the zebrafish genome. Brief Funct Genomic Proteomic 2008, 7(6):427-443.
25. 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(3):R25.
26. Wang W, Lin C, Lu D, Ning Z, Cox T, Melvin D, Wang X, Bradley A, Liu P. Chromosomal transposition of PiggyBac in mouse embryonic stem cells. Proc Natl Acad Sci U S A 2008, 105(27):9290-9295.
27. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002, 2(1):48-58.
28. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.
29. Zhang M, Wang W. Organization of signaling complexes by PDZ-domain scaffold proteins. Accounts Chem Res 2003, 36(7):530-538.
30. Ranganathan R, Ross EM. PDZ domain proteins: scaffolds for signaling complexes. Curr Biol 1997, 7(12):R770-773.
31. Fanning AS, Anderson JM. Protein-protein interactions: PDZ domain networks. Curr Biol 1996, 6(11):1385-1388.
32. Chen SZ, Jiang M, Zhen YS. HERG K+ channel expression-related chemosensitivity in cancer cells and its modulation by erythromycin. Cancer Chemother Pharmacol 2005, 56(2):212-220.
33. Kornau HC, Seeburg PH, Kennedy MB. Interaction of ion channels and receptors with PDZ domain proteins. Curr Opin Neurobiol 1997, 7(3):368-373.
34. Stoeckel H, Takeda K. Plasmalemmal voltage-activated K(+) currents in protoplasts from tobacco BY-2 cells: possible regulation by actin microfilaments?. Protoplasma 2002, 220(1-2):79-87.
35. Casini S, Tan HL, Demirayak I, Remme CA, Amin AS, Scicluna BP, Chatyan H, Ruijter JM, Bezzina CR, van Ginneken AC. Tubulin polymerization modifies cardiac sodium channel expression and gating. Cardiovasc Res 2009, 85(4):691-700.
36. Miyano K, Tang HB, Nakamura Y, Morioka N, Inoue A, Nakata Y. Paclitaxel and vinorelbine, evoked the release of substance P from cultured rat dorsal root ganglion cells through different PKC isoform-sensitive ion channels. Neuropharmacology 2009, 57(1):25-32.
37. Montalbetti N, Li Q, Wu Y, Chen XZ, Cantiello HF. Polycystin-2 cation channel function in the human syncytiotrophoblast is regulated by microtubular structures. J Physiol 2007, 579(Pt 3):717-728.
38. Sonee M, Barron E, Yarber FA, Hamm-Alvarez SF. Taxol inhibits endosomal-lysosomal membrane trafficking at two distinct steps in CV-1 cells. Am J Physiol 1998, 275(6 Pt 1):C1630-1639.
39. Garnett MJ, Edelman EJ, Heidorn SJ, Greenman CD, Dastur A, Lau KW, Greninger P, Thompson IR, Luo X, Soares J. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012, 483(7391):570-575.
40. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, Wilson CJ, Lehar J, Kryukov GV, Sonkin D. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012, 483(7391):603-607.
41. Kong J, Wang F, Brenton JD, Adams DJ. Slingshot: a PiggyBac based transposon system for tamoxifen-inducible 'self-inactivating' insertional mutagenesis. Nucleic Acids Res 2010, 38(18):e173.
42. Smith LL, Yeung J, Zeisig BB, Popov N, Huijbers I, Barnes J, Wilson AJ, Taskesen E, Delwel R, Gil J. Functional crosstalk between Bmi1 and MLL/Hoxa9 axis in establishment of normal hematopoietic and leukemic stem cells. Cell Stem Cell 2011, 8(6):649-662.
43. Zeisig BB, Milne T, Garcia-Cuellar MP, Schreiner S, Martin ME, Fuchs U, Borkhardt A, Chanda SK, Walker J, Soden R. Hoxa9 and Meis1 are key targets for MLL-ENL-mediated cellular immortalization. Mol Cell Biol 2004, 24(2):617-628.
44. Lawrence HJ, Rozenfeld S, Cruz C, Matsukuma K, Kwong A, Komuves L, Buchberg AM, Largman C. Frequent co-expression of the HOXA9 and MEIS1 homeobox genes in human myeloid leukemias. Leukemia 1999, 13(12):1993-1999.
45. 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(13):3714-3725.
46. Rosales-Avina JA, Torres-Flores J, Aguilar-Lemarroy A, Gurrola-Diaz C, Hernandez-Flores G, Ortiz-Lazareno PC, Lerma-Diaz JM, de Celis R, Gonzalez-Ramella O, Barrera-Chaires E. MEIS1, PREP1, and PBX4 are differentially expressed in acute lymphoblastic leukemia: association of MEIS1 expression with higher proliferation and chemotherapy resistance. J Exp Clin Cancer Res 2011, 30:112.
47. Jung MJ, Rho JK, Kim YM, Jung JE, Jin YB, Ko YG, Lee JS, Lee SJ, Lee JC, Park MJ. Upregulation of CXCR4 is functionally crucial for maintenance of stemness in drug-resistant non-small cell lung cancer cells. Oncogene 2013, 32(2):209-221.
48. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006, 5:67.
49. Miki J, Furusato B, Li H, Gu Y, Takahashi H, Egawa S, Sesterhenn IA, McLeod DG, Srivastava S, Rhim JS. Identification of putative stem cell markers, CD133 and CXCR4, in hTERT-immortalized primary nonmalignant and malignant tumor-derived human prostate epithelial cell lines and in prostate cancer specimens. Cancer Res 2007, 67(7):3153-3161.
50. Singh S, Srivastava SK, Bhardwaj A, Owen LB, Singh AP. CXCL12-CXCR4 signalling axis confers gemcitabine resistance to pancreatic cancer cells: a novel target for therapy. Br J Cancer 2010, 103(11):1671-1679.