Plug-and-play genetic access to drosophila cell types using exchangeable exon cassettes

Cell Reports

Volumn 10, Issue 8, 2015, Pages 1410-1421

  Diao, Fengqiu ^a   Ironfield, Holly ^b   Luan, Haojiang ^a   Diao, Feici ^a   Shropshire, William C ^a   Ewer, John ^d   Marr, Elizabeth ^c   Potter, Christopher J ^c   Landgraf, Matthias ^b   White, Benjamin H ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSIDAD DE VALPARAÍSO   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DROSOPHILA; EXON; GAL4 GENE; GENE CASSETTE; GENE EXPRESSION; GENE SEQUENCE; GENETIC CODE; GENETIC MODEL; GENETIC PROCEDURES; GLUTAMATERGIC NERVE CELL; IN VIVO STUDY; INTRON; LARVAL STAGE; NERVE CELL; NONHUMAN; PLUG AND PLAY GENETIC ACCESS; PRIORITY JOURNAL; RNA SPLICING; TRANSGENE; TRANSPOSON; 5' UNTRANSLATED REGION; ANIMAL; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALIA;

5' UNTRANSLATED REGION; DROSOPHILA PROTEIN; GAL4 PROTEIN, DROSOPHILA; RNA SPLICING; TRANSCRIPTION FACTOR;

5' UNTRANSLATED REGIONS; ANIMALS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; DROSOPHILA; DROSOPHILA PROTEINS; EXONS; INTRONS; RNA SPLICE SITES; TRANSCRIPTION FACTORS; TRANSGENES;

EID: 84924533178     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.01.059     Document Type: Article

References (50)

