Expanding the power of recombinase-based labeling to uncover cellular diversity

Development (Cambridge)

Volumn 142, Issue 24, 2015, Pages 4385-4393

  Plummer, Nicholas W ^a   Evsyukova, Irina Y ^a   Robertson, Sabrina D ^a,b   de Marchena, Jacqueline ^a   Tucker, Charles J ^a   Jensen, Patricia ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Cre; Dre; Flp; Intersectional labeling; Norepinephrine

Indexed keywords

CRE RECOMBINASE; DRE RECOMBINASE; ENHANCED GREEN FLUORESCENT PROTEIN; FLUORESCENT DYE; RECOMBINASE; TDTOMATO; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CELL LABELING; CELL POPULATION; CELL STRUCTURE; CELL SUBPOPULATION; CELLS BY BODY ANATOMY; CONTROLLED STUDY; FLUORESCENCE IMAGING; GENE EXPRESSION; GENE MAPPING; HIPPOCAMPUS; MOUSE; NERVE FIBER; NERVE PROJECTION; NONHUMAN; NORADRENERGIC NERVE CELL; NORADRENERGIC SYSTEM; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; AXON; CHICKEN; CYTOLOGY; FEMALE; MALE; METABOLISM; NERVE CELL; STAINING;

ALLELES; ANIMALS; AXONS; CHICKENS; FEMALE; FLUORESCENT DYES; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; MALE; MICE; NEURONS; RECOMBINASES; STAINING AND LABELING;

EID: 84950996832     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.129981     Document Type: Article

References (57)

