A transposon toolkit for gene transfer and mutagenesis in protozoan parasites

Genetica

Volumn 138, Issue 3, 2010, Pages 301-311

  Damasceno, Jeziel D ^a   Beverley, Stephen M ^b   Tosi, Luiz R O ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

In vitro transposition; Leishmania; Mariner; Plasmodium; Protozoan parasite; Trypanosoma

Indexed keywords

DNA BINDING PROTEIN; MARINER TRANSPOSASES; TRANSPOSASE;

ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; GENE TRANSFER; GENOME; HUMAN; LEISHMANIA; MUTAGENESIS; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM; PROTOZOAL INFECTION; TRANSPOSON; TRYPANOSOMA;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GENE TRANSFER TECHNIQUES; GENOME, PROTOZOAN; HUMANS; LEISHMANIA; MUTAGENESIS; PLASMODIUM; PROTOZOAN INFECTIONS; TRANSPOSASES; TRYPANOSOMA;

PROTOZOA; TRYPANOSOMA;

EID: 77949277866     PISSN: 00166707     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10709-009-9406-7     Document Type: Article

References (82)

1. Adelman ZN, Jasinskiene N, James AA (2002) Development and applications of transgenesis in the yellow fever mosquito, Aedes aegypti. Mol Biochem Parasitol 121: 1-10.
2. Akopyants NS, Matlib RS, Bukanova EN, Smeds MR, Brownstein BH, Stormo GD, Beverley SM (2004) Expression profiling using random genomic DNA microarrays identifies differentially expressed genes associated with three major developmental stages of the protozoan parasite Leishmania major. Mol Biochem Parasitol 136: 71-86.
3. Almeida R, Gilmartin BJ, McCann SH, Norrish A, Ivens AC, Lawson D, Levick MP, Smith DF, Dyall SD, Vetrie D et al (2004) Expression profiling of the Leishmania life cycle: cDNA arrays identify developmentally regulated genes present but not annotated in the genome. Mol Biochem Parasitol 136: 87-100.
4. Arensburger P, Kim YJ, Orsetti J, Aluvihare C, O'Brochta DA, Atkinson PW (2005) An active transposable element, Herves, from the African malaria mosquito Anopheles gambiae. Genetics 169: 697-708.
5. Auge-Gouillou C, Hamelin MH, Demattei MV, Periquet G, Bigot Y (2001a) The ITR binding domain of the Mariner Mos-1 transposase. Mol Genet Genomics 265: 58-65.
6. Auge-Gouillou C, Hamelin MH, Demattei MV, Periquet M, Bigot Y (2001b) The wild-type conformation of the Mos-1 inverted terminal repeats is suboptimal for transposition in bacteria. Mol Genet Genomics 265: 51-57.
7. Augusto MJ, Squina FM, Marchini JF, Dias FC, Tosi LR (2004) Specificity of modified Drosophila mariner transposons in the identification of Leishmania genes. Exp Parasitol 108: 109-113.
8. Balaji S, Babu MM, Iyer LM, Aravind L (2005) Discovery of the principal specific transcription factors of apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res 33: 3994-4006.
9. Balciunas D, Wangensteen KJ, Wilber A, Bell J, Geurts A, Sivasubbu S, Wang X, Hackett PB, Largaespada DA, McIvor RS et al (2006) Harnessing a high cargo-capacity transposon for genetic applications in vertebrates. PLoS Genet 2: e169.
10. Balu B, Adams JH (2006) Functional genomics of Plasmodium falciparum through transposon-mediated mutagenesis. Cell Microbiol 8: 1529-1536.
11. Balu B, Shoue DA, Fraser MJ Jr, Adams JH (2005) High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Proc Natl Acad Sci USA 102: 16391-16396.
12. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B et al (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422.
13. Beverley SM (2003a) Trypanosomatid protozoan parasite genetics comes of age: Protozomics!. Nat Rev Genet 4: 11-19.
14. Beverley SM (2003b) Genetic and genomic approaches to the analysis of Leishmania virulence. In: Marr J, Nilsen T, Komuniecki R (eds) Molecular and medical parasitology. Academic Press, New York, pp 111-122.
15. Beverley SM, Akopyants NS, Goyard S, Matlib RS, Gordon JL, Brownstein BH, Stormo GD, Bukanova EN, Hott CT, Li F, MacMillan S, Muo JN, Schwertman LA, Smeds MR, Wang Y (2002) Putting the Leishmania genome to work: functional genomics by transposon trapping and expression profiling. Philos Trans R Soc Lond B, Biol Sci 357: 47-53.
