Abstract
The genetic manipulation of non-drosophilid insect species is possible by the creation of recombinant DNA constructs that can be integrated into host genomes by several transposon-based vector systems. This technology will allow the development and testing of a variety of systems that can improve existing biological control methods, and the development of new highly efficient methods. For programs such as sterile insect technique (SIT), transgenic strains may include fluorescent protein marker genes for detection of released insects, and conditional gene expression systems that will result in male sterility and female lethality for genetic sexing. Conditional expression systems include the yeast GAL4 system and the bacterial Tet-off and Tet-on systems that can, respectively, negatively or positively regulate expression of genes for lethality or sterility depending on a dietary source of tetracycline. Importantly, strains for male sterility must also incorporate an effective system for genetic sexing, since typically, surviving females would remain fertile. Models for the use of these expression systems and associated genetic material come from studies in Drosophila and, while many of these systems should be transferable to other insects, continued research will be necessary in insects of interest to clone genes, optimize germ-line transformation, and perform vector stability studies and risk assessment for their release as transgenic strains.
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References
Abrams, J.M., J. Agapite, K. White &; H. Steller, 1993. Programmed cell death during Drosophila embryogenesis. Development 117: 29–43.
Allen, M.L., D.A. O'Brochta, P.W. Atkinson &; C.S. Levesque, 2001. Stable, germ-line transformation of Culex quinquefasciatus(Diptera: Culicinae). J. Med. Entomol. 38: 701–710.
Ashburner, M., M.A. Hoy &; J. Peloquin, 1998. Transformation of arthropods-research needs and long term prospects. Insect Mol. Biol. 7: 201–213.
Atkinson, P.W. &; D.A. O'Brochta, 2001. Genetic transformation systems in insects. Annu. Rev. Entomol. 46: 317–346.
Atkinson P.W., W.D. Warren &; D.A. O'Brochta, 1993. The hobotransposable element of Drosophilacan be cross-mobilized in houseflies and excises like the Ac element of maize. Proc. Natl. Acad. Sci. USA 90: 9693–9697.
Baker, B.S., 1989. Sex in flies: the splice of life. Nature 340: 521–524.
Bellen, H.J., D. D'Evelyn, M. Harvey &; S.J. Elledge, 1992. Isolation of temperature-sensitive diphtheria toxins in yeast and their effects on Drosophila cells. Development 114: 787–796.
Bello, B., D. Resendez-Perez &; W.J. Gehring, 1998. Spatial and temporal targeting of gene expression in Drosophila by means of a tetracycline-dependent transactivator system. Development 125: 2193–2202.
Belote, J.M. &; B.S. Baker, 1982. Sex determination in Drosophila melanogaster: analysis of transformer-2, a sex-transforming locus. Proc. Natl. Acad. Sci. USA 79: 1568–1572.
Belote, J.M., M.A. Handler, M.F. Wolfner, K.J. Livak &; B.S. Baker, 1985. Sex-specific regulation of yolk protein gene expression in Drosophila. Cell 40: 339–348.
Berghammer, A.J., M. Klingler &; E.A. Wimmer, 1999. A universal marker for transgenic insects. Nature 402: 370–371.
Bieschke, E.T., J.C. Wheeler &; J. Tower, 1998. Doxycyclineinduced transgene expression during Drosophila development and aging. Mol. Gen. Genet. 258: 571–579.
Bonini, N.M. &; M.E. Fortini, 1999. Surviving Drosophila eye development: integrating cell death with differentiation during formation of a neural structure. Bioessays 21: 991–1003.
Brand, A.H. &; N. Perrimon, 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415.
Brand, A.H., A.S. Manoukian &; N. Perrimon, 1994. Ectopic expression in Drosophila. Meth. Cell Biol. 44: 635–654.
Bump, N.J., M. Hackett, M. Hugunin, S. Seshagiri, K. Brady, P. Chen, C. Ferenz, S. Franklin, T. Ghayur, P. Li, P. Licari, J. Mankovich, L. Shi, A.H. Greenberg, L.K. Miller &; W.W. Wong, 1995. Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269: 1885–1888.
Burtis, K.C. &; B.S. Baker, 1989. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56: 997–1010.
Buttgereit, D. &; R. Renkawitz-Pohl, 1993. Expression of beta 1 tubulin (beta Tub56D) in Drosophila testis stem cells is regulated by a short upstream sequence while intron elements guide expression in somatic cells. Mol. Gen. Genet. 241: 263–270.
