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The art and design of genetic screens: Drosophila melanogaster
Abstract
The success of Drosophila melanogaster as a model organism is largely due to the power of forward genetic screens to identify the genes that are involved in a biological process. Traditional screens, such as the Nobel-prize-winning screen for embryonic-patterning mutants, can only identify the earliest phenotype of a mutation. This review describes the ingenious approaches that have been devised to circumvent this problem: modifier screens, for example, have been invaluable for elucidating signal-transduction pathways, whereas clonal screens now make it possible to screen for almost any phenotype in any cell at any stage of development.
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“Genetic modifier screens are commonly applied to identify genes that act in developmental or biochemical pathways in fruit flies, worms, and bacteria10; however, this approach is rare in the mouse11,12.”
From A suppressor screen in Mecp2 mutant mice implicates cholesterol metabolism in Rett syndrome (2013) · cites this paper as [10]
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A suppressor screen in Mecp2 mutant mice implicates cholesterol metabolism in Rett syndrome
Buchovecky, C. M., Turley, S. D., Brown, H. M., Kyle, S. M., McDonald, J. G., Liu, B., Pieper, A. A., Huang, W., Katz, D. M., Russell, D. W., et al. (2013) · Nature Genetics · doi:10.1038/ng.2714 · Cited by 234
Using next-generation sequencing to isolate mutant genes from forward genetic screens
Schneeberger, K. (2014) · Nature reviews genetics · doi:10.1038/nrg3745 · Cited by 233
Chapter 3 Neurogenetics of Courtship and Mating in Drosophila
Villella, A., & Hall, J. C. (2008) · Advances in genetics · doi:10.1016/s0065-2660(08)00603-2 · Cited by 209
Ryder, E., Blows, F., Ashburner, M., Bautista-Llácer, R., Coulson, D., Drummond, J., Webster, J., Gubb, D., Gunton, N., Johnson, G., et al. (2004) · Genetics · doi:10.1534/genetics.104.026658 · Cited by 220
“The powerful approach with Drosophila is the ability to rap-subsequent molecular cloning of the genes involved in idly carry out focused genome-wide screens for path-such pathways has shown how evolution has utilized way components by identifying loci that modify specificbasic molecular building blocks to control a wi…”
BackgroundInfluentialNFκB pathway: A good signaling paradigm and therapeutic target
Tergaonkar, V. (2006) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2006.03.023 · Cited by 219
Caspase-Dependent Cell Death inDrosophila
Hay, B. A., & Guo, M. (2006) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.21.012804.093845 · Cited by 201
“1:397–409 St. Johnston D. 2002.”
BackgroundDahmann, C. (2020) · Methods in Molecular Biology · doi:10.1007/978-1-4939-6371-3 · Cited by 213
Reactive oxygen species: A radical role in development?
Hernández-García, D., Wood, C. D., Castro‐Obregón, S., & Covarrubias, L. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.03.020 · Cited by 199
“Much effort has been invested in sequencing of the genomes of the major model organisms (Caenorhabditis elegans (worm) [93], Drosophila melanogaster (fruitfly) [94], Danio rerio (zebrafish) [95], and Mus musculus (mouse) [96]), a task that is nearing completion.”
BackgroundEusocial insects as emerging models for behavioural epigenetics
Yan, H., Simola, D. F., Bonasio, R., Liebig, J., Berger, S. L., & Reinberg, D. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3787 · Cited by 203
The SILAC Fly Allows for Accurate Protein Quantification in Vivo*
Sury, M., Chen, J.-X., & Selbach, M. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.000323 · Cited by 185
Systematic Approaches to Toxicology in the Zebrafish
Peterson, R. T., & MacRae, C. A. (2011) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010611-134751 · Cited by 178
Carpinelli, M. R., Hilton, D. J., Metcalf, D., Antonchuk, J. L., Hyland, C. D., Mifsud, S. L., Di Rago, L., Hilton, A. A., Willson, T. A., Roberts, A. W., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401496101 · Cited by 179
Loss-of-function genetic tools for animal models: cross-species and cross-platform differences
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Clustering phenotype populations by genome‐wide RNAi and multiparametric imaging
Fuchs, F., Pau, G., Kranz, D., Sklyar, O., Budjan, C., Steinbrink, S., Horn, T. L., Pedal, A., Huber, W. K., & Boutros, M. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.25 · Cited by 160
“Forward genetic screens for visual phenotypes in model organisms have proven a powerful method for associating phenotypes with genes and for the prediction of functional relationships (Jorgensen and Mango, 2002; St Johnston, 2002).”