16. Boucher N, McNicoll F, Dumas C, Papadopoulou B (2002) RNA polymerase I-mediated transcription of a reporter gene integrated into different loci of Leishmania. Mol Biochem Parasitol 119: 153-158.
17. Breman JG, Alilio MS, Mills A (2004) Conquering the intolerable burden of malaria: what's new, what's needed: a summary. Am J Trop Med Hyg 71: 1-15.
18. Carlton J (2003) The Plasmodium vivax genome sequencing project. Trends Parasitol 19: 227-231.
19. Coates CJ, Jasinskiene N, Miyashiro L, James AA (1998) Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci USA 95: 3748-3751.
20. Coleman BI, Duraisingh MT (2008) Transcriptional control and gene silencing in Plasmodium falciparum. Cell Microbiol 10: 1935-1946.
21. Collier LS, Largaespada DA (2005) Hopping around the tumor genome: transposons for cancer gene discovery. Cancer Res 65: 9607-9610.
22. 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.
23. Cooper LD, Marquez-Cedillo L, Singh J, Sturbaum AK, Zhang S, Edwards V, Johnson K, Kleinhofs A, Rangel S, Carollo V et al (2004) Mapping Ds insertions in barley using a sequence-based approach. Mol Genet Genomics 272: 181-193.
24. Croft SL, Sundar S, Fairlamb AH (2006) Drug resistance in leishmaniasis. Clin Microbiol Rev 19: 111-126.
25. El-Sayed NM, Myler PJ, Blandin G, Berriman M, Crabtree J, Aggarwal G, Caler E, Renauld H, Worthey EA, Hertz-Fowler C et al (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science 309: 404-409.
26. Fadool JM, Hartl DL, Dowling JE (1998) Transposition of the mariner element from Drosophila mauritiana in zebrafish. Proc Natl Acad Sci USA 95: 5182-5186.
27. Fischer SE, van Luenen HG, Plasterk RH (1999) Cis requirements for transposition of Tc1-like transposons in C. elegans. Mol Gen Genet 262: 268-274.
28. Fischer SE, Wienholds E, Plasterk RH (2001) Regulated transposition of a fish transposon in the mouse germ line. Proc Natl Acad Sci USA 98: 6759-6764.
29. Fraser MJ, Brusca JS, Smith GE, Summers MD (1985) Transposon-mediated mutagenesis of a baculovirus. Virology 145: 356-361.
30. Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, Guinet F, Nehrbass U, Wellems TE, Scherf A (2000) Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407: 1018-1022.
31. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S et al (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
32. Goryshin IY, Reznikoff WS (1998) Tn5 in vitro transposition. J Biol Chem 273: 7367-7374.
33. Goyard S, Tosi LR, Gouzova J, Majors J, Beverley SM (2001) New Mos1 mariner transposons suitable for the recovery of gene fusions in vivo and in vitro. Gene 280: 97-105.
34. Greenwood B, Mutabingwa T (2002) Malaria in 2002. Nature 415: 670-672.
35. Gueiros-Filho FJ, Beverley SM (1996) Selection against the dihydrofolate reductase-thymidylate synthase (DHFR-TS) locus as a probe of genetic altyerations in Leishmania major. Mol Cell Biol 16: 5655-5663.
36. Gueiros-Filho FJ, Beverley SM (1997) Trans-kingdom transposition of the Drosophila element mariner within the protozoan Leishmania. Science 276: 1716-1719.
37. Hamer L, Adachi K, Montenegro-Chamorro MV, Tanzer MM, Mahanty SK, Lo C, Tarpey RW, Skalchunes AR, Heiniger RW, Frank SA et al (2001a) Gene discovery and gene function assignment in filamentous fungi. Proc Natl Acad Sci USA 98: 5110-5115.
38. Hamer L, DeZwaan TM, Montenegro-Chamorro MV, Frank SA, Hamer JE (2001b) Recent advances in large-scale transposon mutagenesis. Curr Opin Chem Biol 5: 67-73.
39. Holzer TR, McMaster WR, Forney JD (2006) Expression profiling by whole-genome interspecies microarray hybridization reveals differential gene expression in procyclic promastigotes, lesion-derived amastigotes, and axenic amastigotes in Leishmania mexicana. Mol Biochem Parasitol 146: 198-218.
40. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R et al (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436-442.
41. Izsvak Z, Ivics Z, Plasterk RH (2000) Sleeping Beauty, a wide host-range transposon vector for genetic transformation in vertebrates. J Mol Biol 302: 93-102.
42. Jasinskiene N, Coates CJ, Benedict MQ, Cornel AJ, Rafferty CS, James AA, Collins FH (1998) Stable transformation of the yellow fever mosquito, Aedes aegypti, with the Hermes element from the housefly. Proc Natl Acad Sci USA 95: 3743-3747.
43. Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J et al (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22: 561-570.
44. Lampe DJ, Churchill ME, Robertson HM (1996) A purified mariner transposase is sufficient to mediate transposition in vitro. EMBO J 15: 5470-5479.
45. Laurentino EC, Ruiz JC, Brito LO, Fiandt M, Nicoletti LM, Jamur MC, Oliver C, Tosi LR, Cruz AK (2007) The use of Tn5 transposable elements in a gene trapping strategy for the protozoan Leishmania. Int J Parasitol 37: 735-742.
46. Lavoie BD, Chaconas G (1996) Transposition of phage Mu DNA. Curr Top Microbiol Immunol 204: 83-102.
47. Leal S, Acosta-Serrano A, Morris J, Cross GA (2004) Transposon mutagenesis of Trypanosoma brucei identifies glycosylation mutants resistant to concanavalin A. J Biol Chem 279: 28979-28988.
48. Leifso K, Cohen-Freue G, Dogra N, Murray A, McMaster WR (2007) Genomic and proteomic expression analysis of Leishmania promastigote and amastigote life stages: the Leishmania genome is constitutively expressed. Mol Biochem Parasitol 152: 35-46.
49. Lohe AR, Hartl DL (1996) Autoregulation of mariner transposase activity by overproduction and dominant-negative complementation. Mol Biol Evol 13: 549-555.
50. Loukeris TG, Arca B, Livadaras I, Dialektaki G, Savakis C (1995) Introduction of the transposable element Minos into the germ line of Drosophila melanogaster. Proc Natl Acad Sci USA 92: 9485-9489.
51. Lozovsky ER, Nurminsky D, Wimmer EA, Hartl DL (2002) Unexpected stability of mariner transgenes in Drosophila. Genetics 160: 527-535.
52. Mamoun CB, Gluzman IY, Beverley SM, Goldberg DE (2000) Transposition of the Drosophila element mariner within the human malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 110: 405-407.
53. Marchini JF, Cruz AK, Beverley SM, Tosi LR (2003) The H region HTBF gene mediates terbinafine resistance in Leishmania major. Mol Biochem Parasitol 131: 77-81.
54. Martin E, Laloux H, Couette G, Alvarez T, Bessou C, Hauser O, Sookhareea S, Labouesse M, Segalat L (2002) Identification of 1088 new transposon insertions of Caenorhabditis elegans: a pilot study toward large-scale screens. Genetics 162: 521-524.
55. Martinez-Calvillo S, Nguyen D, Stuart K, Myler PJ (2004) Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot Cell 3: 506-517.
56. Mates L, Izsvak Z, Ivics Z (2007) Technology transfer from worms and flies to vertebrates: transposition-based genome manipulations and their future perspectives. Genome Biol 8(Suppl 1): S1.
57. Medhora M, Maruyama K, Hartl DL (1991) Molecular and functional analysis of the mariner mutator element Mos1 in Drosophila. Genetics 128: 311-318.
58. Merkulov GV, Boeke JD (1998) Libraries of green fluorescent protein fusions generated by transposition in vitro. Gene 222: 213-222.
59. Myung KS, Beetham JK, Wilson ME, Donelson JE (2002) Comparison of the post-transcriptional regulation of the mRNAs for the surface proteins PSA (GP46) and MSP (GP63) of Leishmania chagasi. J Biol Chem 277: 16489-16497.
60. Noazin S, Modabber F, Khamesipour A, Smith PG, Moulton LH, Nasseri K, Sharifi I, Khalil EA, Bernal ID, Antunes CM, Kieny MP, Tanner M (2008) First generation leishmaniasis vaccines: a review of field ifficacy trials. Vaccine 26: 6759-6767.
61. O'Donnell RA, Freitas-Junior LH, Preiser PR, Williamson DH, Duraisingh M, McElwain TF, Scherf A, Cowman AF, Crabb BS (2002) A genetic screen for improved plasmid segregation reveals a role for Rep20 in the interaction of Plasmodium falciparum chromosomes. EMBO J 21: 1231-1239.
