Versatile genetic paintbrushes: Brainbow technologies

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 4, Issue 2, 2015, Pages 161-180

  Richier, Benjamin ^a   Salecker, Iris ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; GREEN FLUORESCENT PROTEIN; INTEGRASE; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR; RECOMBINASE; RED FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR GAL4; YELLOW FLUORESCENT PROTEIN; PHOTOPROTEIN;

ANTIBODY LABELING; ARTICLE; BRAINBOW TECHNOLOGY; CELL CLONING; CELL LABELING; CHICKEN; CONFOCAL LASER MICROSCOPY; DNA METHYLATION; DNA RECOMBINATION; DROSOPHILA MELANOGASTER; ELECTROPORATION; EPITOPE MAPPING; GENE DELETION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; TRANSGENE; ZEBRA FISH; ANIMAL; GENETIC PROCEDURES; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; STAINING;

ANIMALIA; DANIO RERIO; DROSOPHILA MELANOGASTER; MUS;

ANIMALS; BASE SEQUENCE; GENETIC TECHNIQUES; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; STAINING AND LABELING; TRANSGENES;

EID: 84923264669     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.166     Document Type: Article

References (103)

1. Lee T. Generating mosaics for lineage analysis in flies. WIREs Dev Biol 2014, 3:69-81.
2. Livet J, Weissman TA, Kang H, Draft RW, Lu J, Bennis RA, Sanes JR, Lichtman JW. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 2007, 450:56-62.
3. Hampel S, Chung P, McKellar CE, Hall D, Looger LL, Simpson JH. Drosophila Brainbow: a recombinase-based fluorescence labeling technique to subdivide neural expression patterns. Nat Methods 2011, 8:253-259.
4. Hadjieconomou D, Rotkopf S, Alexandre C, Bell DM, Dickson BJ, Salecker I. Flybow: genetic multicolor cell labeling for neural circuit analysis in Drosophila melanogaster. Nat Methods 2011, 8:260-266.
5. Shimosako N, Hadjieconomou D, Salecker I. Flybow to dissect circuit assembly in the Drosophila brain. Methods Mol Biol 2014, 1082:57-69.
6. Forster D, Luschnig S. Src42A-dependent polarized cell shape changes mediate epithelial tube elongation in Drosophila. Nat Cell Biol 2012, 14:526-534.
7. Boulina M, Samarajeewa H, Baker JD, Kim MD, Chiba A. Live imaging of multicolor-labeled cells in Drosophila. Development 2013, 140:1605-1613.
8. Chin AL, Lin CY, Fu TF, Dickson BJ, Chiang AS. Diversity and wiring variability of visual local neurons in the Drosophila medulla M6 stratum. J Comp Neurol 2014, 522:3795-3816.
9. Worley MI, Setiawan L, Hariharan IK. TIE-DYE: a combinatorial marking system to visualize and genetically manipulate clones during development in Drosophila melanogaster. Development 2013, 140:3275-3284.
10. Kanca O, Caussinus E, Denes AS, Percival-Smith A, Affolter M. Raeppli: a whole-tissue labeling tool for live imaging of Drosophila development. Development 2014, 141:472-480.
11. Pan YA, Livet J, Sanes JR, Lichtman JW, Schier AF. Multicolor Brainbow imaging in zebrafish. Cold Spring Harb Protoc 2011, 2011:pdb prot5546.
12. Gupta V, Poss KD. Clonally dominant cardiomyocytes direct heart morphogenesis. Nature 2012, 484:479-484.
13. Robles E, Filosa A, Baier H. Precise lamination of retinal axons generates multiple parallel input pathways in the tectum. J Neurosci 2013, 33:5027-5039.
14. Pan YA, Freundlich T, Weissman TA, Schoppik D, Wang XC, Zimmerman S, Ciruna B, Sanes JR, Lichtman JW, Schier AF. Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish. Development 2013, 140:2835-2846.
15. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, Barker N, Klein AM, van Rheenen J, Simons BD, et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010, 143:134-144.
16. Cai D, Cohen KB, Luo T, Lichtman JW, Sanes JR. Improved tools for the Brainbow toolbox. Nat Methods 2013, 10:540-547.
17. Loulier K, Barry R, Mahou P, Le Franc Y, Supatto W, Matho KS, Ieng S, Fouquet S, Dupin E, Benosman R, et al. Multiplex cell and lineage tracking with combinatorial labels. Neuron 2014, 81:505-520.
18. Garcia-Moreno F, Vasistha NA, Begbie J, Molnar Z. CLoNe is a new method to target single progenitors and study their progeny in mouse and chick. Development 2014, 141:1589-1598.
19. Shimomura O, Johnson FH, Saiga Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 1962, 59:223-239.
20. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. Green fluorescent protein as a marker for gene expression. Science 1994, 263:802-805.