Making waves in cancer research: new models in the zebrafish.
Berghmans, S., Jette, C. A., Langenau, D. M., Hsu, K., Stewart, R., Look, T., & Kanki, J. P. (2005) · BioTechniques · doi:10.2144/05392rv02 · Cited by 170
The iBeetle large-scale RNAi screen reveals gene functions for insect development and physiology
Schmitt-Engel, C., Schultheis, D., Schwirz, J., Ströhlein, N., Troelenberg, N., Majumdar, U., Dao, V. A., Grossmann, D., Richter, T., Tech, M., et al. (2015) · Nature Communications · doi:10.1038/ncomms8822 · Cited by 164
“T he importance of Drosophila melanogaster as a model system is in large part due to its amenability to elegant genetic screens, which allow the comprehensive identification of genes required for a given biological process 1,2 .”
BackgroundDevelopment and structure of synaptic contacts in Drosophila
Prokop, A., & Meinertzhagen, I. A. (2005) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2005.11.010 · Cited by 154
Genetics of Aging in the Fruit Fly,Drosophila melanogaster
Helfand, S. L., & Rogina, B. (2003) · Annual Review of Genetics · doi:10.1146/annurev.genet.37.040103.095211 · Cited by 152
Organ Size Control: Lessons from Drosophila
Hariharan, I. K. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.07.012 · Cited by 144
“Mutations that perturb growth have been identified using a variety of approaches in Drosophila (reviewed in Hariharan and Bilder, 2006; St Johnston, 2002).”
BackgroundHormonal and nutritional regulation of insect fat body development and function.
Liu, Y., Liu, H., Liu, S.-M., Wang, S., Jiang, R., & Li, S. (2009) · Archives of Insect Biochemistry and Physiology · doi:10.1002/arch.20290 · Cited by 141
“Using the powerful Drosophila screen approaches (i.e. traditional, modifier, and mosaic screens) and genetic manipulations (i.e. UAS-Gal4, FRT-Plp, and MARCM), many oncogenes and tumor suppressors have been identified (Duffy, 2002; Johnston, 2002).”
BackgroundViruses and antiviral immunity in Drosophila
Xu, J., & Cherry, S. R. (2013) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2013.05.002 · Cited by 146
“For example, many of the classic signal transduction systems were first identified in Drosophila using forward genetic screens and were subsequently found to be conserved in mammalian hosts (Nüsslein-Volhard and Wieschaus, 1980; Ribeiro et al., 2003; Simon, 1994; St Johnston, 2002).”
BackgroundThe legacy of Drosophila imaginal discs
Beira, J. V., & Paro, R. (2016) · Chromosoma · doi:10.1007/s00412-016-0595-4 · Cited by 184
“For example, epistasis experiments clarified the role of spitz as a ligand that can bind to the Egf receptor (torpedo), leading to the activation of downstream kinases encoded by ras and raf and culminating in transcriptional regulation by Pointed (Kumar 2001; St Johnston 2002).”
InfluentialHu, C.-Y., & Aksoy, S. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05180.x · Cited by 130
“RNAi-mediated silencing of attacin expression RNAi-based silencing has been effectively mediated by the expression of hairpin double-stranded (ds) RNA in transgenic Drosophila strains (St Johnston, 2002), as well as by direct intrathoracic injection of dsRNA in mosquitoes (Blandin et al ., 2002).”
BackgroundRead, R. D., Fenton, T. R., Gomez, G. G., Wykosky, J., VandenBerg, S. R., Babić, I., Iwanami, A., Yang, H., Cavenee, W. K., Mischel, P. S., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003253 · Cited by 131
“Flies have orthologs for 75% of human disease genes [10], including nearly all known gliomagenic genes; signaling pathways are highly conserved; versatile genetic tools are available for cell-type specific gene manipulation [11,12]; and Drosophila neural cell types are homologous to their mammalian counterparts [13,14…”
BackgroundiBeetle-Base: a database for RNAi phenotypes in the red flour beetle Tribolium castaneum
Dönitz, J., Schmitt-Engel, C., Grossmann, D., Gerischer, L., Tech, M., Schoppmeier, M., Klingler, M., & Bucher, G. (2014) · Nucleic Acids Res. · doi:10.1093/nar/gku1054 · Cited by 125
“So far, within insects, only the fruit fly Drosophila melanogaster has offered the possibility of saturated forward genetic screens and, hence, most of what we know about insect gene functions is derived from this species (1,2).”
