Transcriptomic and anatomic parcellation of 5-HT3A R expressing cortical interneuron subtypes revealed by single-cell RNA sequencing

Nature Communications

Volumn 8, Issue , 2017, Pages

  Frazer, Sarah ^a   Prados, Julien ^a   Niquille, Mathieu ^a   Cadilhac, Christelle ^a   Markopoulos, Foivos ^a   Gomez, Lucia ^a   Tomasello, Ugo ^a   Telley, Ludovic ^a   Holtmaat, Anthony ^a   Jabaudon, Denis ^a   Dayer, Alexandre ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 2; DLX6 PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; GAD1 PROTEIN; GAD2 PROTEIN; SEROTONIN 3A RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX1; TRANSCRIPTION FACTOR DLX2; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR ER81; TRANSCRIPTION FACTOR MAF; TRANSCRIPTION FACTOR MEIS2; TRANSCRIPTION FACTOR NPAS3; TRANSCRIPTION FACTOR NR2F2; TRANSCRIPTION FACTOR PROX1; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; BIOLOGICAL MARKER; GREEN FLUORESCENT PROTEIN; HOMEODOMAIN PROTEIN; HTR3A PROTEIN, MOUSE; MRG1 PROTEIN, MOUSE; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; NR2F2 PROTEIN, MOUSE; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE; SEROTONIN 3 RECEPTOR;

ANATOMY; CELLS AND CELL COMPONENTS; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC MARKER;

ANATOMICAL CONCEPTS; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; INTERNEURON; MALE; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MOUSE; NERVE CELL NETWORK; NONHUMAN; PROTEIN ANALYSIS; RNA SEQUENCE; SINGLE CELL ANALYSIS; TRANSCRIPTOMICS; WHITE MATTER; ANATOMY AND HISTOLOGY; ANIMAL; C57BL MOUSE; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAMMALIAN EMBRYO; METABOLISM; MICROFLUIDICS; PHYSIOLOGY; PROCEDURES; SEQUENCE ANALYSIS; TRANSGENIC MOUSE;

ANIMALS; BIOMARKERS; CELL ADHESION MOLECULES, NEURONAL; CEREBRAL CORTEX; COUP TRANSCRIPTION FACTOR II; EMBRYO, MAMMALIAN; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GABAERGIC NEURONS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROFLUIDICS; NERVE NET; NERVE TISSUE PROTEINS; RECEPTORS, SEROTONIN, 5-HT3; SEQUENCE ANALYSIS, RNA; SERINE ENDOPEPTIDASES; SINGLE-CELL ANALYSIS;

EID: 85011278195     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14219     Document Type: Article

References (59)

