Expression profiling of mouse subplate reveals a dynamic gene network and disease association with autism and schizophrenia

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 9, 2013, Pages 3555-3560

  Hoerder Suabedissen, Anna ^a   Oeschger, Franziska M ^a   Krishnan, Michelle L ^b   Belgard, T Grant ^a,d   Wang, Wei Zhi ^a   Lee, Sheena ^a   Webber, Caleb ^a   Petretto, Enrico ^c   Edwards, A David ^b   Molnár, Zoltán ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b ST THOMAS HOSPITAL   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Interstitial white matter cells; Microarray; Nxph4; RNAseq; Tpd52l1

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTISM; BRAIN DEVELOPMENT; DISEASE ASSOCIATION; EMBRYO DEVELOPMENT; GENE EXPRESSION PROFILING; MALE; MARKER GENE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RNA SEQUENCE; SCHIZOPHRENIA;

ANIMALS; ANIMALS, NEWBORN; AUTISTIC DISORDER; CEREBRAL CORTEX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; MICE; MICE, INBRED C57BL; ORGAN SPECIFICITY; PROTEIN INTERACTION MAPS; SCHIZOPHRENIA; TIME FACTORS;

EID: 84874481845     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1218510110     Document Type: Article

References (62)

1. Kostovic I, Rakic P (1990) Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297(3): 441-470.
2. Allendoerfer KL, Shatz CJ (1994) The subplate, a transient neocortical structure: Its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 17: 185-218.
3. Price DJ, Aslam S, Tasker L, Gillies K (1997) Fates of the earliest generated cells in the developing murine neocortex. J Comp Neurol 377(3): 414-422.
4. Hoerder-Suabedissen A, Molnár Z (2012) Diversity of early-born subplate neurons. Cereb Cortex, PMID: 22628460.
5. Chen Y, Magnani D, Theil T, Pratt T, Price DJ (2012) Evidence that descending cortical axons are essential for thalamocortical axons to cross the pallial-subpallial boundary in the embryonic forebrain. PLoS ONE 7(3):e33105.
6. McConnell SK, Ghosh A, Shatz CJ (1989) Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245(4921): 978-982.
7. Ghosh A, Antonini A, McConnell SK, Shatz CJ (1990) Requirement for subplate neurons in the formation of thalamocortical connections. Nature 347(6289): 179-181.
8. Dupont E, Hanganu IL, Kilb W, Hirsch S, Luhmann HJ (2006) Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 439(7072): 79-83.
9. Yang JW, Hanganu-Opatz IL, Sun JJ, Luhmann HJ (2009) Three patterns of oscillatory activity differentially synchronize developing neocortical networks in vivo. J Neurosci 29(28): 9011-9025.
10. Kanold PO, Kara P, Reid RC, Shatz CJ (2003) Role of subplate neurons in functional maturation of visual cortical columns. Science 301(5632): 521-525.
11. Kanold PO, Shatz CJ (2006) Subplate neurons regulate maturation of cortical inhibition and outcome of ocular dominance plasticity. Neuron 51(5): 627-638.
12. Friedlander MJ, Torres-Reveron J (2009) The changing roles of neurons in the cortical subplate. Front Neuroanat 3: 15.
13. Suárez-Solá ML, et al. (2009) Neurons in the white matter of the adult human neocortex. Front Neuroanat 3: 7.
14. García-Marín V, Blazquez-Llorca L, Rodriguez JR, Gonzalez-Soriano J, DeFelipe J (2010) Differential distribution of neurons in the gyral white matter of the human cerebral cortex. J Comp Neurol 518(23): 4740-4759.
15. Kostović I, Judaš M, Sedmak G (2011) Developmental history of the subplate zone, subplate neurons and interstitial white matter neurons: Relevance for schizophrenia. Int J Dev Neurosci 29(3): 193-205.
16. Osheroff H, Hatten ME (2009) Gene expression profiling of preplate neurons destined for the subplate: Genes involved in transcription, axon extension, neurotransmitter regulation, steroid hormone signaling, and neuronal survival. Cereb Cortex 19(Suppl 1):i126-i134.
17. Oeschger FM, et al. (2012) Gene expression analysis of the embryonic subplate. Cereb Cortex 22(6): 1343-1359.
18. Hoerder-Suabedissen A, et al. (2009) Novel markers reveal subpopulations of subplate neurons in the murine cerebral cortex. Cereb Cortex 19(8): 1738-1750.
19. Belgard TG, et al. (2011) A transcriptomic atlas of mouse neocortical layers. Neuron 71(4): 605-616.
20. Lage K, et al. (2007) A human phenome-interactome network of protein complexes implicated in genetic disorders. Nat Biotechnol 25(3): 309-316.
21. Akbarian S, et al. (1996) Maldistribution of interstitial neurons in prefrontal white matter of the brains of schizophrenic patients. Arch Gen Psychiatry 53(5): 425-436.
22. Eastwood SL, Harrison PJ (2005) Interstitial white matter neuron density in the dorsolateral prefrontal cortex and parahippocampal gyrus in schizophrenia. Schizophr Res 79(2-3): 181-188.
23. Hutsler JJ, Love T, Zhang H (2007) Histological and magnetic resonance imaging assessment of cortical layering and thickness in autism spectrum disorders. Biol Psychiatry 61(4): 449-457.
24. Avino TA, Hutsler JJ (2010) Abnormal cell patterning at the cortical gray-white matter boundary in autism spectrum disorders. Brain Res 1360: 138-146.
25. Ang LC, Shul DD (1995) Peptidergic neurons of subcortical white matter in aging and Alzheimer's brain. Brain Res 674(2): 329-335.