BackgroundLarge-Scale Transgenic Drosophila Resource Collections for Loss- and Gain-of-Function Studies
Zirin, J. D., Hu, Y., Liu, L., Yang‐Zhou, D., Colbeth, R., Yan, D., Ewen‐Campen, B., Tao, R., Vogt, E., VanNest, S., et al. (2020) · Genetics · doi:10.1534/genetics.119.302964 · Cited by 125
“LOF was classically achieved in vivo in Drosophila using random mutagenesis (St Johnston 2002) and in more recent years, is achieved by knockdown using RNA interference (RNAi) (Dietzl et al. 2007), or knockout using CRISPR-Cas9 (Port et al. 2014).”
BackgroundTetrahymena as a Unicellular Model Eukaryote: Genetic and Genomic Tools
Ruehle, M. D., Orias, E., & Pearson, C. G. (2016) · Genetics · doi:10.1534/genetics.114.169748 · Cited by 123
“…screening of mutants entails the rapid assessment of cells for classes of phenotypes (Forsburg 2001; Patton and Zon 2001; Casselton and Zolan 2002; Jorgensen and Mango 2002; Page and Grossniklaus 2002; St Johnston 2002; Shuman and Silhavy 2003; Kile and Hilton 2005; Candela and Hake 2008).”
BackgroundRunx3 Inactivation Is a Crucial Early Event in the Development of Lung Adenocarcinoma
Lee, Y., Lee, J.-W., Jang, J., Chi, X., Kim, J., Li, Y., Kim, M., Kim, D.-M., Choi, B.-S., Kim, E., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.10.003 · Cited by 126
Feng, H., Langenau, D. M., Madge, J. A., Quinkertz, A., Gutiérrez, A., Neuberg, D. S., Kanki, J. P., & Look, A. T. (2007) · British Journal of Haematology · doi:10.1111/j.1365-2141.2007.06625.x · Cited by 120
“Although genetic screens designed to identify enhancers or suppressors of a given phenotype have been successfully performed in invertebrate systems, such as Drosophila. melanogaster (St Johnston, 2002), invertebrate models are generally limited in their recapitulation of human disease pathologies.”
BackgroundRegulation of organ size: Insights from the Drosophila Hippo signaling pathway
Kango‐Singh, M., & Singh, A. (2009) · Developmental Dynamics · doi:10.1002/dvdy.21996 · Cited by 107
O'Kane, C. (2002) · doi:10.1006/rwgn.2001.1698 · Cited by 116
Modeling human neurodegenerative diseases in transgenic systems
Sosa, M. A. G., Gasperi, R. D., & Elder, G. A. (2011) · Human Genetics · doi:10.1007/s00439-011-1119-1 · Cited by 114
The art and design of genetic screens: mouse
Kile, B. T., & Hilton, D. J. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1636 · Cited by 104
Microfluidic chamber arrays for whole-organism behavior-based chemical screening
Chung, K., Zhan, M., Srinivasan, J., Sternberg, P., Gong, E. S., Schroeder, F. C., & Lu, H. (2011) · Lab on a Chip · doi:10.1039/c1lc20400a · Cited by 113
The Epicurean Fly: Using Drosophila Melanogaster to Study Metabolism
Bharucha, K. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e318191fc68 · Cited by 113
“Unbiased forward genetic screens are a staple of Drosophila research; they provide the opportunity for the establishment of new and unexpected paradigms that can sometimes elude hypothesis-driven research (23,24).”
BackgroundChapter 3 Mapping and Manipulating Neural Circuits in the Fly Brain
Simpson, J. H. (2009) · Advances in genetics · doi:10.1016/s0065-2660(09)65003-3 · Cited by 105
Drosophila as a Model to Study Mitochondrial Dysfunction in Parkinson's DiseasePreprint
Guo, M. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a009944 · Cited by 111
Storkebaum, E., Leitão-Gonçalves, R., Godenschwege, T., Nangle, L., Mejía, M., Bosmans, I., Ooms, T., Jacobs, A., van Dijck, P., Yang, X.-L., et al. (2009) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0905339106 · Cited by 108
“S5), which can be used in future genetic screens for putative disease modifying genes, an experimental approach for which Drosophila is ideally suited (23).”