1. Anastassiadis, K., Fu, J., Patsch, C., Hu, S., Weidlich, S., Duerschke, K., Buchholz, F., Edenhofer, F. and Stewart, A. F. (2009). Dre recombinase, like Cre, is a highly efficient site-specific recombinase in E. coli, mammalian cells and mice. Dis. Model. Mech. 2, 508-515.
2. Andrews, B. J., Proteau, G. A., Beatty, L. G. and Sadowski, P. D. (1985). The FLP recombinase of the 2μ circle DNA of yeast: interaction with its target sequences. Cell 40, 795-803.
3. Awatramani, R., Soriano, P., Rodriguez, C., Mai, J. J. and Dymecki, S. M. (2003). Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat. Genet. 35, 70-75.
4. Bang, S. J., Jensen, P., Dymecki, S. M. and Commons, K. G. (2012). Projections and interconnections of genetically defined serotonin neurons in mice. Eur. J. Neurosci. 35, 85-96.
5. Chandler, D. J. and Waterhouse, B. D. (2012). Evidence for broad versus segregated projections from cholinergic and noradrenergic nuclei to functionally and anatomically discrete subregions of prefrontal cortex. Front. Behav. Neurosci. 6, 20.
6. Chandler, D. J., Lamperski, C. S. and Waterhouse, B. D. (2013). Identification and distribution of projections from monoaminergic and cholinergic nuclei to functionally differentiated subregions of prefrontal cortex. Brain Res. 1522, 38-58.
7. Chandler, D. J., Gao, W.-J. and Waterhouse, B. D. (2014). Heterogeneous organization of the locus coeruleus projections to prefrontal and motor cortices. Proc. Natl. Acad. Sci. USA 111, 6816-6821.
8. Chung, K., Wallace, J., Kim, S.-Y., Kalyanasundaram, S., Andalman, A. S., Davidson, T. J., Mirzabekov, J. J., Zalocusky, K. A., Mattis, J., Denisin, A. K. et al. (2013). Structural and molecular interrogation of intact biological systems. Nature 497, 332-337.
9. Cocas, L. A., Miyoshi, G., Carney, R. S. E., Sousa, V. H., Hirata, T., Jones, K. R., Fishell, G., Huntsman, R. R. and Corbin, J. G. (2009). Emx1-lineage progenitors differentially contribute to neural diversity in the striatum and amygdala. J. Neurosci. 29, 15933-15946.
10. Duan, B., Cheng, L., Bourane, S., Britz, O., Padilla, C., Garcia-Campmany, L., Krashes, M., Knowlton,W., Velasquez, T., Ren, X. et al. (2014). Identification of spinal circuits transmitting and gating mechanical pain. Cell 159, 1417-1432.
11. Dymecki, S. M. and Tomasiewicz, H. (1998). Using Flp-recombinase to characterize expansion of Wnt1-expressing neural progenitors in the mouse. Dev. Biol. 201, 57-65.
12. Ertürk, A., Becker, K., Jährling, N., Mauch, C. P., Hojer, C. D., Egen, J. G., Hellal, F., Bradke, F., Sheng, M. and Dodt, H.-U. (2012). Three-dimensional imaging of solvent-cleared organs using 3DISCO. Nat. Protoc. 7, 1983-1995.
13. Farago, A. F., Awatramani, R. B. and Dymecki, S. M. (2006). Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron 50, 205-218.
14. Fenno, L. E., Mattis, J., Ramakrishnan, C., Hyun, M., Lee, S. Y., He, M., Tucciarone, J., Selimbeyoglu, A., Berndt, A., Grosenick, L. et al. (2014). Targeting cells with single vectors using multiple-feature Boolean logic. Nat. Methods 11, 763-772.
15. Friedrich, G. and Soriano, P. (1991). Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5, 1513-1523.
16. George, S. H. L., Gertsenstein, M., Vintersten, K., Korets-Smith, E., Murphy, J., Stevens, M. E., Haigh, J. J. and Nagy, A. (2007). Developmental and adult phenotyping directly from mutant embryonic stem cells. Proc. Natl. Acad. Sci. USA 104, 4455-4460.
17. Gong, S., Doughty, M., Harbaugh, C. R., Cummins, A., Hatten, M. E., Heintz, N. and Gerfen, C. R. (2007). Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J. Neurosci. 27, 9817-9823.
18. Hama, H., Kurokawa, H., Kawano, H., Ando, R., Shimogori, T., Noda, H., Fukami, K., Sakaue-Sawano, A. and Miyawaki, A. (2011). Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat. Neurosci. 14, 1481-1488.
19. Hermann, M., Stillhard, P., Wildner, H., Seruggia, D., Kapp, V., Sanchez-Iranzo, H., Mercader, N., Montoliu, L., Zeilhofer, H. U. and Pelczar, P. (2014). Binary recombinase systems for high-resolution conditional mutagenesis. Nucleic Acids Res. 42, 3894-3907.
20. Holets, V. R., Hökfelt, T., Rökaeus, A., Terenius, L. and Goldstein, M. (1988). Locus coeruleus neurons in the rat containing neuropeptide Y, tyrosine hydroxylase or galanin and their efferent projections to the spinal cord, cerebral cortex and hypothalamus. Neuroscience 24, 893-906.
21. Huang, Z. J. (2014). Toward a genetic dissection of cortical circuits in the mouse. Neuron 83, 1284-1302.
22. Jensen, P. and Dymecki, S. M. (2014). Essentials of recombinase-based genetic fate mapping in mice. Methods Mol. Biol. 1092, 437-454.
23. Jensen, P., Farago, A. F., Awatramani, R. B., Scott, M. M., Deneris, E. S. and Dymecki, S. M. (2008). Redefining the serotonergic system by genetic lineage. Nat. Neurosci. 11, 417-419.
24. Kato, S., Kuramochi, M., Takasumi, K., Kobayashi, K., Inoue, K.-i., Takahara, D., Hitoshi, S., Ikenaka, K., Shimada, T., Takada, M. et al. (2011). Neuron-specific gene transfer through retrograde transport of lentiviral vector pseudotyped with a novel type of fusion envelope glycoprotein. Hum. Gene Ther. 22, 1511-1523.
25. Ke, M.-T., Fujimoto, S. and Imai, T. (2013). SeeDB: a simple and morphologypreserving optical clearing agent for neuronal circuit reconstruction. Nat. Neurosci. 16, 1154-1161.
26. Kim, J. C., Cook, M. N., Carey, M. R., Shen, C., Regehr,W. G. and Dymecki, S. M. (2009). Linking genetically defined neurons to behavior through a broadly applicable silencing allele. Neuron 63, 305-315.
27. Kimmel, R. A., Turnbull, D. H., Blanquet, V., Wurst, W., Loomis, C. A. and Joyner, A. L. (2000). Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev. 14, 1377-1389.
