RNA-seq analysis of developing olfactory bulb projection neurons

Molecular and Cellular Neuroscience

Volumn 74, Issue , 2016, Pages 78-86

  Kawasawa, Yuka Imamura ^a   Salzberg, Anna C ^a   Li, Mingfeng ^b   Šestan, Nenad ^b   Greer, Charles A ^b   Imamura, Fumiaki ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alternative splicing; Cell type specific transcriptome; Mitral cell; Neuronal development; Olfactory bulb; Pyramidal neuron; RNA seq

Indexed keywords

GREEN FLUORESCENT PROTEIN; TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE EXPRESSION PROFILING; GENOME ANALYSIS; MITRAL CELL; MOLECULAR MODEL; MOUSE; NEOCORTEX; NERVE PROJECTION; NEXT GENERATION SEQUENCING; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; RNA SEQUENCE; SEQUENCE ANALYSIS; TRANSCRIPTOMICS; ANIMAL; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; METABOLISM; NERVE CELL; OPEN READING FRAME;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; NEURONS; OLFACTORY BULB; OPEN READING FRAMES; TRANSCRIPTOME;

EID: 84964968297     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2016.03.009     Document Type: Article

References (60)

1. Anders S., Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010, 11:R106.
2. Arlotta P., Molyneaux B.J., Chen J., Inoue J., Kominami R., Macklis J.D. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 2005, 45:207-221.
3. Blanchart A., De Carlos J.A., López-Mascaraque L. Time frame of mitral cell development in the mice olfactory bulb. J. Comp. Neurol. 2006, 496:529-543.
4. Brill M.S., Snapyan M., Wohlfrom H., Ninkovic J., Jawerka M., Mastick G.S., Ashery-Padan R., Saghatelyan A., Berninger B., Götz M. A dlx2- and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J. Neurosci. 2008, 28:6439-6452.
5. Brooks A.N., Yang L., Duff M.O., Hansen K.D., Park J.W., Dudoit S., Brenner S.E., Graveley B.R. Conservation of an RNA regulatory map between Drosophila and mammals. Genome Res. 2011, 21:193-202.
6. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., Thompson W.J., Barres B.A. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 2008, 28:264-278.
7. Calinski T., Harabasz J. A dendrite method for cluster analysis. Commun. Stat. 1974, 3:1-27.
8. Campbell G.R., Baudhuin A., Vranizan K., Ngai J. Transcription factors expressed in olfactory bulb local progenitor cells revealed by genome-wide transcriptome profiling. Mol. Cell. Neurosci. 2011, 46:548-561.
9. Chen B., Schaevitz L.R., McConnell S.K. Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:17184-17189.
10. Chen J.G., Rašin M.R., Kwan K.Y., Šestan N. Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:17792-17797.
11. Conesa A., Nueda M.J., Ferrer A., Talon M. maSigPro: a method to identify significantly differential expression profiles in time-course microarray experiments. Bioinformatics 2006, 22:1096-1102.
12. Darmanis S., Sloan S.A., Zhang Y., Enge M., Caneda C., Shuer L.M., Hayden Gephart M.G., Barres B.A., Quake S.R. A survey of human brain transcriptome diversity at the single cell level. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:7285-7290.
13. Feng W., Simoes-de-Souza F., Finger T.E., Restrepo D., Williams T. Disorganized olfactory bulb lamination in mice deficient for transcription factor AP-2epsilon. Mol. Cell. Neurosci. 2009, 42:161-171.
14. Fertuzinhos S., Li M., Kawasawa Y.I., Ivic V., Franjic D., Singh D., Crair M., Sestan N. Laminar and temporal expression dynamics of coding and noncoding RNAs in the mouse neocortex. Cell Rep. 2014, 6:938-950.
15. Flicek P., Ahmed I., Amode M.R., Barrell D., Beal K., Brent S., Carvalho-Silva D., Clapham P., Coates G., Fairley S., Fitzgerald S., Gil L., Garcia-Giron C., Gordon L., Hourlier T., Hunt S., Juettemann T., Kahari A.K., Keenan S., Komorowska M., Kulesha E., Longden I., Maurel T., McLaren W.M., Muffato M., Nag R., Overduin B., Pignatelli M., Pritchard B., Pritchard E., Riat H.S., Ritchie G.R., Ruffier M., Schuster M., Sheppard D., Sobral D., Taylor K., Thormann A., Trevanion S., White S., Wilder S.P., Aken B.L., Birney E., Cunningham F., Dunham I., Harrow J., Herrero J., Hubbard T.J., Johnson N., Kinsella R., Parker A., Spudich G., Yates A., Zadissa A., Searle S.M. Ensembl 2013. Nucleic Acids Res. 2013, 41:D48-D55.