1. Huang, Z. J. Toward a genetic dissection of cortical circuits in the mouse. Neuron 83, 1284-1302 (2014).
2. Kepecs, A. & Fishell, G. Interneuron cell types are fit to function. Nature 505, 318-326 (2014).
3. Fishell, G. & Rudy, B. Mechanisms of inhibition within the telencephalon: 'Where the Wild Things Are'. Annu. Rev. Neurosci. 34, 535-567 (2011).
4. Defelipe, J. et al. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14, 202-216 (2013).
5. Kessaris, N., Magno, L., Rubin, A. N. & Oliveira, M. G. Genetic programs controlling cortical interneuron fate. Curr. Opin. Neurobiol. 26, 79-87 (2014).
6. Gelman, D. M. & Marín, O. Generation of interneuron diversity in the mouse cerebral cortex. Eur. J. Neurosci. 31, 2136-2141 (2010).
7. Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G. & Alvarez-Buylla, A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2, 461-466 (1999).
8. Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G. & Alvarez-Buylla, A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128, 3759-3771 (2001).
9. Anderson, S. A., Marín, O., Horn, C., Jennings, K. & Rubenstein, J. L. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128, 353-363 (2001).
10. Taniguchi, H., Lu, J. & Huang, Z. J. The spatial and temporal origin of chandelier cells in mouse neocortex. Science 339, 70-74 (2013).
11. Fogarty, M. et al. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27, 10935-10946 (2007).
12. Xu, Q., Tam, M. & Anderson, S. A. Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J. Comp. Neurol. 506, 16-29 (2008).
13. Butt, S. J. et al. The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59, 722-732 (2008).
14. Butt, S. J. et al. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48, 591-604 (2005).
15. Nery, S., Fishell, G. & Corbin, J. G. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat. Neurosci. 5, 1279-1287 (2002).
16. Miyoshi, G. et al. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30, 1582-1594 (2010).
17. Gelman, D. M. et al. The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J. Neurosci. 29, 9380-9389 (2009).
18. Vucurovic, K. et al. Serotonin 3A receptor subtype as an early and protracted marker of cortical interneuron subpopulations. Cereb. Cortex 20, 2333-2347 (2010).
19. Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G. & Rudy, B. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J. Neurosci. 30, 16796-16808 (2010).
20. Murthy, S. et al. Serotonin receptor 3A controls interneuron migration into the neocortex. Nat. Commun. 5, 5524 (2014).
21. Rubin, A. N. & Kessaris, N. PROX1: a lineage tracer for cortical interneurons originating in the lateral/caudal ganglionic eminence and preoptic area. PLoS ONE 8, e77339 (2013).
22. Miyoshi, G. et al. Prox1 regulates the subtype-specific development of caudal ganglionic eminence-derived GABAergic cortical interneurons. J. Neurosci. 35, 12869-12889 (2015).
23. Touzot, A., Ruiz-Reig, N., Vitalis, T. & Studer, M. Molecular control of two novel migratory paths for CGE-derived interneurons in the developing mouse brain. Development 143, 1753-1765 (2016).
24. Kanatani, S., Yozu, M., Tabata, H. & Nakajima, K. COUP-TFII is preferentially expressed in the caudal ganglionic eminence and is involved in the caudal migratory stream. J. Neurosci. 28, 13582-13591 (2008).
25. Cai, Y. et al. Nuclear receptor COUP-TFII-expressing neocortical interneurons are derived from the medial and lateral/caudal ganglionic eminence and define specific subsets of mature interneurons. J. Comp. Neurol. 521, 479-497 (2013).
26. Du, T., Xu, Q., Ocbina, P. J. & Anderson, S. A. NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development 135, 1559-1567 (2008).
27. Liodis, P. et al. Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J. Neurosci. 27, 3078-3089 (2007).
28. Batista-Brito, R. et al. The cell-intrinsic requirement of Sox6 for cortical interneuron development. Neuron 63, 466-481 (2009).
29. Azim, E., Jabaudon, D., Fame, R. M. & Macklis, J. D. SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat. Neurosci. 12, 1238-1247 (2009).
30. Lodato, S. et al. Loss of COUP-TFI alters the balance between caudal ganglionic eminence-and medial ganglionic eminence-derived cortical interneurons and results in resistance to epilepsy. J. Neurosci. 31, 4650-4662 (2011).
