Multi-Scale Molecular Deconstruction of the Serotonin Neuron System

Neuron

Volumn 88, Issue 4, 2015, Pages 774-791

  Okaty, Benjamin W ^a   Freret, Morgan E ^a   Rood, Benjamin D ^a   Brust, Rachael D ^a   Hennessy, Morgan L ^a   deBairos, Danielle ^a   Kim, Jun Chul ^b   Cook, Melloni N ^c   Dymecki, Susan M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c University of Memphis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL FATE; CELL FUNCTION; CELL POPULATION; CELL SELECTION; CONTROLLED STUDY; GENE EXPRESSION; GENE INACTIVATION; GENETIC VARIABILITY; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA SEQUENCE; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; ANIMAL; BRAIN; CLASSIFICATION; CYTOLOGY; ELECTROPHYSIOLOGY; GENE EXPRESSION PROFILING; KNOCKOUT MOUSE; METABOLISM; SEQUENCE ANALYSIS;

ANIMALS; BRAIN; ELECTROPHYSIOLOGICAL PHENOMENA; GENE EXPRESSION PROFILING; MICE; MICE, KNOCKOUT; PHENOTYPE; SEQUENCE ANALYSIS, RNA; SEROTONERGIC NEURONS;

EID: 84953706727     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.10.007     Document Type: Article

References (51)

