The NemaGENETAG initiative: Large scale transposon insertion gene-tagging in Caenorhabditis elegans

Genetica

Volumn 137, Issue 1, 2009, Pages 39-46

  Bazopoulou, Daphne ^a   Tavernarakis, Nektarios ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

Caenorhabditis elegans; Gene tagging; Mariner; Mos1; Tc1; Transposon

Indexed keywords

MUTANT PROTEIN;

ANIMAL; CAENORHABDITIS ELEGANS; GENE EXPRESSION REGULATION; GENE TRANSFER; GENETICS; GENOMICS; HUMAN; METHODOLOGY; REVIEW; TRANSPOSON;

ANIMALS; CAENORHABDITIS ELEGANS; DNA TRANSPOSABLE ELEMENTS; GENE TRANSFER TECHNIQUES; GENOMICS; HUMANS; MUTAGENESIS, INSERTIONAL; MUTANT PROTEINS;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 70349983047     PISSN: 00166707     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10709-009-9361-3     Document Type: Review

References (60)

1. Antoshechkin I, Sternberg PW (2007) The versatile worm: genetic and genomic resources for Caenorhabditis elegans research. Nat Rev Genet 8(7):518-532. doi:10.1038/nrg2105.
2. Asakawa K, Suster ML, Mizusawa K, Nagayoshi S, Kotani T, Urasaki A, Kishimoto Y, Hibi M, Kawakami K (2008) Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. Proc Natl Acad Sci USA 105(4):1255-1260. doi:10.1073/pnas.0704963105.
3. Awazu S, Matsuoka T, Inaba K, Satoh N, Sasakura Y (2007) High-throughput enhancer trap by remobilization of transposon Minos in Ciona intestinalis. Genesis 45(5):307-317. doi:10.1002/dvg.20290.
4. Balciunas D, Davidson AE, Sivasubbu S, Hermanson SB, Welle Z, Ekker SC (2004) Enhancer trapping in zebrafish using the Sleeping Beauty transposon. BMC Genomics 5(1):62. doi:10.1186/1471-2164-5-62.
5. Bessereau JL (2006) Insertional mutagenesis in C. elegans using the Drosophila transposon Mos1: a method for the rapid identification of mutated genes. Methods Mol Biol 351:59-73.
6. Bessereau JL, Wright A, Williams DC, Schuske K, Davis MW, Jorgensen EM (2001) Mobilization of a Drosophila transposon in the Caenorhabditis elegans germ line. Nature 413(6851):70-74. doi:10.1038/35092567.
7. Bonin CP, Mann RS (2004) A piggyBac transposon gene trap for the analysis of gene expression and function in Drosophila. Genetics 167(4):1801-1811. doi:10.1534/genetics.104.027557.
8. Boulin T, Bessereau JL (2007) Mos1-mediated insertional mutagenesis in Caenorhabditis elegans. Nat Protocols 2(5):1276-1287. doi:10.1038/nprot.2007.192.
9. Boulin T, Gielen M, Richmond JE, Williams DC, Paoletti P, Bessereau JL (2008) Eight genes are required for functional reconstitution of the Caenorhabditis elegans levamisole-sensitive acetylcholine receptor. Proc Natl Acad Sci USA 105(47):18590-18595. doi:10.1073/pnas.0806933105.
10. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71-94.
11. Catteruccia F, Nolan T, Loukeris TG, Blass C, Savakis C, Kafatos FC, Crisanti A (2000) Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405(6789):959-962. doi:10.1038/35016096.
12. Ding S, Wu X, Li G, Han M, Zhuang Y, Xu T (2005) Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122(3):473-483. doi:10.1016/j.cell.2005.07.013.
13. Drabek D, Zagoraiou L, de Wit T, Langeveld A, Roumpaki C, Mamalaki C, Savakis C, Grosveld F (2003) Transposition of the Drosophila hydei Minos transposon in the mouse germ line. Genomics 81(2):108-111. doi:10.1016/S0888-7543(02)00030-7.
14. Duverger Y, Belougne J, Scaglione S, Brandli D, Beclin C, Ewbank JJ (2007) A semi-automated high-throughput approach to the generation of transposon insertion mutants in the nematode Caenorhabditis elegans. Nucleic Acids Res 35(2):e11. doi:10.1093/nar/gkl1046.