Cary, L.C., M. Goebel, H.H. Corsaro, H.H. Wang, E. Rosen &; M.J. Fraser, 1989. Transposon mutagenesis of baculoviruses: analysis of Trichoplusia nitransposon IFP2 insertions within the FP-Locus of nuclear polyhedrosis viruses. Virology 161: 8–17.
Castrillon, D.H., P. Gonczy, S. Alexander, R. Rawson, C.G. Eberhart, S. Viswanathan, S. DiNardo &; S.A. Wasserman, 1993. Toward a molecular genetic analysis of spermatogenesis in Drosophilamelanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135: 489–505.
Catteruccia, F., T. Nolan, T.G. Loukeris, C. Blass, C. Savakis, F.C. Kafatos &; A. Crisanti, 2000. Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405: 959–962.
Chalfie, M., Y. Tu, G. Euskirchen, W. Ward &; D.C. Prasher, 1994. Green fluorescent protein as a marker for gene expression. Science 263: 802–805.
Chen, A.C., H.R. Kim, R.T. Mayer &; J.O. Norman, 1987. Vitellogenesis in the stable fly, Stomoxys calcitrans. Comp. Biochem. Physiol. 88B: 897–903.
Coates, C.J., N. Jasinskiene, L. Miyashiro &; A.A. James, 1998. Marinertransposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc. Natl. Acad. Sci. USA 95: 3742–3751.
Evans, E.K., T. Kuwana, S.L. Strum, J.J. Smith, D.D. Newmeyer &; S. Kornbluth, 1997. Reaper-induced apoptosis in a vertebrate system. EMBO J. 16: 7372–7381.
Fackenthal, J.D., F.R. Turner &; E.C. Raff, 1993. Tissue-specific microtubule functions in Drosophila spermatogenesis require the beta 2-tubulin isotype-specific carboxy terminus. Dev. Biol. 158: 2132–2136.
Fackenthal, J.D., J.A. Hutchens, F.R. Turner &; E.C. Raff, 1995. Structural analysis of mutations in the Drosophila beta 2-tubulin isoform reveals regions in the beta-tubulin molecular required for general and for tissue-specific microtubule functions. Genetics 139: 267–286.
Fortini, M.E., M.A. Simon &; G.M. Rubin, 1992. Signalling by the sevenless protein tyrosine kinase is mimicked by Ras1 activation. Nature 355: 559–561.
Franke, A. &; B.S. Baker, 2000. Dosage compensation. Curr. Opin. Cell. Biol. 12: 351–354.
Franz, G. &; C. Savakis, 1991. Minos, a new transposable element from Drosophila hydei, is a member of the Tc-1-like family of transposons. Nucl. Acids Res. 19: 6646.
Franz, G.F., Ph. Kerremans, P. Rendon &; J. Hendrichs, 1996. Development and application of genetic sexing systems for the Mediterranean fruit fly based on a temperature sensitive lethal, pp. 185–193 in Fruit Fly Pests: A World Assessment of Their Biology and Management, edited by B.A. McPheron &; G.J. Steck. St. Lucie Press, Orlando, FL.
Fraser, M.J., 2000. The TTAA-specific family of transposable elements: identification, functional characterization, and utility for transformation of insects, pp. 248–268 in Insect Transgenesis: Methods and Applications, edited by A.M. Handler &; A.A. James. CRC Press, Boca Raton, FL.
Fraser, M.J., G.E. Smith &; M.D. Summers, 1983. Acquisition of host-cell DNA-sequences by baculoviruses-relationship between host DNA insertions and FP mutants of Autographacalifornicaand Galleria mellonellanuclear polyhedrosis viruses. J. Virol. 47: 287–300.
Fryxell, K.J. &; T.A. Miller, 1995. Autocidal biological control: a general strategy for insect control based on genetic transformation with a highly conserved gene. Biol. Microbiol. Contr. 88: 1221–1232.
Furlong, E.E., D. Profitt &; M.P. Scott, 2001. Automated sorting of live transgenic embryos. Nat. Biotechnol. 19: 153–156.
Gossen, M. &; H. Bujard, 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89: 5547–5551.
Gossen, M., S. Freundlieb, G. Bender, G. Muller, W. Hillen &; H. Bujard, 1995. Transcriptional activation by tetracyclines in mammalian cells. Science 268: 1766–1769.
Grether, M.E., J.M. Abrams, J. Agapite, K. White &; H. Steller, 1995. The head involution defective gene of Drosophila melanogasterfunctions in programmed cell death. Genes Dev. 9: 1694–1708.
Hagler, J.R. &; C.G. Jackson, 2001. Methods for marking insects: current techniques and future prospects. Annu. Rev. Entomol. 46: 511–543.