1. Anderson M.S., Halpern M.E., Keshishian H. Identification of the neuropeptide transmitter proctolin in Drosophila larvae: characterization of muscle fiber-specific neuromuscular endings. J.Neurosci. 1988, 8:242-255.
2. Bischof J., Maeda R.K., Hediger M., Karch F., Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 2007, 104:3312-3317.
3. Branda C.S., Dymecki S.M. Talking about a revolution: The impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 2004, 6:7-28.
4. Buckingham S.D., Biggin P.C., Sattelle B.M., Brown L.A., Sattelle D.B. Insect GABA receptors: splicing, editing, and targeting by antiparasitics and insecticides. Mol. Pharmacol. 2005, 68:942-951.
5. Daniels R.W., Gelfand M.V., Collins C.A., DiAntonio A. Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS. J.Comp. Neurol. 2008, 508:131-152.
6. Demir E., Dickson B.J. fruitless splicing specifies male courtship behavior in Drosophila. Cell 2005, 121:785-794.
7. DiAntonio A. Glutamate receptors at the Drosophila neuromuscular junction. Fly Neuromuscular Junction: Structure and Function 2006, 165-179. Elsevier Academic Press. V. Budnik, C. Ruiz-Cañada (Eds.).
8. Diao F., White B.H. A novel approach for directing transgene expression in Drosophila: T2A-Gal4 in-frame fusion. Genetics 2012, 190:1139-1144.
9. Fujioka M., Lear B.C., Landgraf M., Yusibova G.L., Zhou J., Riley K.M., Patel N.H., Jaynes J.B. Even-skipped, acting as a repressor, regulates axonal projections in Drosophila. Development 2003, 130:5385-5400.
10. Gao S., Takemura S.Y., Ting C.Y., Huang S., Lu Z., Luan H., Rister J., Thum A.S., Yang M., Hong S.T., et al. The neural substrate of spectral preference in Drosophila. Neuron 2008, 60:328-342.
11. Gohl D.M., Silies M.A., Gao X.J., Bhalerao S., Luongo F.J., Lin C.C., Potter C.J., Clandinin T.R. A versatile invivo system for directed dissection of gene expression patterns. Nat. Methods 2011, 8:231-237.
12. Gnerer J.P., Venken K.J.T., Dierick H.A. Gene-specific cell labeling using MiMIC transposons. Nucleic Acids Res. 2015, 3. Published online February 20, 2015.
13. Gratz S.J., Cummings A.M., Nguyen J.N., Hamm D.C., Donohue L.K., Harrison M.M., Wildonger J., O'Connor-Giles K.M. Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 2013, 194:1029-1035.
14. Harrison J.B., Chen H.H., Sattelle E., Barker P.J., Huskisson N.S., Rauh J.J., Bai D., Sattelle D.B. Immunocytochemical mapping of a C-terminus anti-peptide antibody to the GABA receptor subunit, RDL in the nervous system in Drosophila melanogaster. Cell Tissue Res. 1996, 284:269-278.
15. Hekmat-Scafe D.S., Mercado A., Fajilan A.A., Lee A.W., Hsu R., Mount D.B., Tanouye M.A. Seizure sensitivity is ameliorated by targeted expression of K+-Cl- cotransporter function in the mushroom body of the Drosophila brain. Genetics 2010, 184:171-183.
16. Honegger H.W., Dewey E.M., Ewer J. Bursicon, the tanning hormone of insects: recent advances following the discovery of its molecular identity. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2008, 194:989-1005.
17. Kitamoto T., Wang W., Salvaterra P.M. Structure and organization of the Drosophila cholinergic locus. J.Biol. Chem. 1998, 273:2706-2713.
18. Kosman D., Small S., Reinitz J. Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev. Genes Evol. 1998, 208:290-294.
19. Kuzin A., Kundu M., Ekatomatis A., Brody T., Odenwald W.F. Conserved sequence block clustering and flanking inter-cluster flexibility delineate enhancers that regulate nerfin-1 expression during Drosophila CNS development. Gene Expr. Patterns 2009, 9:65-72.
20. Lai S.L., Lee T. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 2006, 9:703-709.
21. Livet J., Weissman T.A., Kang H., Draft R.W., Lu J., Bennis R.A., Sanes J.R., Lichtman J.W. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 2007, 450:56-62.
22. Luan H., White B.H. Combinatorial methods for refined neuronal gene targeting. Curr. Opin. Neurobiol. 2007, 17:572-580.
23. Luan H., Peabody N.C., Vinson C.R., White B.H. Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 2006, 52:425-436.
24. Luan H., Diao F., Peabody N.C., White B.H. Command andcompensation in a neuromodulatory decision network. J.Neurosci. 2012, 32:880-889.
25. Luo C.W., Dewey E.M., Sudo S., Ewer J., Hsu S.Y., Honegger H.W., Hsueh A.J. Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2. Proc. Natl. Acad. Sci. USA 2005, 102:2820-2825.
26. Mahr A., Aberle H. The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr. Patterns 2006, 6:299-309.