16. Forgy E.W. Cluster analysis of multivariate data: efficiency versus interpretability of classifications. Biometrics 1965, 21:768-769.
17. Gabellec M.M., Panzanelli P., Sassoe-Pognetto M., Lledo P.M. Synapse-specific localization of vesicular glutamate transporters in the rat olfactory bulb. Eur. J. Neurosci. 2007, 25:1373-1383.
18. Galjart N. CLIPs and CLASPs and cellular dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6:487-498.
19. Han W., Kwan K.Y., Shim S., Lam M.M., Shin Y., Xu X., Zhu Y., Li M., Sestan N. TBR1 directly represses Fezf2 to control the laminar origin and development of the corticospinal tract. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3041-3046.
20. Harrison S.J., Nishinakamura R., Monaghan A.P. Sall1 regulates mitral cell development and olfactory nerve extension in the developing olfactory bulb. Cereb. Cortex 2007.
21. Harrison S.J., Parrish M., Monaghan A.P. Sall3 is required for the terminal maturation of olfactory glomerular interneurons. J. Comp. Neurol. 2008, 507:1780-1794.
22. Hinds J.W. Early neuron differentiation in the mouse of olfactory bulb. I. Light microscopy. J. Comp. Neurol. 1972, 146:233-252.
23. Hinds J.W., Hinds P.L. Synapse formation in the mouse olfactory bulb. I. Quantitative studies. J. Comp. Neurol. 1976, 169:15-40.
24. Hooper J.E. A survey of software for genome-wide discovery of differential splicing in RNA-seq data. Hum. Genomics 2014, 8:3.
25. Howe E.A., Sinha R., Schlauch D., Quackenbush J. RNA-seq analysis in MeV. Bioinformatics 2011, 27:3209-3210.
26. Imamura F., Greer C.A. Pax6 regulates Tbr1 and Tbr2 expressions in olfactory bulb mitral cells. Mol. Cell. Neurosci. 2013, 54:58-70.
27. Imamura F., Nagao H., Naritsuka H., Murata Y., Taniguchi H., Mori K. A leucine-rich repeat membrane protein, 5T4, is expressed by a subtype of granule cells with dendritic arbors in specific strata of the mouse olfactory bulb. J. Comp. Neurol. 2006, 495:754-768.
28. Imamura F., Ayoub A.E., Rakic P., Greer C.A. Timing of neurogenesis is a determinant of olfactory circuitry. Nat. Neurosci. 2011, 14:331-337.
29. Inaki K., Nishimura S., Nakashiba T., Itohara S., Yoshihara Y. Laminar organization of the developing lateral olfactory tract revealed by differential expression of cell recognition molecules. J. Comp. Neurol. 2004, 479:243-256.
30. Kiyama H., Sato M., Emson P.C., Tohyama M. Transient expression of neurotensin mRNA in the mitral cells of rat olfactory bulb during development. Neurosci. Lett. 1991, 128:85-89.
31. Koenigkam-Santos M., Santos A.C., Versiani B.R., Diniz P.R., Junior J.E., de Castro M. Quantitative magnetic resonance imaging evaluation of the olfactory system in Kallmann syndrome: correlation with a clinical smell test. Neuroendocrinology 2011, 94:209-217.
32. Kwan K.Y., Sestan N., Anton E.S. Transcriptional co-regulation of neuronal migration and laminar identity in the neocortex. Development 2012, 139:1535-1546.
33. Lalani S.R., Safiullah A.M., Fernbach S.D., Harutyunyan K.G., Thaller C., Peterson L.E., McPherson J.D., Gibbs R.A., White L.D., Hefner M., Davenport S.L., Graham J.M., Bacino C.A., Glass N.L., Towbin J.A., Craigen W.J., Neish S.R., Lin A.E., Belmont J.W. Spectrum of CHD7 mutations in 110 individuals with CHARGE syndrome and genotype-phenotype correlation. Am. J. Hum. Genet. 2006, 78:303-314.
34. Lei W.L., Xing S.G., Deng C.Y., Ju X.C., Jiang X.Y., Luo Z.G. Laminin/beta1 integrin signal triggers axon formation by promoting microtubule assembly and stabilization. Cell Res. 2012, 22:954-972.
35. Mallamaci A., Iannone R., Briata P., Pintonello L., Mercurio S., Boncinelli E., Corte G. EMX2 protein in the developing mouse brain and olfactory area. Mech. Dev. 1998, 77:165-172.
36. McKenna W.L., Betancourt J., Larkin K.A., Abrams B., Guo C., Rubenstein J.L., Chen B. Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J. Neurosci. 2011, 31:549-564.