Handler, A.M., 1992. Molecular genetic mechanisms for sexspecific selection, pp. 11–32 in Advances in Insect Rearing for Research and PestManagement, edited by T.E. Anderson &; N.C. Leppla. Westview Press, Boulder, CO.
Handler, A.M., 1997. Developmental regulation of yolk protein gene expression in Anastrepha suspensa. Arch. Insect Biochem. Physiol. 36: 25–35.
Handler, A.M., 2001. A current perspective on insect gene transfer. Insect Biochem. Mol. Biol. 31: 111–128.
Handler, A.M. &; R.A. Harrell, 1999. Germline transformation of Drosophila melanogasterwith the piggyBactransposon vector. Insect Mol. Biol. 8: 449–458.
Handler, A.M. &; R.A. Harrell, 2001a. Transformation of the Caribbean fruit fly with a piggyBactransposon vector marked with polyubiquitin-regulated GFP. Insect Biochem. Mol. Biol. 31: 199–205.
Handler, A.M. &; R.A. Harrell, 2001b. Polyubiquitin-regulated DsRed marker for transgenic insects. Biotechniques 31: 820–828.
Handler, A.M. &; A.A. James, 2000. Insect Transgenesis: Methods and Applications. CRC Press, Boca Raton, FL.
Handler, A.M. &; S.D. McCombs, 2000. The moth transposon, piggyBac, mediates germ-line transformation in the Oriental fruit fly and exists in its genome. Insect Mol. Biol. 9: 605–612.
Handler, A.M., S.P. Gomez &; D.A. O'Brochta, 1993. A functional analysis of the P-element gene-transfer vector in insects. Arch. Insect Biochem. Physiol. 22: 373–384.
Handler, A.M., S.D. McCombs, M.J. Fraser &; S.H. Saul, 1998. The lepidopteran transposon vector, piggyBac, mediates germline transformation in the Mediterranean fruitfly. Insect Mol. Biol. 9: 605–612.
Haymer, D.S. &; J.L. Marsh, 1986. Germ line and somatic instability of a whitemutation in Drosophila mauritianadue to a transposable element. Dev. Genet. 6: 281–291.
Hediger, M., M. Niessen, E.A. Wimmer, A. Dübendorfer &; D. Bopp, 2001. Genetic transformation of the housefly Musca domesticawith the lepidopteran derived transposon piggyBac. Insect Mol. Biol. 10: 113–119.
Heinrich, J.C. &; M.J. Scott, 2000. A repressible female-specific lethal genetic system for making transgenic insect strains suitable for a sterile-release program. Proc. Natl. Acad. Sci. USA 97: 8229–8232.
Heinrichs, V. &; B.S. Baker, 1995. The Drosophila SR protein RBP1 contributes to the regulation of doublesex alternative splicing by recognizing RBP1 RNA target sequences. EMBO J. 14: 3987–4000.
Horn, C., B. Jaunich &; E.A. Wimmer, 2000. Highly sensitive, fluorescent transformation marker for Drosophila transgenesis. Dev. Genes Evol. 210: 623–629.
Hoyle, H.D., J.A. Hutchens, F.R. Turner &; E.C. Raff, 1995. Regulation of beta-tubulin function and expression in Drosophila spermatogenesis. Dev. Genet. 16: 148–170.
Jasinskiene, N., C.J. Coates &; A.A. James, 2000. Structure of Hermes integrations in the germline of the yellow fever mosquito, Aedes aegypti. Insect Mol. Biol. 9: 11–18.
Jasinskiene, N., C.J. Coates, M.Q. Benedict, A.J. Cornel, C.S. Rafferty, A.A. James &; F.H. Collins, 1998. Stable, transposon mediated transformation of the yellow fever mosquito, Aedes aegypti, using the Hermeselement from the housefly. Proc. Natl. Acad. Sci. USA 95: 3743–3747.
Jiang, C., E.H. Baehrecke &; C.S. Thummel, 1997. Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124: 4673–4683.
Kalb, J.M., A.J. DiBenedetto &; M.F. Wolfner, 1993. Probing the function of Drosophila melanogasteraccessory glands by directed cell ablation. Proc. Natl. Acad. Sci. USA 90: 8093–8097.
Kelley, R.L., I. Solovyeva, L.M. Lyman, R. Richman, V. Solovyev &; M.I. Kuroda, 1995. Expression of msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila. Cell 81: 867–877.