15. Eimer S, Gottschalk A, Hengartner M, Horvitz HR, Richmond J, Schafer WR, Bessereau JL (2007) Regulation of nicotinic receptor trafficking by the transmembrane Golgi protein UNC-50. EMBO J 26(20):4313-4323. doi:10.1038/sj.emboj.7601858.
16. Faucheux M, Netter S, Bloyer S, Moussa M, Boissonneau E, Lemeunier F, Wegnez M, Theodore L (2001) Advantages of a P-element construct containing MtnA sequences for the identification of patterning and cell determination genes in Drosophila melanogaster. Mol Genet Genomics 265(1):14-22. doi:10.1007/s004380000391.
17. Franz G, Savakis C (1991) Minos, a new transposable element from Drosophila hydei, is a member of the Tc1-like family of transposons. Nucleic Acids Res 19(23):6646. doi:10.1093/nar/19.23.6646.
18. Gally C, Eimer S, Richmond JE, Bessereau JL (2004) A transmembrane protein required for acetylcholine receptor clustering in Caenorhabditis elegans. Nature 431(7008):578-582. doi:10.1038/nature02893.
19. Geurts AM, Wilber A, Carlson CM, Lobitz PD, Clark KJ, Hackett PB, McIvor RS, Largaespada DA (2006) Conditional gene expression in the mouse using a Sleeping Beauty gene-trap transposon. BMC Biotechnol 6:30. doi:10.1186/1472-6750-6-30.
20. Granger L, Martin E, Segalat L (2004) Mos as a tool for genome-wide insertional mutagenesis in Caenorhabditis elegans: results of a pilot study. Nucleic Acids Res 32(14):e117. doi:10.1093/nar/gnh111.
21. Grossman GL, Rafferty CS, Fraser MJ, Benedict MQ (2000) The piggyBac element is capable of precise excision and transposition in cells and embryos of the mosquito, Anopheles gambiae. Insect Biochem Mol Biol 30(10):909-914. doi:10.1016/S0965-1748(00)00092-8.
22. Handler AM, McCombs SD (2000) The piggyBac transposon mediates germ-line transformation in the Oriental fruit fly and closely related elements exist in its genome. Insect Mol Biol 9(6):605-612. doi:10.1046/j.1365-2583.2000.00227.x.
23. Handler AM, McCombs SD, Fraser MJ, Saul SH (1998) The lepidopteran transposon vector, piggyBac, mediates germ-line transformation in the Mediterranean fruit fly. Proc Natl Acad Sci USA 95(13):7520-7525. doi:10.1073/pnas.95.13.7520.
24. Hediger M, Niessen M, Wimmer EA, Dubendorfer A, Bopp D (2001) Genetic transformation of the housefly Musca domestica with the lepidopteran derived transposon piggyBac. Insect Mol Biol 10(2):113-119. doi:10.1046/j.1365-2583.2001.00243.x.
25. Horn C, Offen N, Nystedt S, Hacker U, Wimmer EA (2003) piggyBac-based insertional mutagenesis and enhancer detection as a tool for functional insect genomics. Genetics 163(2):647-661.
26. Klinakis AG, Loukeris TG, Pavlopoulos A, Savakis C (2000) Mobility assays confirm the broad host-range activity of the Minos transposable element and validate new transformation tools. Insect Mol Biol 9(3):269-275. doi:10.1046/j.1365-2583.2000.00183.x.
27. Korswagen HC, Park JH, Ohshima Y, Plasterk RH (1997) An activating mutation in a Caenorhabditis elegans Gs protein induces neural degeneration. Genes Dev 11(12):1493-1503. doi:10.1101/gad.11.12.1493.
28. Li X, Lobo N, Bauser CA, Fraser MJ Jr (2001) The minimum internal and external sequence requirements for transposition of the eukaryotic transformation vector piggyBac. Mol Genet Genomics 266(2):190-198. doi:10.1007/s004380100525.
29. Lobo N, Li X, Fraser MJ Jr (1999) Transposition of the piggyBac element in embryos of Drosophila melanogaster, Aedes aegypti and Trichoplusia ni. Mol Gen Genet 261(4-5):803-810. doi:10.1007/s004380050024.
30. Lobo N, Li X, Hua-van A, Fraser MJ Jr (2001) Mobility of the piggyBac transposon in embryos of the vectors of Dengue fever (Aedes albopictus) and La Crosse encephalitis (Ae. triseriatus). Mol Genet Genomics 265(1):66-71. doi:10.1007/s004380000388.