28. Lewandoski, M., Meyers, E. N. and Martin, G. R. (1997). Analysis of Fgf8 gene function in vertebrate development. Cold Spring Harb. Symp. Quant. Biol. 62, 159-168.
29. Lundgren, O., Jodal, M., Jansson, M., Ryberg, A. T. and Svensson, L. (2011). Intestinal epithelial stem/progenitor cells are controlled by mucosal afferent nerves. PLoS ONE 6, e16295.
30. Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R. et al. (2010). A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140.
31. Madisen, L., Garner, A. R., Shimaoka, D., Chuong, A. S., Klapoetke, N. C., Li, L., van der Bourg, A., Niino, Y., Egolf, L., Monetti, C. et al. (2015). Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance. Neuron 85, 942-958.
32. Matthies, H. J. G., Han, Q., Shields, A., Wright, J., Moore, J. L., Winder, D. G., Galli, A. and Blakely, R. D. (2009). Subcellular localization of the antidepressantsensitive norepinephrine transporter. BMC Neurosci. 10, 65.
33. McCall, J. G., Al-Hasani, R., Siuda, E. R., Hong, D. Y., Norris, A. J., Ford, C. P. and Bruchas, M. R. (2015). CRH engagement of the locus coeruleus noradrenergic system mediates stress-induced anxiety. Neuron 87, 605-620.
34. Miller, M. A., Kolbe, P. E., Leverenz, J. B., Peskind, E. R. and Raskind, M. A. (1999). Preservation of noradrenergic neurons in the locus coeruleus that coexpress galaning mRNA in Alzheimer's disease. J. Neurochem. 73, 2028-2036.
35. Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J. B., Battiste, J., Johnson, J. E., Machold, R. P. and Fishell, G. (2010). Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30, 1582-1594.
36. Niwa, H., Yamamura, K. and Miyazaki, J. (1991). Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
37. O'Gorman, S. (2005). Second branchial arch lineages of the middle ear of wild-type and Hoxa2 mutant mice. Dev. Dyn. 234, 124-131.
38. Olpe, H.-R. and Steinmann, M. (1991). Responses of locus coeruleus neurons to neuropeptides. Prog. Brain Res. 88, 241-248.
39. Paxinos, G. and Franklin, K. B. J. (2013). The Mouse Brain in Stereotaxic Coordinates. San Diego: Academic Press.
40. Poulin, J.-F., Zou, J., Drouin-Ouellet, J., Kim, K.-Y., Cicchetti, F. and Awatramani, R. B. (2014). Defining midbrain dopaminergic neuron diversity by single-cell gene expression profiling. Cell Rep. 9, 930-943.
41. Raymond, C. S. and Soriano, P. (2007). High-efficiency FLP and ϕC31 site-specific recombination in mammalian cells. PLoS ONE 2, e162.
42. Renier, N., Wu, Z., Simon, D. J., Yang, J., Ariel, P. and Tessier-Lavigne, M. (2014). iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159, 896-910.
43. Robertson, S. D., Plummer, N. W., de Marchena, J. and Jensen, P. (2013). Developmental origins of central norepinephrine neuron diversity. Nat. Neurosci. 16, 1016-1023.
44. Rodriguez, C. I., Buchholz, F., Galloway, J., Sequerra, R., Kasper, J., Ayala, R., Stewart, A. F. and Dymecki, S. M. (2000). High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25, 139-140.
45. Sakamoto, M., Ieki, N., Miyoshi, G., Mochimaru, D., Miyachi, H., Imura, T., Yamaguchi, M., Fishell, G., Mori, K., Kageyama, R. et al. (2014). Continuous postnatal neurogenesis contributes to formation of the olfactory bulb neural circuits and flexible olfactory associative learning. J. Neurosci. 34, 5788-5799.
46. Sauer, B. (1993). Manipulation of transgenes by site-specific recombination: use of Cre recombinase. Methods Enzymol. 225, 890-900.
47. Sauer, B. and McDermott, J. (2004). DNA recombination with a heterospecific Cre homolog identified from comparison of the pac-c1 regions of P1-related phages. Nucleic Acids Res. 32, 6086-6095.
48. Schwarz, L. A., Miyamachi, K., Gao, X. J., Beier, K. T., Weissbourd, B., DeLoach, K. E., Ren, J., Ibanes, S., Malenka, R. C., Kremer, E. J. et al. (2015). Viral-genetic tracing of the input-output organization of a central noradrenaline circuit. Nature 524, 88-92.
49. Sciolino, N. R., Smith, J. M., Stranahan, A. M., Freeman, K. G., Edwards, G. L., Weinshenker, D. and Holmes, P. V. (2015). Galanin mediates features of neural and behavioral stress resilience afforded by exercise. Neuropharmacology 89, 255-264.
50. Sevcik, J., Finta, E. P. and Illes, P. (1993). Galanin receptors inhibit the spontaneous firing of locus coeruleus neurones and interact with μ-opioid receptors. Eur. J. Pharmacol. 230, 223-230.
51. Soudais, C., Laplace-Builhe, C., Kissa, K. and Kremer, E. J. (2001). Preferential transduction of neurons by canine adenovirus vectors and their efficient retrograde transport in vivo. FASEB J. 15, 2283-2285.
52. Sternberg, N. and Hamilton, D. (1981). Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites. J. Mol. Biol. 150, 467-486.
53. Xu, Z.-Q., Shi, T.-J. S. and Hökfelt, T. (1998). Galanin/GMAP- and NPY-like immunoreactivities in locus coeruleus and noradrenergic nerve terminals in the hippocampal formation and cortex with notes on the galanin-R1 and -R2 receptors. J. Comp. Neurol. 392, 227-251.
54. Yamamoto, M., Shook, N. A., Kanisicak, O., Yamamoto, S., Wosczyna, M. N., Camp, J. R. and Goldhamer, D. J. (2009). A multifunctional reporter mouse line for Cre- and FLP-dependent lineage analysis. Genesis 47, 107-114.
55. Yang, B., Treweek, J. B., Kulkarni, R. P., Deverman, B. E., Chen, C.-K., Lubeck, E., Shah, S., Cai, L. and Gradinaru, V. (2014). Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 158, 945-958.
56. Zinyk, D. L., Mercer, E. H., Harris, E. Anderson, D. J. and Joyner, A. L. (1998). Fate mapping of the mouse midbrain-hindbrain constriction using a site-specific recombination system. Curr. Biol. 8, 665-672.
57. Zufferey, R., Donello, J. E., Trono, T. J. and Hope, T. J. (1999). Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J. Virol. 73, 2886-2892.