Kemphues, K.J., T.C. Kaufman, R.A. Raff &; E.C. Raff, 1982. The testis-specific β-tubulin subunit in Drosophila melanogasterhas multiple functions in spermatogenesis. Cell 31: 655–670.
Kistner, A., M. Gossen, F. Zimmermann, J. Jerecic, C. Ullmer, H. Lubbert &; H. Bujard, 1996. Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice. Proc. Natl. Acad. Sci. USA 93: 10933–10938.
Kondo, T., T. Yokokura &; S. Nagata, 1997. Activation of distinct caspase-like proteases by fas and reaper in Drosophila cells. Proc. Natl. Acad. Sci. USA 94: 11951–11956.
Lidholm, D.A., A.R. Lohe &; D.L. Hartl, 1993. The transposable element marinermediates germline transformation in Drosophila melanogaster. Genetics 134: 859–868.
Lobo, N.F., A. Hua-Van, X. Li, B.M. Nolen &; M.J. Fraser, 2002. Germ line transformation of the yellow fever mosquito, Aedes aegypti, mediated by transpositional insertion of a piggyBacvector. Insect Mol. Biol. 11: 133–139.
Loukeris, T.G., I. Livadaras, B. Arca, S. Zabalou &; C. Savakis, 1995. Gene transfer into the Medfly, Ceratitis capitata, with a Drosophila hydeitransposable element. Science 270: 2002–2005.
Marin, I., M.L. Siegal &; B.S. Baker, 2000. The evolution of dosagecompensation mechanisms. Bioessays 22: 1106–1114.
Matz, M.V., A.F. Fradkov, Y.A. Labas, A.P. Savitsky, A.J. Zaraisky, M.L. Markelov &; S.A. Lukyanov, 1999. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat. Biotechnol. 17: 969–973.
Medhora, M.M., A.H. MacPeek &; D.L. Hartl, 1988. Excision of the Drosophilatransposable element mariner: identification and characterization of the Mosfactor. EMBO J. 7: 2185–2189.
Michel, K., A. Stamenova, A.C. Pinkerton, G. Franz, A.S. Robinson, A. Gariou-Papalexiou, A. Zacharopoulou, D.A. O'Brochta &; P.W. Atkinson, 2001. Hermes-mediated germ-line transformation of the Mediterranean fruit fly Ceratitis capitata. Insect Mol. Biol. 10: 155–162.
Moffat, K.G., J.H. Gould, H.K. Smith &; C.J. O'Kane, 1992. Inducible cell ablation in Drosophila by cold-sensitive ricin A chain. Development 114: 681–687.
Nassif, C., A. Daniel, J.A. Lengyel, V. Hartenstein &; C. Nassif, 1998. The role of morphogenetic cell death during Drosophila embryonic head development. Dev. Biol. 197: 170–186.
Nurminsky, D.I., M.V. Nurminskaya, D. De Aguiar &; D.L. Hartl, 1998. Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature 396: 572–575.
O'Brochta, D.A. &; P.W. Atkinson, 1996. Transposable elements and gene transformation in non-drosophilids. Insect Biochem. Mol. Biol. 26: 739–753.
O'Brochta, D.A., P.W. Atkinson &; M.J. Lehane, 2000. Transformation of Stomoxys calcitranswith a Hermes gene vector. Insect Mol. Biol. 9: 531–538.
O'Brochta, D.A., W.D. Warren, K.J. Saville &; P.W. Atkinson, 1995. Hermes, a functional non-drosophilid insect gene vector. Genetics 142: 907–914.
Peloquin, J.J., S. Thibault, R. Staten &; T.A. Miller, 2000. Germ-line transformation of pink bollworm (Lepidoptera: Gelechiidae) mediated by the piggyBactransposable element. InsectMol. Biol. 9: 323–333.
Perera, O.P., R.A. Harrell &; A.M. Handler, 2002. Germ-line transformation of the South American malaria vector, Anopheles albimanus, with a piggyBac/EGFPtransposon vector is routine and highly efficient. Insect Mol. Biol. 11: 291–297.
Pinkerton, A.C., K.D. Michel, D.A. O'Brochta &; P.W. Atkinson, 2000. Green fluorescent protein as a genetic marker in transgenic Aedes aegypti. Insect Mol. Biol. 9: 1–10.
Prasher, D.C., V.K. Eckenrode, W.W. Ward, F.G. Prendergast &; M.J. Cormier, 1992. Primary structure of the Aequorea victoriagreen fluorescent protein. Gene 111: 229–233.
Pronk, G.J., K. Ramer, P. Amiri &; L.T. Williams, 1996. Requirement of an ICE-like protease for induction of apoptosis and ceramide generation by REAPER. Science 271: 808–810.