31. Lorenzen MD, Berghammer AJ, Brown SJ, Denell RE, Klingler M, Beeman RW (2003) piggyBac-mediated germline transformation in the beetle Tribolium castaneum. Insect Mol Biol 12(5):433-440. doi:10.1046/j.1365-2583.2003.00427.x.
32. Loukeris TG, Arca B, Livadaras I, Dialektaki G, Savakis C (1995a) Introduction of the transposable element Minos into the germ line of Drosophila melanogaster. Proc Natl Acad Sci USA 92(21):9485-9489. doi:10.1073/pnas.92.21.9485.
33. Loukeris TG, Livadaras I, Arca B, Zabalou S, Savakis C (1995b) Gene transfer into the medfly, Ceratitis capitata, with a Drosophila hydei transposable element. Science 270(5244):2002-2005. doi:10.1126/science.270.5244.2002.
34. Matsuoka T, Awazu S, Satoh N, Sasakura Y (2004) Minos transposon causes germline transgenesis of the ascidian Ciona savignyi. Dev Growth Differ 46(3):249-255. doi:10.1111/j.1440-169X.2004.00742.x.
35. Morales ME, Mann VH, Kines KJ, Gobert GN, Fraser MJ Jr, Kalinna BH, Correnti JM, Pearce EJ, Brindley PJ (2007) piggyBac transposon mediated transgenesis of the human blood fluke, Schistosoma mansoni. FASEB J 21(13):3479-3489. doi:10.1096/fj.07-8726com.
36. Nagayoshi S, Hayashi E, Abe G, Osato N, Asakawa K, Urasaki A, Horikawa K, Ikeo K, Takeda H, Kawakami K (2008) Insertional mutagenesis by the Tol2 transposon-mediated enhancer trap approach generated mutations in two developmental genes: tcf7 and synembryn-like. Development 135(1):159-169. doi:10.1242/dev.009050.
37. Nolan T, Bower TM, Brown AE, Crisanti A, Catteruccia F (2002) piggyBac-mediated germline transformation of the malaria mosquito Anopheles stephensi using the red fluorescent protein dsRED as a selectable marker. J Biol Chem 277(11):8759-8762. doi:10.1074/jbc.C100766200.
38. Parinov S, Kondrichin I, Korzh V, Emelyanov A (2004) Tol2 transposon-mediated enhancer trap to identify developmentally regulated zebrafish genes in vivo. Dev Dyn 231(2):449-459. doi:10.1002/dvdy.20157.
39. Pavlopoulos A, Averof M (2005) Establishing genetic transformation for comparative developmental studies in the crustacean Parhyale hawaiensis. Proc Natl Acad Sci USA 102(22):7888-7893. doi:10.1073/pnas.0501101102.
40. Pavlopoulos A, Berghammer AJ, Averof M, Klingler M (2004) Efficient transformation of the beetle Tribolium castaneum using the Minos transposable element: quantitative and qualitative analysis of genomic integration events. Genetics 167(2):737-746. doi:10.1534/genetics.103.023085.
41. Peloquin JJ, Thibault ST, Staten R, Miller TA (2000) Germ-line transformation of pink bollworm (Lepidoptera: gelechiidae) mediated by the piggyBac transposable element. Insect Mol Biol 9(3):323-333. doi:10.1046/j.1365-2583.2000.00194.x.
42. Perera OP, Harrell IR, Handler AM (2002) Germ-line transformation of the South American malaria vector, Anopheles albimanus, with a piggyBac/EGFP transposon vector is routine and highly efficient. Insect Mol Biol 11(4):291-297. doi:10.1046/j.1365-2583.2002.00336.x.
43. Plasterk RH, Izsvak Z, Ivics Z (1999) Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends Genet 15(8):326-332. doi:10.1016/S0168-9525(99)01777-1.
44. Ren X, Han Z, Miller TA (2006) Excision and transposition of piggyBac transposable element in tobacco budworm embryos. Arch Insect Biochem Physiol 63(2):49-56. doi:10.1002/arch.20140.
45. Robert V, Bessereau JL (2007) Targeted engineering of the Caenorhabditis elegans genome following Mos1-triggered chromosomal breaks. EMBO J 26(1):170-183. doi:10.1038/sj.emboj.7601463.
46. Robert VJ, Davis MW, Jorgensen EM, Bessereau JL (2008) Gene conversion and end-joining-repair double-strand breaks in the Caenorhabditis elegans germline. Genetics 180(1):673-679. doi:10.1534/genetics.108.089698.