BackgroundBarata, D. B., van Blitterswijk, C., & Habibović, P. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.09.009 · Cited by 128
“Such models are not only useful in developmental, genetic and disease studies, but they may also aid development of organ- and tissue regenerative strategies [44,46].”
BackgroundDrosophila melanogaster Oogenesis: An Overview
McLaughlin, J. M., & Bratu, D. P. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2851-4_1 · Cited by 125
Luschnig, S., Moussian, B., Krauss, J., Desjeux, I., Perković, J., & Nüsslein-Volhard, C. (2004) · Genetics · doi:10.1534/genetics.167.1.325 · Cited by 106
“…induced mutations: Although chemical mutagenesis has proven highly effi-female-sterile screen (Schüpbach and Wieschaus 1989; reviewed in St. Johnston 2002) and the two generations cient in terms of allowing rapid isolation of large numbers of mutants, genetic mapping of chemically…”
BackgroundInfluentialThe genetics of cell death: approaches, insights and opportunities in Drosophila
Hay, B. A., Huh, J. R., & Guo, M. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1491 · Cited by 108
“In addition, the development of sophisticated genetic screens makes it possible to search for genes that participate in particular signal-transduction pathways or biological processes in essentially any cell type (reviewed in Ref”
BackgroundComparative mapping of the 22q11.2 deletion region and the potential of simple model organisms
Guna, A., Butcher, N. J., & Bassett, A. S. (2015) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-015-9113-x · Cited by 117
Westermann, B. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.12.003 · Cited by 105
Drosophila as a screening tool to study human neurodegenerative diseases
Lenz, S., Karsten, P., Schulz, J. B., & Voigt, A. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12446 · Cited by 101
“Reverse genetic screens explore the functions of predefined genes (St Johnston 2002).”
BackgroundIn vivo assessment of CdSe-ZnS quantum dots: coating dependent bioaccumulation and genotoxicity.
Galeone, A., Vecchio, G., Malvindi, M., Brunetti, V., Cingolani, R., & Pompa, P. (2012) · Nanoscale · doi:10.1039/c2nr31826a · Cited by 93
Drosophila Models of Parkinson's Disease
Whitworth, A. J. (2011) · Advances in genetics · doi:10.1016/b978-0-12-380860-8.00001-x · Cited by 110
“There are a large number of approaches available for conducting genetic modifier screens in Drosophila (St. Johnston, 2002).”
MethodTranscription Factor Networks in Drosophila melanogaster
Rhee, D. Y., Cho, D.-Y., Zhai, B., Slattery, M. G., Ma, L., Mintseris, J., Wong, C. Y., White, K. P., Celniker, S., Przytycka, T. M., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.08.038 · Cited by 92
“Genetic screens, especially in Drosophila, have been used as a powerful tool to define networks of proteins that share function (Fortini and Artavanis-Tsakonas, 1994; Go and Artavanis-Tsakonas, 1998; Sen et al., 2013; St Johnston, 2002; Xu and ArtavanisTsakonas, 1990).”
MethodUse of model organisms for the study of neuronal ceroid lipofuscinosis
Bond, M., Holthaus, S.-M. K., Tammen, I., Tear, G., & Russell, C. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.01.009 · Cited by 92
Tinman/Nkx2-5 acts via miR-1 and upstream of Cdc42 to regulate heart function across species
Qian, L., Wythe, J. D., Liu, J.-D., Cartry, J., Vogler, G., Mohapatra, B., Otway, R., Huang, Y., King, I. N., Maillet, M., et al. (2011) · Journal of Cell Biology · doi:10.1083/jcb.201006114 · Cited by 90
“…to identify molecular–genetic pathways involved in cardiac contractility and rhythm can now be executed, leading to the identification of novel cardiac regulators that can then be examined in mammals (Adams and Sekelsky, 2002; St Johnston, 2002; Wessells and Bodmer, 2004; Neely et al., 2010).”