62. Pays E (2005) Regulation of antigen gene expression in Trypanosoma brucei. Trends Parasitol 21: 517-520.
63. Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, Quail MA, Peters N, Adlem E, Tivey A, Aslett M et al (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39: 839-847.
64. Robinson KA, Goyard S, Beverley SM (2004) In vitro shuttle mutagenesis using engineered mariner transposons. Methods Mol Biol 270: 299-318.
65. Ross-Macdonald P, Coelho PS, Roemer T, Agarwal S, Kumar A, Jansen R, Cheung KH, Sheehan A, Symoniatis D, Umansky L et al (1999a) Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature 402: 413-418.
66. Ross-Macdonald P, Sheehan A, Friddle C, Roeder GS, Snyder M (1999b) Transposon mutagenesis for the analysis of protein production, function, and localization. Methods Enzymol 303: 512-532.
67. Rubin EJ, Akerley BJ, Novik VN, Lampe DJ, Husson RN, Mekalanos JJ (1999) In vivo transposition of mariner-based elements in enteric bacteria and mycobacteria. Proc Natl Acad Sci USA 96: 1645-1650.
68. Sakamoto H, Thiberge S, Akerman S, Janse CJ, Carvalho TG, Menard R (2005) Towards systematic identification of Plasmodium essential genes by transposon shuttle mutagenesis. Nucleic Acids Res 33: e174.
69. Saxena A, Lahav T, Holland N, Aggarwal G, Anupama A, Huang Y, Volpin H, Myler PJ, Zilberstein D (2007) Analysis of the Leishmania donovani transcriptome reveals an ordered progression of transient and permanent changes in gene expression during differentiation. Mol Biochem Parasitol 152: 53-65.
70. Sherman A, Dawson A, Mather C, Gilhooley H, Li Y, Mitchell R, Finnegan D, Sang H (1998) Transposition of the Drosophila element mariner into the chicken germ line. Nat Biotechnol 16: 1050-1053.
71. Silva EK, Gehrke AR, Olszewski K, León I, Chahal JS, Bulyk ML, Llinás M (2008) Specific DNA-binding by apicomplexan AP2 transcription factors. Proc Natl Acad Sci USA 105: 8393-8398.
72. Simarro PP, Jannin J, Cattand P (2008) Eliminating human African trypanosomiasis: where do we stand and what comes next? PLoS Med 5: e55.
73. Singh J, Zhang S, Chen C, Cooper L, Bregitzer P, Sturbaum A, Hayes PM, Lemaux PG (2006) High-frequency Ds remobilization over multiple generations in barley facilitates gene tagging in large genome cereals. Plant Mol Biol 62: 937-950.
74. Spradling AC, Stern D, Beaton A, Rhem EJ, Laverty T, Mozden N, Misra S, Rubin GM (1999) The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics 153: 135-177.
75. Squina FM, Pedrosa AL, Nunes VS, Cruz AK, Tosi LR (2007) Shuttle mutagenesis and targeted disruption of a telomere-located essential gene of Leishmania. Parasitology 134: 511-522.
76. Targett GA, Greenwood BM (2008) Malaria vaccines and their potential role in the elimination of malaria. Malaria J 7: 1-9.
77. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL et al (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36: 283-287.
78. Tosi LR, Beverley SM (2000) cis and trans factors affecting Mos1 mariner evolution and transposition in vitro, and its potential for functional genomics. Nucleic Acids Res 28: 784-790.
79. Urasaki A, Morvan G, Kawakami K (2006) Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics 174: 639-649.
80. Wilson MH, Coates CJ, George AL Jr (2007) PiggyBac transposon-mediated gene transfer in human cells. Mol Ther 15: 139-145.
81. Zayed H, Izsvak Z, Walisko O, Ivics Z (2004) Development of hyperactive sleeping beauty transposon vectors by mutational analysis. Mol Ther 9: 292-304.
82. Zhang JK, Pritchett MA, Lampe DJ, Robertson HM, Metcalf WW (2000) In vivo transposon mutagenesis of the methanogenic archaeon Methanosarcina acetivorans C2A using a modified version of the insect mariner-family transposable element Himar1. Proc Natl Acad Sci USA 97: 9665-9670.