47. Rodrigues FG, Oliveira SB, Rocha BC, Moreira LA (2006) Germline transformation of Aedes fluviatilis (Diptera:Culicidae) with the piggyBac transposable element. Mem Inst Oswaldo Cruz 101(7):755-757. doi:10.1590/S0074-02762006000700008.
48. Sasakura Y, Awazu S, Chiba S, Kano S, Satoh N (2003) Application of Minos, one of the Tc1/mariner superfamily transposable elements, to ascidian embryos as a tool for insertional mutagenesis. Gene 308:11-20. doi:10.1016/S0378-1119(03)00426-8.
49. Sasakura Y, Konno A, Mizuno K, Satoh N, Inaba K (2008) Enhancer detection in the ascidian Ciona intestinalis with transposase-expressing lines of Minos. Dev Dyn 237(1):39-50. doi:10.1002/dvdy.21333.
50. Score PR, Belur LR, Frandsen JL, Geurts JL, Yamaguchi T, Somia NV, Hackett PB, Largaespada DA, McIvor RS (2006) Sleeping Beauty-mediated transposition and long-term expression in vivo: use of the LoxP/Cre recombinase system to distinguish transposition-specific expression. Mol Ther 13(3):617-624. doi:10.1016/j.ymthe.2005.10.015.
51. Shinmyo Y, Mito T, Matsushita T, Sarashina I, Miyawaki K, Ohuchi H, Noji S (2004) piggyBac-mediated somatic transformation of the two-spotted cricket, Gryllus bimaculatus. Dev Growth Differ 46(4):343-349. doi:10.1111/j.1440-169x.2004.00751.x.
52. Sumitani M, Yamamoto DS, Oishi K, Lee JM, Hatakeyama M (2003) Germline transformation of the sawfly, Athalia rosae (Hymenoptera: Symphyta), mediated by a piggyBac-derived vector. Insect Biochem Mol Biol 33(4):449-458. doi:10.1016/S0965-1748(03)00009-2.
53. Tamura T, Thibert C, Royer C, Kanda T, Abraham E, Kamba M, Komoto N, Thomas JL, Mauchamp B, Chavancy G, Shirk P, Fraser M, Prudhomme JC, Couble P (2000) Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nat Biotechnol 18(1):81-84. doi:10.1038/71978.
54. The C. elegans Sequencing Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282(5396):2012-2018. doi:10.1126/science.282.5396.2012.
55. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL, Ryner L, Cheung LM, Chong A, Erickson C, Fisher WW, Greer K, Hartouni SR, Howie E, Jakkula L, Joo D, Killpack K, Laufer A, Mazzotta J, Smith RD, Stevens LM, Stuber C, Tan LR, Ventura R, Woo A, Zakrajsek I, Zhao L, Chen F, Swimmer C, Kopczynski C, Duyk G, Winberg ML, Margolis J (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36(3):283-287. doi:10.1038/ng1314.
56. Uchino K, Imamura M, Shimizu K, Kanda T, Tamura T (2007) Germ line transformation of the silkworm, Bombyx mori, using the transposable element Minos. Mol Genet Genomics 277(3):213-220. doi:10.1007/s00438-006-0176-y.
57. Wang W, Lin C, Lu D, Ning Z, Cox T, Melvin D, Wang X, Bradley A, Liu P (2008) Chromosomal transposition of PiggyBac in mouse embryonic stem cells. Proc Natl Acad Sci USA 105(27):9290-9295. doi:10.1073/pnas.0801017105.
58. Williams DC, Boulin T, Ruaud AF, Jorgensen EM, Bessereau JL (2005) Characterization of Mos1-mediated mutagenesis in Caenorhabditis elegans: a method for the rapid identification of mutated genes. Genetics 169(3):1779-1785. doi:10.1534/genetics.104.038265.
59. Zagoraiou L, Drabek D, Alexaki S, Guy JA, Klinakis AG, Langeveld A, Skavdis G, Mamalaki C, Grosveld F, Savakis C (2001) In vivo transposition of Minos, a Drosophila mobile element, in mammalian tissues. Proc Natl Acad Sci USA 98(20):11474-11478. doi:10.1073/pnas.201392398.
60. Zhang H, Shinmyo Y, Hirose A, Mito T, Inoue Y, Ohuchi H, Loukeris TG, Eggleston P, Noji S (2002) Extrachromosomal transposition of the transposable element Minos in embryos of the cricket Gryllus bimaculatus. Dev Growth Differ 44(5):409-417. doi:10.1046/j.1440-169X.2002.00654.x.