21. Shagin DA, Barsova EV, Yanushevich YG, Fradkov AF, Lukyanov KA, Labas YA, Semenova TN, Ugalde JA, Meyers A, Nunez JM, et al. GFP-like proteins as ubiquitous metazoan superfamily: evolution of functional features and structural complexity. Mol Biol Evol 2004, 21:841-850.
22. Ai HW, Henderson JN, Remington SJ, Campbell RE. Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging. Biochem J 2006, 400:531-540.
23. Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, Markelov ML, Lukyanov SA. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol 1999, 17:969-973.
24. Karasawa S, Araki T, Nagai T, Mizuno H, Miyawaki A. Cyan-emitting and orange-emitting fluorescent proteins as a donor/acceptor pair for fluorescence resonance energy transfer. Biochem J 2004, 381:307-312.
25. Sakaue-Sawano A, Kurokawa H, Morimura T, Hanyu A, Hama H, Osawa H, Kashiwagi S, Fukami K, Miyata T, Miyoshi H, et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 2008, 132:487-498.
26. Shcherbo D, Murphy CS, Ermakova GV, Solovieva EA, Chepurnykh TV, Shcheglov AS, Verkhusha VV, Pletnev VZ, Hazelwood KL, Roche PM, et al. Far-red fluorescent tags for protein imaging in living tissues. Biochem J 2009, 418:567-574.
27. Ai HW, Shaner NC, Cheng Z, Tsien RY, Campbell RE. Exploration of new chromophore structures leads to the identification of improved blue fluorescent proteins. Biochemistry (Mosc) 2007, 46:5904-5910.
28. Subach OM, Gundorov IS, Yoshimura M, Subach FV, Zhang J, Gruenwald D, Souslova EA, Chudakov DM, Verkhusha VV. Conversion of red fluorescent protein into a bright blue probe. Chem Biol 2008, 15:1116-1124.
29. Tsien RY. The green fluorescent protein. Annu Rev Biochem 1998, 67:509-544.
30. Miyawaki A, Tsien RY. Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol 2000, 327:472-500.
31. Rizzo MA, Springer GH, Granada B, Piston DW. An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 2004, 22:445-449.
32. Goedhart J, van Weeren L, Hink MA, Vischer NO, Jalink K, Gadella TW Jr. Bright cyan fluorescent protein variants identified by fluorescence lifetime screening. Nat Methods 2010, 7:137-139.
33. Goedhart J, von Stetten D, Noirclerc-Savoye M, Lelimousin M, Joosen L, Hink MA, van Weeren L, Gadella TW Jr, Royant A. Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat Commun 2012, 3:751.
34. Zapata-Hommer O, Griesbeck O. Efficiently folding and circularly permuted variants of the Sapphire mutant of GFP. BMC Biotechnol 2003, 3:5.
35. Ai HW, Hazelwood KL, Davidson MW, Campbell RE. Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors. Nat Methods 2008, 5:401-403.
36. Zacharias DA, Violin JD, Newton AC, Tsien RY. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002, 296:913-916.
37. Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J Biol Chem 2001, 276:29188-29194.
38. Strack RL, Bhattacharyya D, Glick BS, Keenan RJ. Noncytotoxic orange and red/green derivatives of DsRed-Express2 for whole-cell labeling. BMC Biotechnol 2009, 9:32.
39. Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, Tsien RY. Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods 2008, 5:545-551.
40. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY. A monomeric red fluorescent protein. Proc Natl Acad Sci USA 2002, 99:7877-7882.
41. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 2004, 22:1567-1572.
42. Zamoyska R, Vollmer AC, Sizer KC, Liaw CW, Parnes JR. Two Lyt-2 polypeptides arise from a single gene by alternative splicing patterns of mRNA. Cell 1985, 43:153-163.
43. Liaw CW, Zamoyska R, Parnes JR. Structure, sequence, and polymorphism of the Lyt-2T cell differentiation antigen gene. J Immunol 1986, 137:1037-1043.
44. Hancock JF, Cadwallader K, Paterson H, Marshall CJ. A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO J 1991, 10:4033-4039.
45. Jiang W, Hunter T. Analysis of cell-cycle profiles in transfected cells using a membrane-targeted GFP. Biotechniques 1998, 24:349-350 352, 354.
46. Kay JN, Roeser T, Mumm JS, Godinho L, Mrejeru A, Wong RO, Baier H. Transient requirement for ganglion cells during assembly of retinal synaptic layers. Development 2004, 131:1331-1342.
47. Kalderon D, Roberts BL, Richardson WD, Smith AE. A short amino acid sequence able to specify nuclear location. Cell 1984, 39:499-509.