1. Allers K.A., Sharp T. Neurochemical and anatomical identification of fast- and slow-firing neurones in the rat dorsal raphe nucleus using juxtacellular labelling methods in vivo. Neuroscience 2003, 122:193-204.
2. Anders S., McCarthy D.J., Chen Y., Okoniewski M., Smyth G.K., Huber W., Robinson M.D. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nat. Protoc. 2013, 8:1765-1786.
3. Awatramani R., Soriano P., Rodriguez C., Mai J.J., Dymecki S.M. Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat. Genet. 2003, 35:70-75.
4. Bang S.J., Jensen P., Dymecki S.M., Commons K.G. Projections and interconnections of genetically defined serotonin neurons in mice. Eur. J. Neurosci. 2012, 35:85-96.
5. Braff D.L., Geyer M.A., Swerdlow N.R. Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl.) 2001, 156:234-258.
6. Brennecke P., Anders S., Kim J.K., Kołodziejczyk A.A., Zhang X., Proserpio V., Baying B., Benes V., Teichmann S.A., Marioni J.C., Heisler M.G. Accounting for technical noise in single-cell RNA-seq experiments. Nat. Methods 2013, 10:1093-1095.
7. Brust R.D., Corcoran A.E., Richerson G.B., Nattie E., Dymecki S.M. Functional and developmental identification of a molecular subtype of brain serotonergic neuron specialized to regulate breathing dynamics. Cell Rep. 2014, 9:2152-2165.
8. Calizo L.H., Akanwa A., Ma X., Pan Y.Z., Lemos J.C., Craige C., Heemstra L.A., Beck S.G. Raphe serotonin neurons are not homogenous: electrophysiological, morphological and neurochemical evidence. Neuropharmacology 2011, 61:524-543.
9. Campbell D.B., Sutcliffe J.S., Ebert P.J., Militerni R., Bravaccio C., Trillo S., Elia M., Schneider C., Melmed R., Sacco R., et al. A genetic variant that disrupts MET transcription is associated with autism. Proc. Natl. Acad. Sci. USA 2006, 103:16834-16839.
10. Campbell D.B., Datta D., Jones S.T., Batey Lee E., Sutcliffe J.S., Hammock E.A., Levitt P. Association of oxytocin receptor (OXTR) gene variants with multiple phenotype domains of autism spectrum disorder. J. Neurodev. Disord. 2011, 3:101-112.
11. Crawford L.K., Craige C.P., Beck S.G. Increased intrinsic excitability of lateral wing serotonin neurons of the dorsal raphe: a mechanism for selective activation in stress circuits. J. Neurophysiol. 2010, 103:2652-2663.
12. Dougherty J.D., Maloney S.E., Wozniak D.F., Rieger M.A., Sonnenblick L., Coppola G., Mahieu N.G., Zhang J., Cai J., Patti G.J., et al. The disruption of Celf6, a gene identified by translational profiling of serotonergic neurons, results in autism-related behaviors. J. Neurosci. 2013, 33:2732-2753.
13. Duncan J.R., Paterson D.S., Hoffman J.M., Mokler D.J., Borenstein N.S., Belliveau R.A., Krous H.F., Haas E.A., Stanley C., Nattie E.E., et al. Brainstem serotonergic deficiency in sudden infant death syndrome. JAMA 2010, 303:430-437.
14. Dymecki S.M., Ray R.S., Kim J.C. Mapping cell fate and function using recombinase-based intersectional strategies. Methods Enzymol. 2010, 477:183-213.
15. Fishell G., Heintz N. The neuron identity problem: form meets function. Neuron 2013, 80:602-612.
16. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 2007, Academic Press. Third Edition.
17. Gaspar P., Lillesaar C. Probing the diversity of serotonin neurons. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 367:2382-2394.
18. Hale M.W., Lowry C.A. Functional topography of midbrain and pontine serotonergic systems: implications for synaptic regulation of serotonergic circuits. Psychopharmacology (Berl.) 2011, 213:243-264.
19. Hempel C.M., Sugino K., Nelson S.B. A manual method for the purification of fluorescently labeled neurons from the mammalian brain. Nat. Protoc. 2007, 2:2924-2929.
20. Hendricks T., Francis N., Fyodorov D., Deneris E.S. The ETS domain factor Pet-1 is an early and precise marker of central serotonin neurons and interacts with a conserved element in serotonergic genes. J. Neurosci. 1999, 19:10348-10356.
21. Huh C.G., Factor V.M., Sánchez A., Uchida K., Conner E.A., Thorgeirsson S.S. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc. Natl. Acad. Sci. USA 2004, 101:4477-4482.
22. Jacob S., Brune C.W., Carter C.S., Leventhal B.L., Lord C., Cook E.H. Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism. Neurosci. Lett. 2007, 417:6-9.
23. Jensen P., Farago A.F., Awatramani R.B., Scott M.M., Deneris E.S., Dymecki S.M. Redefining the serotonergic system by genetic lineage. Nat. Neurosci. 2008, 11:417-419.
24. Kharchenko P.V., Silberstein L., Scadden D.T. Bayesian approach to single-cell differential expression analysis. Nat. Methods 2014, 11:740-742.
25. Kim J.C., Cook M.N., Carey M.R., Shen C., Regehr W.G., Dymecki S.M. Linking genetically defined neurons to behavior through a broadly applicable silencing allele. Neuron 2009, 63:305-315.
