Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates

Jeremy A. Miller, Jason Nathanson, Daniel Franjic, Sungbo Shim, Rachel A. Dalley, Sheila Shapouri, Kimberly A. Smith, Susan M. Sunkin, Amy Bernard, Jeffrey L. Bennett, Chang Kyu Lee, Michael J. Hawrylycz, Allan R. Jones, David G Amaral, Nenad Šestan, Fred H. Gage, Ed S. Lein

Research output: Contribution to journalArticle

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Abstract

The neurogenic potential of the subgranular zone (SGZ) of the hippocampal dentate gyrus is likely to be regulated by molecular cues arising from its complex heterogeneous cellular environment. Through transcriptome analysis using laser microdissection coupled with DNA microarrays, in combination with analysis of genome-wide in situ hybridization data, we identified 363 genes selectively enriched in adult mouse SGZ. These genes reflect expression in the different constituent cell types, including progenitor and dividing cells, immature granule cells, astrocytes, oligodendrocytes and GABAergic interneurons. Similar transcriptional profiling in the rhesus monkey dentate gyrus across postnatal development identified a highly overlapping set of SGZ-enriched genes, which can be divided based on temporal profiles to reflect maturation of glia versus granule neurons. Furthermore, we identified a neurogenesis-related gene network with decreasing postnatal expression that is highly correlated with the declining number of proliferating cells in dentate gyrus over postnatal development. Many of the genes in this network showed similar postnatal downregulation in mouse, suggesting a conservation of molecular mechanisms underlying developmental and adult neurogenesis in rodents and primates. Conditional deletion of Sox4 and Sox11, encoding two neurogenesis-related transcription factors central in this network, produces a mouse with no hippocampus, confirming the crucial role for these genes in regulating hippocampal neurogenesis.

Original languageEnglish (US)
Pages (from-to)4633-4644
Number of pages12
JournalDevelopment (Cambridge)
Volume140
Issue number22
DOIs
StatePublished - Nov 15 2013

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Neurogenesis
Primates
Rodentia
Dentate Gyrus
Gene Regulatory Networks
Genes
Parahippocampal Gyrus
Microdissection
Oligodendroglia
Gene Expression Profiling
Interneurons
Oligonucleotide Array Sequence Analysis
Macaca mulatta
Neuroglia
Astrocytes
In Situ Hybridization
Cues
Hippocampus
Lasers
Transcription Factors

Keywords

  • Development
  • Hippocampus
  • Neurogenesis
  • Rhesus monkey
  • Subgranular zone
  • Transcriptome

ASJC Scopus subject areas

  • Developmental Biology
  • Molecular Biology

Cite this

Miller, J. A., Nathanson, J., Franjic, D., Shim, S., Dalley, R. A., Shapouri, S., ... Lein, E. S. (2013). Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates. Development (Cambridge), 140(22), 4633-4644. https://doi.org/10.1242/dev.097212

Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates. / Miller, Jeremy A.; Nathanson, Jason; Franjic, Daniel; Shim, Sungbo; Dalley, Rachel A.; Shapouri, Sheila; Smith, Kimberly A.; Sunkin, Susan M.; Bernard, Amy; Bennett, Jeffrey L.; Lee, Chang Kyu; Hawrylycz, Michael J.; Jones, Allan R.; Amaral, David G; Šestan, Nenad; Gage, Fred H.; Lein, Ed S.

In: Development (Cambridge), Vol. 140, No. 22, 15.11.2013, p. 4633-4644.

Research output: Contribution to journalArticle

Miller, JA, Nathanson, J, Franjic, D, Shim, S, Dalley, RA, Shapouri, S, Smith, KA, Sunkin, SM, Bernard, A, Bennett, JL, Lee, CK, Hawrylycz, MJ, Jones, AR, Amaral, DG, Šestan, N, Gage, FH & Lein, ES 2013, 'Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates', Development (Cambridge), vol. 140, no. 22, pp. 4633-4644. https://doi.org/10.1242/dev.097212
Miller, Jeremy A. ; Nathanson, Jason ; Franjic, Daniel ; Shim, Sungbo ; Dalley, Rachel A. ; Shapouri, Sheila ; Smith, Kimberly A. ; Sunkin, Susan M. ; Bernard, Amy ; Bennett, Jeffrey L. ; Lee, Chang Kyu ; Hawrylycz, Michael J. ; Jones, Allan R. ; Amaral, David G ; Šestan, Nenad ; Gage, Fred H. ; Lein, Ed S. / Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates. In: Development (Cambridge). 2013 ; Vol. 140, No. 22. pp. 4633-4644.
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