31. Erbel-Sieler, C. et al. Behavioral and regulatory abnormalities in mice deficient in the NPAS1 and NPAS3 transcription factors. Proc. Natl Acad. Sci. USA 101, 13648-13653 (2004).
32. Stanco, A. et al. NPAS1 represses the generation of specific subtypes of cortical interneurons. Neuron 84, 940-953 (2014).
33. McKinsey, G. L. et al. Dlx1&2-dependent expression of Zfhx1b (Sip1, Zeb2) regulates the fate switch between cortical and striatal interneurons. Neuron 77, 83-98 (2013).
34. Tasic, B. et al. Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat. Neurosci. 19, 335-346 (2016).
35. Zeisel, A. et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347, 1138-1142 (2015)
36. Von Engelhardt, J., Khrulev, S., Eliava, M., Wahlster, S. & Monyer, H. 5-HT(3A) receptor-bearing white matter interstitial GABAergic interneurons are functionally integrated into cortical and subcortical networks. J. Neurosci. 31, 16844-16854 (2011).
37. Clancy, B., Silva-Filho, M. & Friedlander, M. J. Structure and projections of white matter neurons in the postnatal rat visual cortex. J. Comp. Neurol. 434, 233-252 (2001).
38. Suárez-Solá, M. L. et al. Neurons in the white matter of the adult human neocortex. Front. Neuroanat. 3, 7 (2009).
39. Judaš, M., Sedmak, G., Pletikos, M. & Jovanov-Milošević, N. Populations of subplate and interstitial neurons in fetal and adult human telencephalon. J. Anat. 217, 381-399 (2010).
40. Kostovic, I. & Rakic, P. Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J. Neurocytol. 9, 219-242 (1980).
41. Okhotin, V. E. & Kalinichenko, S. G. Subcortical white matter interstitial cells: their connections, neurochemical specialization, and role in the histogenesis of the cortex. Neurosci. Behav. Physiol. 33, 177-194 (2003)
42. Telley, L. et al. Sequential transcriptional waves direct the differentiation of newborn neurons in the mouse neocortex. Science 351, 1443-1446 (2016)
43. Macosko, E. Z. et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161, 1202-1214 (2015).
44. Kharchenko, P. V., Silberstein, L. & Scadden, D. T. Bayesian approach to single-cell differential expression analysis. Nat. Methods 11, 740-742 (2014)
45. Agoston, Z. et al. Meis2 is a Pax6 co-factor in neurogenesis and dopaminergic periglomerular fate specification in the adult olfactory bulb. Development 141, 28-38 (2014).
46. Allen, Z. J., Waclaw, R. R., Colbert, M. C. & Campbell, K. Molecular identity of olfactory bulb interneurons: transcriptional codes of periglomerular neuron subtypes. J. Mol. Histol. 38, 517-525 (2007).
47. Stenman, J., Toresson, H. & Campbell, K. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J. Neurosci. 23, 167-174 (2003)
48. Saino-Saito, S. et al. ER81 and CaMKIV identify anatomically and phenotypically defined subsets of mouse olfactory bulb interneurons. J. Comp. Neurol. 502, 485-496 (2007).
49. Redmond, L., Hockfield, S. & Morabito, M. A. The divergent homeobox gene PBX1 is expressed in the postnatal subventricular zone and interneurons of the olfactory bulb. J. Neurosci. 16, 2972-2982 (1996).
50. Jiang, X., Zhang, M., You, Y. & Liu, F. The production of somatostatin interneurons in the olfactory bulb is regulated by the transcription factor sp8. PLoS ONE 8, e70049 (2013).
51. Li, X. et al. The transcription factor Sp8 is required for the production of parvalbumin-expressing interneurons in the olfactory bulb. J. Neurosci. 31, 8450-8455 (2011).
52. Waclaw, R. R. et al. The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 49, 503-516 (2006).
53. Ma, T. et al. A subpopulation of dorsal lateral/caudal ganglionic eminencederived neocortical interneurons expresses the transcription factor Sp8. Cereb. Cortex 22, 2120-2130 (2012).
54. Riccio, O. et al. New pool of cortical interneuron precursors in the early postnatal dorsal white matter. Cereb. Cortex 22, 86-98 (2012).
55. Jiménez, D., López-Mascaraque, L. M., Valverde, F. & De Carlos, J. A. Tangential migration in neocortical development. Dev. Biol. 244, 155-169 (2002).
56. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012).
57. Anders, S., Pyl, P. T. & Huber, W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015)
58. Arber, S. et al. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 26, 485-498 (2000).
59. De Marco Garcia, N. V., Karayannis, T. & Fishell, G. Neuronal activity is required for the development of specific cortical interneuron subtypes. Nature 472, 351-355 (2011).