26. Kimmel R.A., Turnbull D.H., Blanquet V., Wurst W., Loomis C.A., Joyner A.L. Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev. 2000, 14:1377-1389.
27. Kinney H.C., Richerson G.B., Dymecki S.M., Darnall R.A., Nattie E.E. The brainstem and serotonin in the sudden infant death syndrome. Annu. Rev. Pathol. 2009, 4:517-550.
28. Kiyasova V., Fernandez S.P., Laine J., Stankovski L., Muzerelle A., Doly S., Gaspar P. A genetically defined morphologically and functionally unique subset of 5-HT neurons in the mouse raphe nuclei. J. Neurosci. 2011, 31:2756-2768.
29. Lambert N., Wermenbol V., Pichon B., Acosta S., van den Ameele J., Perazzolo C., Messina D., Musumeci M.F., Dessars B., De Leener A., et al. A familial heterozygous null mutation of MET in autism spectrum disorder. Autism Res. 2014, 7:617-622.
30. Lerer E., Levi S., Salomon S., Darvasi A., Yirmiya N., Ebstein R.P. Association between the oxytocin receptor (OXTR) gene and autism: relationship to Vineland Adaptive Behavior Scales and cognition. Mol. Psychiatry 2008, 13:980-988.
31. Liu X., Kawamura Y., Shimada T., Otowa T., Koishi S., Sugiyama T., Nishida H., Hashimoto O., Nakagami R., Tochigi M., et al. Association of the oxytocin receptor (OXTR) gene polymorphisms with autism spectrum disorder (ASD) in the Japanese population. J. Hum. Genet. 2010, 55:137-141.
32. Lyubimova A., Itzkovitz S., Junker J.P., Fan Z.P., Wu X., van Oudenaarden A. Single-molecule mRNA detection and counting in mammalian tissue. Nat. Protoc. 2013, 8:1743-1758.
33. Maloney S.E., Rieger M.A., Dougherty J.D. Identifying essential cell types and circuits in autism spectrum disorders. Int. Rev. Neurobiol. 2013, 113:61-96.
34. Masland R.H. Neuronal cell types. Curr. Biol. 2004, 14:R497-R500.
35. Nelson S.B., Sugino K., Hempel C.M. The problem of neuronal cell types: a physiological genomics approach. Trends Neurosci. 2006, 29:339-345.
36. O'Hearn E., Molliver M.E. Organization of raphe-cortical projections in rat: a quantitative retrograde study. Brain Res. Bull. 1984, 13:709-726.
37. Okaty B.W., Sugino K., Nelson S.B. Cell type-specific transcriptomics in the brain. J. Neurosci. 2011, 31:6939-6943.
38. Okaty B.W., Sugino K., Nelson S.B. A quantitative comparison of cell-type-specific microarray gene expression profiling methods in the mouse brain. PLoS ONE 2011, 6:e16493.
39. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
40. Rudie J.D., Hernandez L.M., Brown J.A., Beck-Pancer D., Colich N.L., Gorrindo P., Thompson P.M., Geschwind D.H., Bookheimer S.Y., Levitt P., Dapretto M. Autism-associated promoter variant in MET impacts functional and structural brain networks. Neuron 2012, 75:904-915.
41. Scott M.M., Wylie C.J., Lerch J.K., Murphy R., Lobur K., Herlitze S., Jiang W., Conlon R.A., Strowbridge B.W., Deneris E.S. A genetic approach to access serotonin neurons for in vivo and in vitro studies. Proc. Natl. Acad. Sci. USA 2005, 102:16472-16477.
42. Shalek A.K., Satija R., Adiconis X., Gertner R.S., Gaublomme J.T., Raychowdhury R., Schwartz S., Yosef N., Malboeuf C., Lu D., et al. Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature 2013, 498:236-240.
43. Shalek A.K., Satija R., Shuga J., Trombetta J.J., Gennert D., Lu D., Chen P., Gertner R.S., Gaublomme J.T., Yosef N., et al. Single-cell RNA-seq reveals dynamic paracrine control of cellular variation. Nature 2014, 510:363-369.
44. Spaethling J.M., Piel D., Dueck H., Buckley P.T., Morris J.F., Fisher S.A., Lee J., Sul J.Y., Kim J., Bartfai T., et al. Serotonergic neuron regulation informed by in vivo single-cell transcriptomics. FASEB J. 2014, 28:771-780.
45. Sugino K., Hempel C.M., Miller M.N., Hattox A.M., Shapiro P., Wu C., Huang Z.J., Nelson S.B. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat. Neurosci. 2006, 9:99-107.
46. Voiculescu O., Charnay P., Schneider-Maunoury S. Expression pattern of a Krox-20/Cre knock-in allele in the developing hindbrain, bones, and peripheral nervous system. Genesis 2000, 26:123-126.
47. Wu H.H., Levitt P. Prenatal expression of MET receptor tyrosine kinase in the fetal mouse dorsal raphe nuclei and the visceral motor/sensory brainstem. Dev. Neurosci. 2013, 35:1-16.
48. Wu S., Jia M., Ruan Y., Liu J., Guo Y., Shuang M., Gong X., Zhang Y., Yang X., Zhang D. Positive association of the oxytocin receptor gene (OXTR) with autism in the Chinese Han population. Biol. Psychiatry 2005, 58:74-77.
49. Wylie C.J., Hendricks T.J., Zhang B., Wang L., Lu P., Leahy P., Fox S., Maeno H., Deneris E.S. Distinct transcriptomes define rostral and caudal serotonin neurons. J. Neurosci. 2010, 30:670-684.
50. Young M.D., Wakefield M.J., Smyth G.K., Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010, 11:R14.
51. Zheng H. Generation of a Tac1 cre knock-in allele 2013, MGI Direct Data Submission.