48. Emery G, Hutterer A, Berdnik D, Mayer B, Wirtz-Peitz F, Gaitan MG, Knoblich JA. Asymmetric Rab 11 endosomes regulate delta recycling and specify cell fate in the Drosophila nervous system. Cell 2005, 122:763-773.
49. Rizzuto R, Brini M, Pizzo P, Murgia M, Pozzan T. Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. Curr Biol 1995, 5:635-642.
50. Shaner NC, Steinbach PA, Tsien RY. A guide to choosing fluorescent proteins. Nat Methods 2005, 2:905-909.
51. Mahou P, Zimmerley M, Loulier K, Matho KS, Labroille G, Morin X, Supatto W, Livet J, Debarre D, Beaurepaire E. Multicolor two-photon tissue imaging by wavelength mixing. Nat Methods 2012, 9:815-818.
52. Hama H, Kurokawa H, Kawano H, Ando R, Shimogori T, Noda H, Fukami K, Sakaue-Sawano A, Miyawaki A. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat Neurosci 2011, 14:1481-1488.
53. Chung K, Deisseroth K. CLARITY for mapping the nervous system. Nat Methods 2013, 10:508-513.
54. Badaloni A, Bonanomi D, Albieri I, Givogri I, Bongarzone E, Valtorta F, Consalez GG. Transgenic mice expressing a dual, CRE-inducible reporter for the analysis of axon guidance and synaptogenesis. Genesis 2007, 45:405-412.
55. Feinberg EH, Vanhoven MK, Bendesky A, Wang G, Fetter RD, Shen K, Bargmann CI. GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 2008, 57:353-363.
56. Gordon MD, Scott K. Motor control in a Drosophila taste circuit. Neuron 2009, 61:373-384.
57. Han C, Jan LY, Jan YN. Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc Natl Acad Sci USA 2011, 108:9673-9678.
58. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
59. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A, Takeuchi H, Aigaki T, Matsuzaki F, Nakagoshi H, Tanimura T, et al. GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 2002, 34:58-61.
60. Pfeiffer BD, Jenett A, Hammonds AS, Ngo TT, Misra S, Murphy C, Scully A, Carlson JW, Wan KH, Laverty TR, et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci USA 2008, 105:9715-9720.
61. Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C, Dionne H, Pfeiffer BD, Cavallaro A, Hall D, Jeter J, et al. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2012, 2:991-1001.
62. Kvon EZ, Kazmar T, Stampfel G, Yanez-Cuna JO, Pagani M, Schernhuber K, Dickson BJ, Stark A. Genome-scale functional characterization of Drosophila developmental enhancers in vivo. Nature 2014, 512:91-95.
63. Lee T, Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
64. McGuire SE, Mao Z, Davis RL. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE 2004, 220:pl6.
65. Lai SL, Lee T. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 2006, 9:703-709.
66. Pfeiffer BD, Ngo TT, Hibbard KL, Murphy C, Jenett A, Truman JW, Rubin GM. Refinement of tools for targeted gene expression in Drosophila. Genetics 2010, 186:735-755.
67. Potter CJ, Tasic B, Russler EV, Liang L, Luo L. The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 2010, 141:536-548.
68. Golic KG, Lindquist S. The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 1989, 59:499-509.
69. Branda CS, Dymecki SM. Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev Cell 2004, 6:7-28.
70. Griffin R, Binari R, Perrimon N. Genetic odyssey to generate marked clones in Drosophila mosaics. Proc Natl Acad Sci USA 2014, 111:4756-4763.
71. Gaj T, Sirk SJ, Barbas CF 3rd. Expanding the scope of site-specific recombinases for genetic and metabolic engineering. Biotechnol Bioeng 2014, 111:1-15.
72. Lee G, Saito I. Role of nucleotide sequences of loxP spacer region in Cre-mediated recombination. Gene 1998, 216:55-65.
73. McLeod M, Craft S, Broach JR. Identification of the crossover site during FLP-mediated recombination in the Saccharomyces cerevisiae plasmid 2 microns circle. Mol Cell Biol 1986, 6:3357-3367.
74. Senecoff JF, Cox MM. Directionality in FLP protein-promoted site-specific recombination is mediated by DNA-DNA pairing. J Biol Chem 1986, 261:7380-7386.
75. Schlake T, Bode J. Use of mutated FLP recognition target (FRT) sites for the exchange of expression cassettes at defined chromosomal loci. Biochemistry (Mosc) 1994, 33:12746-12751.
76. Larsen C, Franch-Marro X, Hartenstein V, Alexandre C, Vincent JP. An efficient promoter trap for detection of patterned gene expression and subsequent functional analysis in Drosophila. Proc Natl Acad Sci USA 2006, 103:17813-17817.