BackgroundThe expanding role of mouse genetics for understanding human biology and disease
Nguyen, D. N., & Xu, T. (2008) · Disease Models & Mechanisms · doi:10.1242/dmm.000232 · Cited by 83
“Extensively used in lower organism models, modifier screens have made a great impact on our understanding and the uncovering of major signaling pathways that regulate developmental and biological processes (Jorgensen and Mango, 2002; St Johnston, 2002).”
BackgroundIyer, J. S., Wang, Q., Le, T., Pizzo, L., Grönke, S., Ambegaokar, S. S., Imai, Y., Srivastava, A., Troisí, B. L., Mardon, G., et al. (2016) · G3 Genes Genomes Genetics · doi:10.1534/g3.116.027060 · Cited by 92
“Drosophila provides awealthofgenetic,cellular,andmolecularbiologytools,whichhavebeen instrumentalinunderstandingbasicbiologicalprocesses(StJohnston 2002).”
CoinFLP: a system for efficient mosaic screening and for visualizing clonal boundaries in Drosophila
Bosch, J. A., Tran, N.-H., & Hariharan, I. K. (2015) · Development · doi:10.1242/dev.114603 · Cited by 81
“Many of the genes that regulate development in a variety of organisms have been discovered in genetic screens that utilize the Drosophila eye (St Johnston, 2002).”
BackgroundRad, R., Rad, L., Wang, W. T., Strong, A., Ponstingl, H., Bronner, I. F., Mayho, M., Steiger, K., Weber, J., Hieber, M., et al. (2014) · Nature Genetics · doi:10.1038/ng.3164 · Cited by 83
Chari, S., & Dworkin, I. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003661 · Cited by 84
A Drosophila Model of Alzheimer's Disease
Crowther, D. C., Page, R., Chandraratna, D., & Lomas, D. A. (2006) · Methods in Enzymology · doi:10.1016/s0076-6879(06)12015-7 · Cited by 55
Li, M., Yu, J., Tilgner, K., Ong, S. H., Koike-Yusa, H., & Yusa, K. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.027 · Cited by 96
“Hypothe-sis-free forward genetics applied in yeast, Drosophila , and Caenorhabditis elegans has provided deeper insights into diverse biological processes (Forsburg, 2001; Jorgensen and Mango, 2002; St Johnston, 2002).”
Extracellular matrix and its receptors indrosophilaneural development
Broadie, K. S., Baumgartner, S., & Prokop, A. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20935 · Cited by 77
“…recording combine with sophisticated and versatile genetic research strategies, including conducting unbiased screens for molecules contributing to neurological processes of interest (St Johnston, 2002; Venken and Bellen, 2005; Venken et al., 2009; Giacomotto and Segalat, 2010; Zhang et al., 2010).”
BackgroundTripathi, B. K., & Irvine, K. D. (2022) · Genetics · doi:10.1093/genetics/iyac020 · Cited by 136
Dujardin, S., Colin, M., & Buée, L. (2014) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12200 · Cited by 101
Tailoring the genome: the power of genetic approaches
Nagy, A., Perrimon, N., Sandmeyer, S. B., & Plasterk, R. H. A. (2003) · Nature Genetics · doi:10.1038/ng1115 · Cited by 75
Fradkin, L., Kamphorst, J., Diantonio, A., Goodman, C., & Noordermeer, J. N. (2002) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.212511099 · Cited by 80
Recombinases and their use in gene activation, gene inactivation, and transgenesis.
Bischof, J., & Basler, K. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-583-1_10 · Cited by 80
The Maize Oil Yellow1 (Oy1) Gene Encodes the I Subunit of Magnesium Chelatase
Sawers, R. J. H., Viney, J., Farmer, P. R., Bussey, R. R., Olsefski, G. T., Anufrikova, K., Hunter, C., & Brutnell, T. (2005) · Plant Molecular Biology · doi:10.1007/s11103-005-2880-0 · Cited by 80
Whole-animal imaging, gene function, and the Zebrafish Phenome Project
Cheng, K. C., Xin, X., Clark, D. P., & Rivière, P. J. L. (2011) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2011.08.006 · Cited by 77
Systematic quantification of gene interactions by phenotypic array analysis
Hartman, J. L., & Tippery, N. P. (2004) · Genome biology · doi:10.1186/gb-2004-5-7-r49 · Cited by 68
“In contrast, experimental genetic methods relying on inbred genetic backgrounds and controlled environments have found phenotypic enhancement and suppression to be ubiquitous [5-7].”