26. Pinto D, et al. (2010) Functional impact of global rare copy number variation in autism spectrum disorders. Nature 466(7304): 368-372.
27. Sun J, et al. (2009) A multi-dimensional evidence-based candidate gene prioritization approach for complex diseases-schizophrenia as a case. Bioinformatics 25(19): 2595-6602.
28. Bertram L, McQueen MB, Mullin K, Blacker D, Tanzi RE (2007) Systematic metaanalyses of Alzheimer disease genetic association studies: The AlzGene database. Nat Genet 39(1): 17-23.
29. Su AI, et al. (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101(16): 6062-6067.
30. Hlavanda E, et al. (2007) Phosphorylation blocks the activity of tubulin polymerization- promoting protein (TPPP): Identification of sites targeted by different kinases. J Biol Chem 282(40): 29531-29539.
31. Rakić S, Davis C, Molnár Z, Nikolić M, Parnavelas JG (2006) Role of p35/Cdk5 in preplate splitting in the developing cerebral cortex. Cereb Cortex 16(Suppl 1):i35-i45.
32. Artigiani S, et al. (2004) Plexin-B3 is a functional receptor for semaphorin 5A. EMBO Rep 5(7): 710-714.
33. Matsumoto-Miyai K, et al. (2009) Coincident pre- and postsynaptic activation induces dendritic filopodia via neurotrypsin-dependent agrin cleavage. Cell 136(6): 1161-1171.
34. Voineskos AN, et al. (2011) Neurexin-1 and frontal lobe white matter: An overlapping intermediate phenotype for schizophrenia and autism spectrum disorders. PLoS ONE 6(6):e20982.
35. Bedogni F, et al. (2010) Tbr1 regulates regional and laminar identity of postmitotic neurons in developing neocortex. Proc Natl Acad Sci USA 107(29): 13129-13134.
36. Mowry BJ, Gratten J (2013) The emerging spectrum of allelic variation in schizophrenia: Current evidence and strategies for the identification and functional characterization of common and rare variants. Mol Psychiatry 18(1): 38-52.
37. Ayoub AE, Kostovic I (2009) New horizons for the subplate zone and its pioneering neurons. Cereb Cortex 19(8): 1705-1707.
38. McKellar CE, Shatz CJ (2009) Synaptogenesis in purified cortical subplate neurons. Cereb Cortex 19(8): 1723-1737.
39. Clascá F, Angelucci A, Sur M (1995) Layer-specific programs of development in neocortical projection neurons. Proc Natl Acad Sci USA 92(24): 11145-11149.
40. Lai T, et al. (2008) SOX5 controls the sequential generation of distinct corticofugal neuron subtypes. Neuron 57(2): 232-247.
41. Kwan KY, et al. (2008) SOX5 postmitotically regulates migration, postmigratory differentiation, and projections of subplate and deep-layer neocortical neurons. Proc Natl Acad Sci USA 105(41): 16021-16026.
42. De Carlos JA, O'Leary DD (1992) Growth and targeting of subplate axons and establishment of major cortical pathways. J Neurosci 12(4): 1194-1211.
43. Molnár Z, Blakemore C (1995) How do thalamic axons find their way to the cortex? Trends Neurosci 18(9): 389-397.
44. Molnár Z, Adams R, Blakemore C (1998) Mechanisms underlying the early establishment of thalamocortical connections in the rat. J Neurosci 18(15): 5723-5745.
45. HerrmannK, Antonini A, Shatz CJ (1994) Ultrastructural evidence for synaptic interactions between thalamocortical axons and subplate neurons. Eur J Neurosci 6(11): 1729-1742.
46. Friauf E, Shatz CJ (1991) Changing patterns of synaptic input to subplate and cortical plate during development of visual cortex. J Neurophysiol 66(6): 2059-2071.
47. Molnár Z, Kurotani T, Higashi S, Yamamoto N, Toyama K (2003) Development of functional thalamocortical synapses studied with current source-density analysis in whole forebrain slices in the rat. Brain Res Bull 60(4): 355-371.
48. Kanold PO, Luhmann HJ (2010) The subplate and early cortical circuits. Annu Rev Neurosci 33: 23-48.
49. Hanganu IL, Kilb W, Luhmann HJ (2002) Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J Neurosci 22(16): 7165-7176.
50. Stritt C, et al. (2009) Paracrine control of oligodendrocyte differentiation by SRF-directed neuronal gene expression. Nat Neurosci 12(4): 418-427.
51. Hevner RF, et al. (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29(2): 353-366.
52. Wang WZ, Oeschger FM, Lee S, Molnár Z (2009) High quality RNA from multiple brain regions simultaneously acquired by laser capture microdissection. BMC Mol Biol 10: 69.
53. Gentleman RC, et al. (2004) Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 5(10):R80.
54. Smyth GK (2005) Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor, eds Gentleman RC, et al. (Springer, New York), pp 397-420.
55. Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20(3): 307-315.
56. Trapnell C, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5): 511-515.
57. Visel A, Thaller C, Eichele G (2004) GenePaint.org: An atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 32(Database issue):D552-D556.
58. Ng L, et al. (2009) An anatomic gene expression atlas of the adult mouse brain. Nat Neurosci 12(3): 356-362.
59. Lein ES, et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445(7124): 168-176.
60. GenMAPP (2011) GO-Elite: Pathway Analysis Tool. Available at www.genmapp.org/go-elite/. Accessed November 11, 2011.
61. Maere S, Heymans K, Kuiper M (2005) BiNGO: A Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21(16): 3448-3449.
62. Zhang C, et al. (2012) Mosaic: Making biological sense of complex networks. Bioinformatics 28(14): 1943-1944.