77. Voziyanov Y, Konieczka JH, Stewart AF, Jayaram M. Stepwise manipulation of DNA specificity in Flp recombinase: progressively adapting Flp to individual and combinatorial mutations in its target site. J Mol Biol 2003, 326:65-76.
78. Thorpe HM, Wilson SE, Smith MC. Control of directionality in the site-specific recombination system of the Streptomyces phage phiC31. Mol Microbiol 2000, 38:232-241.
79. Groth AC, Olivares EC, Thyagarajan B, Calos MP. A phage integrase directs efficient site-specific integration in human cells. Proc Natl Acad Sci USA 2000, 97:5995-6000.
80. Siegal ML, Hartl DL. Transgene Coplacement and high efficiency site-specific recombination with the Cre/loxP system in Drosophila. Genetics 1996, 144:715-726.
81. Golic KG. Site-specific recombination between homologous chromosomes in Drosophila. Science 1991, 252:958-961.
82. Struhl G, Basler K. Organizing activity of wingless protein in Drosophila. Cell 1993, 72:527-540.
83. Duffy JB, Harrison DA, Perrimon N. Identifying loci required for follicular patterning using directed mosaics. Development 1998, 125:2263-2271.
84. Le X, Langenau DM, Keefe MD, Kutok JL, Neuberg DS, Zon LI. Heat shock-inducible Cre/Lox approaches to induce diverse types of tumors and hyperplasia in transgenic zebrafish. Proc Natl Acad Sci USA 2007, 104:9410-9415.
85. Nern A, Pfeiffer BD, Svoboda K, Rubin GM. Multiple new site-specific recombinases for use in manipulating animal genomes. Proc Natl Acad Sci USA 2011, 108:14198-14203.
86. Venken KJ, Bellen HJ. Emerging technologies for gene manipulation in Drosophila melanogaster. Nat Rev Genet 2005, 6:167-178.
87. Anastassiadis K, Glaser S, Kranz A, Berhardt K, Stewart AF. A practical summary of site-specific recombination, conditional mutagenesis, and tamoxifen induction of CreERT2. Methods Enzymol 2010, 477:109-123.
88. Huang J, Zhou W, Dong W, Watson AM, Hong Y. Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering. Proc Natl Acad Sci USA 2009, 106:8284-8289.
89. Heidmann D, Lehner CF. Reduction of Cre recombinase toxicity in proliferating Drosophila cells by estrogen-dependent activity regulation. Dev Genes Evol 2001, 211:458-465.
90. Venken KJ, He Y, Hoskins RA, Bellen HJ. P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 2006, 314:1747-1751.
91. Bischof J, Maeda RK, 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.
92. Venken KJ, Schulze KL, Haelterman NA, Pan H, He Y, Evans-Holm M, Carlson JW, Levis RW, Spradling AC, Hoskins RA, et al. MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nat Methods 2011, 8:737-743.
93. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
94. St Johnston D. Using mutants, knockdowns, and transgenesis to investigate gene function in Drosophila. WIREs Dev Biol 2013, 2:587-613.
95. Akitake CM, Macurak M, Halpern ME, Goll MG. Transgenerational analysis of transcriptional silencing in zebrafish. Dev Biol 2011, 352:191-201.
96. Card JP, Kobiler O, McCambridge J, Ebdlahad S, Shan Z, Raizada MK, Sved AF, Enquist LW. Microdissection of neural networks by conditional reporter expression from a Brainbow herpesvirus. Proc Natl Acad Sci USA 2011, 108:3377-3382.
97. Chen F, LoTurco J. A method for stable transgenesis of radial glia lineage in rat neocortex by piggyBac mediated transposition. J Neurosci Methods 2012, 207:172-180.
98. Garcia-Marques J, Lopez-Mascaraque L. Clonal identity determines astrocyte cortical heterogeneity. Cereb Cortex 2013, 23:1463-1472.
99. Timofeev K, Joly W, Hadjieconomou D, Salecker I. Localized netrins act as positional cues to control layer-specific targeting of photoreceptor axons in Drosophila. Neuron 2012, 75:80-93.
100. Oliva C, Choi CM, Nicolai LJ, Mora N, De Geest N, Hassan BA. Proper connectivity of Drosophila motion detector neurons requires Atonal function in progenitor cells. Neural Dev 2014, 9:4.
101. von Hilchen CM, Bustos AE, Giangrande A, Technau GM, Altenhein B. Predetermined embryonic glial cells form the distinct glial sheaths of the Drosophila peripheral nervous system. Development 2013, 140:3657-3668.
102. Di Girolamo N, Bobba S, Raviraj V, Delic NC, Slapetova I, Nicovich PR, Halliday GM, Wakefield D, Whan R, Lyons GJ. Tracing the fate of limbal epithelial progenitor cells in the murine cornea. Stem Cells 2014. doi:10.1002/stem.1769.
103. Szymczak-Workman AL, Vignali KM, Vignali DA. Design and construction of 2A peptide-linked multicistronic vectors. Cold Spring Harb Protoc 2012, 2012:199-204.