Raff, E.C., J.D. Fackenthal, J.A. Hutchens, H.D. Hoyle &; F.R. Turner, 1997. Microtubule architecture specified by a β-tubulin isoform. Science 275: 70–73.
Ryner, L.C. &; B.S. Baker, 1991. Regulation of doublesex premRNA processing occurs by 149-1-splice site activation. Genes Dev. 5: 2071–2085.
Saccone, G., I. Peluso, D. Artiaco, E. Giordano, D. Bopp &; L.C. Polito, 1998. The Ceratitis capitatahomologue of the Drosophila sex-determining gene sex-lethal is structurally conserved, but not sex-specifically regulated. Development 125: 1495–1500.
Sarkar, A., C.J. Coates, S. Whyard, U. Willhoeft, P.W. Atkinson &; D.A. O'Brochta, 1997. The Hermes element from Musca domesticacan transpose in four families of cyclorrhaphan flies. Genetica 99: 15–29.
Shearman, D.C. &; M. Frommer, 1998. The Bactrocera tryonihomologue of the Drosophila melanogastersex-determination gene doublesex. Insect Mol. Biol. 7: 355–366.
Sosnowski, B.A., J.M. Belote &; M. McKeown, 1989. Sex-specific alternative splicing of RNA from the transformergene results from sequence-dependent splice site blockage. Cell 58: 449–459.
Sosnowski, B.A., D.D. Davis, R.T. Boggs, S.J. Madigan &; M. McKeown, 1994. Multiple portions of a small region of the Drosophila transformer gene are required for efficient in vivosex-specific regulated RNA splicing and in vitrosex-lethal binding. Dev. Biol. 161: 302–312.
Sundararajan, P., P.W. Atkinson &; D.A. O'Brochta, 1999. Transposable element interactions in insects: crossmobilization of hoboand Hermes. Insect Mol. Biol. 8: 359–368.
Tamura, T., C. Kunert &; J. Postlethwait, 1985. Sex-and cell-specific regulation of yolk polypeptide genes introduced into Drosophila by P-element-mediated gene transfer. Proc. Natl. Acad. Sci. USA 82: 7000–7004.
Tamura, T., T. Thibert, C. Royer, T. Kanda, A. Eappen, M. Kamba, N. Kômoto, J.-L. Thomas, B.M.G. Chavancy, P. Shirk, M. Fraser, J.-C. Prud'homme &; P. Couble, 2000. A piggyBacelementderived vector efficiently promotes germ-line transformation in the silkworm Bombyx moriL. Nat. Biotechnol. 18: 81–84.
Thomas, D.T., C.A. Donnelly, R.J. Wood &; L.S. Alphey, 2000. Insect population control using a dominant, repressible, lethal genetic system. Science 287: 2474–2476.
Vucic, D., S. Seshagiri &; L.K. Miller, 1997. Characterization of reaper-and FADD-induced apoptosis in a lepidopteran cell line. Mol. Cell. Biol. 17: 667–676.
Warren, W.D., P.W. Atkinson &; D.A. O'Brochta, 1994. The Hermestransposable element from the house fly, Musca domestica, is a short inverted repeat-type element of the hobo, Ac, and Tam3 (hAT) element family. Genet. Res. Camb. 64: 87–97.
White, K., E. Tahaoglu &; H. Steller, 1996. Cell killing by the Drosophila gene reaper. Science 271: 805–807.
White, K., M.E. Grether, J.M. Abrams, L. Young, K. Farrell &; H. Steller, 1994. Genetic control of programmed cell death in Drosophila. Science 264: 677–683.
Wing, J.P., L. Zhou, L.M. Schwartz &; J.R. Nambu, 1998. Distinct cell killing properties of the Drosophila reaper, head involution defective, and grim genes. Cell Death Differ. 5: 930–939.
Yoshiyama, M., H. Honda &; K. Kimura, 2000. Successful transformation of the housefly, Musca domestica(Diptera: Muscidae) with the transposable element, mariner. Appl. Entomol. Zool. 35: 321–325.
Zhou, L., A. Schnitzler, J. Agapite, L.M. Schwartz, H. Steller &; J.R. Nambu, 1997. Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system midline cells. Proc. Natl. Acad. Sci. USA 94: 5131–5136.
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Handler, A.M. Prospects for Using Genetic Transformation for Improved SIT and New Biocontrol Methods. Genetica 116, 137–149 (2002). https://doi.org/10.1023/A:1020924028450
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DOI: https://doi.org/10.1023/A:1020924028450