Botham, C. M., Wandler, A. M., & Guillemin, K. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000064 · Cited by 76
“Finally, Drosophila are amenable to forward genetic approaches that will facilitate the discovery of host factors required for CagA function in eukaryotic cells [22].”
BackgroundGoto, A., Blandin, S., Royet, J., Reichhart, J., & Levashina, E. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg852 · Cited by 76
“melanogaster (8,9), gene silencing in Drosophila adults is mainly achieved by establishment of transgenic strains expressing hairpin constructs against the targeted genes (1).”
Panchal, K., & Tiwari, A. K. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.03.001 · Cited by 85
Mirkovic, I., & Mlodzik, M. (2006) · Development · doi:10.1242/dev.02468 · Cited by 65
“To minimize the RhoAassociated defects that are not linked to rotation [e.g. general cellular architecture as RhoA null clones are cell lethal (Strutt et al., 1997)], we expressed UAS-RhoAIR [lowering endogenous RhoA levels through RNA interference (Billuart et al., 2001)] in the R3/R4 precursors.”
Kim, Y. Y., Um, J., Yoon, J.-H., Kim, H.-J., Lee, D., Lee, Y. J., Jee, H. J., Kim, Y. M., Jang, J. S., Jang, Y., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201900073r · Cited by 87
“Powerful and convenient genetic tools aremajor advantages of theDrosophilamodel (42, 43).”
BackgroundVenken, K. J. T., & Bellen, H. J. (2014) · Methods · doi:10.1016/j.ymeth.2014.02.025 · Cited by 78
Drosophila melanogaster and the development of biology in the 20th century.
Arias, A. M. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-583-1_1 · Cited by 72
The quest for the best target genes for RNAi ‐mediated pest control
Cedden, D., & Bucher, G. (2024) · Insect Molecular Biology · doi:10.1111/imb.12966 · Cited by 65
Drosophila Models of Tauopathies: What Have We Learned?
Gistelinck, M., Lambert, J., Callaerts, P., Dermaut, B., & Dourlen, P. (2012) · International Journal of Alzheimer s Disease · doi:10.1155/2012/970980 · Cited by 60
“All these tools give to researchers using Drosophila the possibility to perform in-depth reverse genetic studies as well as large-scale forward genetic screens, enabling the identification of novel biological pathways in an unbiased manner [17].”
Drosophila, Genetic Screens, and Cardiac Function
Wolf, M. J., & Rockman, H. A. (2011) · Circulation Research · doi:10.1161/circresaha.111.244897 · Cited by 62
Discovery and Use of Small Molecules for Probing Biological Processes in Zebrafish
Peterson, R. T., & Fishman, M. C. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)76026-4 · Cited by 70
Large-scale identification of chemically induced mutations in Drosophila melanogasterPreprint
Haelterman, N. A., Jiang, L.-C., Li, Y.-M., Bayat, V., Sandoval, H., Ugur, B., Tan, K., Zhang, K., Bei, D., Xiong, B., et al. (2014) · Genome Research · doi:10.1101/gr.174615.114 · Cited by 68
“Numerous mutagenesis screens have been performed since the introduction of Drosophila as a model organism (St. Johnston 2002).”
Metadata
- Authors
- St Johnston, D.
- Venue
- Nature Reviews Genetics
- Published
- 2002-03
- Volume
- 3
- Issue
- 3
- Pages
- 176-188
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2027125425
- Cited by
- 644
- References
- 0
- Citations by year
- 2026: 7 · 2025: 17 · 2024: 26 · 2023: 23 · 2022: 25 · 2021: 28 · 2020: 40 · 2019: 33 · 2018: 38 · 2017: 29 · 2016: 30 · 2015: 40 · 2014: 41 · 2013: 32 · 2012: 36
- FWCI
- 1.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Diptera species taxonomy and behavior
- Keywords
- forward genetic screen, Drosophila melanogaster, modifier screen, embryonic patterning, signaling pathways
- MeSH terms
- Animals, Crosses, Genetic, Drosophila melanogaster, Enhancer Elements, Genetic, Eye, Female, Genetic Testing, Male, Phenotype, Gene Expression, Genes, Suppressor, Mutagenesis, Genes, Insect
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