27. Nagarkar-Jaiswal S., Lee P.-T., Campbell M.E., Chen K., Anguiano-Zarate S., Gutierrez M.C., Busby T., Lin W.-W., He Y., Schulze K.L., et al. A library of MiMICs allows tagging of genes and reversible spatial and temporal knockdown of proteins in Drosophila. eLife 2015, 4. 10.7554/eLife.05338.
28. Park D., Han M., Kim Y.C., Han K.A., Taghert P.H. Ap-let neurons-a peptidergic circuit potentially controlling ecdysial behavior in Drosophila. Dev. Biol. 2004, 269:95-108.
29. Pfeiffer B.D., Ngo T.T., Hibbard K.L., Murphy C., Jenett A., Truman J.W., Rubin G.M. Refinement of tools for targeted gene expression in Drosophila. Genetics 2010, 186:735-755.
30. Potter C.J., Tasic B., Russler E.V., Liang L., Luo L. The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 2010, 141:536-548.
31. Rayburn L.Y.M., Rhea J., Jocoy S.R., Bender M. The proprotein convertase amontillado (amon) is required during Drosophila pupal development. Dev. Biol. 2009, 333:48-56.
32. Ren X., Sun J., Housden B.E., Hu Y., Roesel C., Lin S., Liu L.P., Yang Z., Mao D., Sun L., et al. Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9. Proc. Natl. Acad. Sci. USA 2013, 110:19012-19017.
33. Rhea J.M., Wegener C., Bender M. The proprotein convertase encoded by amontillado (amon) is required in Drosophila corpora cardiaca endocrine cells producing the glucose regulatory hormone AKH. PLoS Genet. 2010, 6:e1000967.
34. Riabinina O., Luginbuhl D., Marr E., Liu S., Wu M.N., Luo L., Potter C.J. Improved and expanded Q-system reagents for genetic manipulations. Nat. Methods 2015, Published online January 12, 2015. 10.1038/nmeth.3250.
35. Salvaterra P.M., Kitamoto T. Drosophila cholinergic neurons and processes visualized with Gal4/UAS-GFP. Brain Res. Gene Expr. Patterns 2001, 1:73-82.
36. Sánchez-Soriano N., Prokop A. The influence of pioneer neurons on a growing motor nerve in Drosophila requires the neural cell adhesion molecule homolog FasciclinII. J.Neurosci. 2005, 25:78-87.
37. Seruggia D., Montoliu L. The new CRISPR-Cas system: RNA-guided genome engineering to efficiently produce any desired genetic alteration in animals. Transgenic Res. 2014, 23:707-716.
38. Shah S., Hyde D.R. Two Drosophila genes that encode the alph and beta subunits of the brain soluble guanylyl cyclase. J.Biol. Chem. 1995, 270:15368-15376.
39. Sharma Y., Cheung U., Larsen E.W., Eberl D.F. PPTGAL, aconvenient Gal4 P-element vector for testing expression of enhancer fragments in Drosophila. Genesis 2002, 34:115-118.
40. Siekhaus D.E., Fuller R.S. A role for amontillado, the Drosophila homolog of the neuropeptide precursor processing protease PC2, in triggering hatching behavior. J.Neurosci. 1999, 19:6942-6954.
41. Skora A.D., Spradling A.C. Epigenetic stability increases extensively during Drosophila follicle stem cell differentiation. Proc. Natl. Acad. Sci. USA 2010, 107:7389-7394.
42. Tang W., Ehrlich I., Wolff S.B.E., Michalski A.M., Wölfl S., Hasan M.T., Lüthi A., Sprengel R. Faithful expression of multiple proteins via 2A-peptide self-processing: a versatile and reliable method for manipulating brain circuits. J.Neurosci. 2009, 29:8621-8629.
43. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
44. Vactor D.V., Sink H., Fambrough D., Tsoo R., Goodman C.S. Genes that control neuromuscular specificity in Drosophila. Cell 1993, 73:1137-1153.
45. Venken K.J., Schulze K.L., Haelterman N.A., Pan H., He Y., Evans-Holm M., Carlson J.W., Levis R.W., Spradling A.C., Hoskins R.A., Bellen H.J. MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nat. Methods 2011, 8:737-743.
46. Venken K.J., Simpson J.H., Bellen H.J. Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 2011, 72:202-230.
47. Wegener C., Herbert H., Kahnt J., Bender M., Rhea J.M. Deficiency of prohormone convertase dPC2 (AMONTILLADO) results in impaired production of bioactive neuropeptide hormones in Drosophila. J.Neurochem. 2011, 118:581-595.
48. Yasuyama K., Kitamoto T., Salvaterra P.M. Immunocytochemical study of choline acetyltransferase in Drosophila melanogaster: an analysis of cis-regulatory regions controlling expression in the brain of cDNA-transformed flies. J.Comp. Neurol. 1995, 361:25-37.
49. Yizhar O., Fenno L.E., Davidson T.J., Mogri M., Deisseroth K. Optogenetics in neural systems. Neuron 2011, 71:9-34.
50. Yuan Q., Song Y., Yang C.H., Jan L.Y., Jan Y.N. Female contact modulates male aggression via a sexually dimorphic GABAergic circuit in Drosophila. Nat. Neurosci. 2014, 17:81-88.