37. Miller A.M., Treloar H.B., Greer C.A. Composition of the migratory mass during development of the olfactory nerve. J. Comp. Neurol. 2010, 518:4825-4841.
38. Mizuguchi R., Naritsuka H., Mori K., Yoshihara Y. Tbr2 deficiency in mitral and tufted cells disrupts excitatory-inhibitory balance of neural circuitry in the mouse olfactory bulb. J. Neurosci. 2012, 32:8831-8844.
39. Molyneaux B.J., Arlotta P., Hirata T., Hibi M., Macklis J.D. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 2005, 47:817-831.
40. Molyneaux B.J., Arlotta P., Menezes J.R., Macklis J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 2007, 8:427-437.
41. Molyneaux B.J., Goff L.A., Brettler A.C., Chen H.H., Brown J.R., Hrvatin S., Rinn J.L., Arlotta P. DeCoN: genome-wide analysis of in vivo transcriptional dynamics during pyramidal neuron fate selection in neocortex. Neuron 2015, 85:275-288.
42. Mori K., Sakano H. How is the olfactory map formed and interpreted in the mammalian brain?. Annu. Rev. Neurosci. 2011, 34:467-499.
43. Nagai Y., Sano H., Yokoi M. Transgenic expression of Cre recombinase in mitral/tufted cells of the olfactory bulb. Genesis 2005, 43:12-16.
44. Nagayama S., Homma R., Imamura F. Neuronal organization of olfactory bulb circuits. Front. Neural Circuits 2014, 8:98.
45. Nakajima D., Nakayama M., Kikuno R., Hirosawa M., Nagase T., Ohara O. Identification of three novel non-classical cadherin genes through comprehensive analysis of large cDNAs. Brain Res. Mol. Brain Res. 2001, 94:85-95.
46. Okaty B.W., Sugino K., Nelson S.B. Cell type-specific transcriptomics in the brain. J. Neurosci. 2011, 31:6939-6943.
47. Pinto G., Abadie V., Mesnage R., Blustajn J., Cabrol S., Amiel J., Hertz-Pannier L., Bertrand A.M., Lyonnet S., Rappaport R., Netchine I. CHARGE syndrome includes hypogonadotropic hypogonadism and abnormal olfactory bulb development. J. Clin. Endocrinol. Metab. 2005, 90:5621-5626.
48. 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.
49. Shaker T., Dennis D., Kurrasch D.M., Schuurmans C. Neurog1 and Neurog2 coordinately regulate development of the olfactory system. Neural Dev. 2012, 7:28.
50. Shibata M., Gulden F.O., Sestan N. From trans to cis: transcriptional regulatory networks in neocortical development. Trends Genet. 2015, 31:77-87.
51. Sun J., Nishiyama T., Shimizu K., Kadota K. TCC: an R package for comparing tag count data with robust normalization strategies. BMC Bioinformatics 2013, 14:219.
52. Trapnell C., Pachter L., Salzberg S.L. TopHat: discovering splice junctions with RNA-seq. Bioinformatics 2009, 25:1105-1111.
53. Trapnell C., Williams B.A., Pertea G., Mortazavi A., Kwan G., van Baren M.J., Salzberg S.L., Wold B.J., Pachter L. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28:511-515.
54. Treloar H.B., Purcell A.L., Greer C.A. Glomerular formation in the developing rat olfactory bulb. J. Comp. Neurol. 1999, 413:289-304.
55. van de Leemput J., Boles N.C., Kiehl T.R., Corneo B., Lederman P., Menon V., Lee C., Martinez R.A., Levi B.P., Thompson C.L., Yao S., Kaykas A., Temple S., Fasano C.A. CORTECON: a temporal transcriptome analysis of in vitro human cerebral cortex development from human embryonic stem cells. Neuron 2014, 83:51-68.
56. Waclaw R.R., Allen Z.J., Bell S.M., Erdelyi F., Szabo G., Potter S.S., Campbell K. The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 2006, 49:503-516.
57. Walz A., Omura M., Mombaerts P. Development and topography of the lateral olfactory tract in the mouse: imaging by genetically encoded and injected fluorescent markers. J. Neurobiol. 2006, 66:835-846.
58. Wickham H. ggplot2 2009, Springer-Verlag, New York.
59. Wolfer D.P., Giger R.J., Stagliar M., Sonderegger P., Lipp H.P. Expression of the axon growth-related neural adhesion molecule TAG-1/axonin-1 in the adult mouse brain. Anat. Embryol. (Berl.) 1998, 197:177-185.
60. Yoshihara S., Omichi K., Yanazawa M., Kitamura K., Yoshihara Y. Arx homeobox gene is essential for development of mouse olfactory system. Development 2005, 132:751-762.