Evolution of Osteocrin as an activity-regulated factor in the primate brain

Ataman, Bulent; Boulting, Gabriella L.; Harmin, David A.; Yang, Marty G.; Baker-Salisbury, Mollie; Yap, Ee-Lynn; Malik, Athar N.; Mei, Kevin; Rubin, Alex A.; Spiegel, Ivo; Durresi, Ershela; Sharma, Nikhil; Hu, Linda; Pletikos, Mihovil; Griffith, Eric C.; Partlow, Jennifer N.; Stevens, Christine; Adli, Mazhar; Chahrour, Maria H.; Šestan, Nenad; Walsh, Christopher A.; Березовский, В. К.; Livingstone, Margaret S.; Greenberg, Michael E.

doi:10.1038/nature20111

Cited by 109 publications

(122 citation statements)

References 45 publications

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“…This process occurs in a transcription-independent manner [30]. Once active, IEGs promote the transcription of late response genes in an activity-dependent and cell-type specific manner [4, 6, 28, 31–33]. Importantly, these transcriptional responses mimic gene induction events observed in intact rodent brain in response to physiological stimuli such as visual experience, seizures and cocaine exposure [34–37].…”

Section: Resultsmentioning

confidence: 99%

Rem2 signaling affects neuronal structure and function in part by regulation of gene expression

Kenny

Royer

Moore

et al. 2017

Molecular and Cellular Neuroscience

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The central nervous system has the remarkable ability to convert changes in the environment in the form of sensory experience into long-term alterations in synaptic connections and dendritic arborization, in part through changes in gene expression. Surprisingly, the molecular mechanisms that translate neuronal activity into changes in neuronal connectivity and morphology remain elusive. Rem2, a member of the Rad/Rem/Rem2/Gem/Kir (RGK) subfamily of small Ras-like GTPases, is a positive regulator of synapse formation and negative regulator of dendritic arborization. Here we identify that one output of Rem2 signaling is the regulation of gene expression. Specifically, we demonstrate that Rem2 signaling modulates the expression of genes required for a variety of cellular processes from neurite extension to synapse formation and synaptic function. Our results highlight Rem2 as a unique molecule that transduces changes in neuronal activity detected at the cell membrane to morphologically relevant changes in gene expression in the nucleus.

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Section: Resultsmentioning

confidence: 99%

Rem2 signaling affects neuronal structure and function in part by regulation of gene expression

Kenny

Royer

Moore

et al. 2017

Molecular and Cellular Neuroscience

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“…), such as acquisition of Osteocrin in primates (Ataman et al . ). Here, we discuss the potential roles of Foxg1 in the acquisition of specific features from cerebrum expansion to neuronal circuit formation.…”

Section: Conversion In the Cis‐regulatory Network And The Foxg1 Functmentioning

confidence: 97%

Evolutionary conservation and conversion of Foxg1 function in brain development

Kumamoto

Hanashima

2017

Dev Growth Differ

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Among the forkhead box protein family, Foxg1 is a unique transcription factor that plays pleiotropic and non-redundant roles in vertebrate brain development. The emergence of the telencephalon at the rostral end of the neural tube and its subsequent expansion that is mediated by Foxg1 was a key reason for the vertebrate brain to acquire higher order information processing, where Foxg1 is repetitively used in the sequential events of telencephalic development to control multi-steps of brain circuit formation ranging from cell cycle control to neuronal differentiation in a clade- and species-specific manner. The objective of this review is to discuss how the evolutionary changes in cis- and trans-regulatory network that is mediated by a single transcription factor has contributed to determining the fundamental vertebrate brain structure and its divergent roles in instructing species-specific neuronal circuitry and functional specialization.

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“…In rare cases, a gene was enriched as a specific marker in one cell class in primates (e.g. OSTN in PVALB + interneurons) but not detected at all in mouse interneurons 20 , or vice versa (e.g., HTR3A , which encodes serotonin receptor 3a, see also 7 ). Other examples included synuclein gamma ( Sncg ), the short transient receptor potential channel 3 ( Trpc3 ), and the IQ motif containing GTPase activating protein 2 ( Iqgap2 ), which were expressed specifically in certain classes of interneurons in mice, but were either widely expressed ( SNCG ) or enriched in a different population ( TRPC3, IQGAP2 ) among neocortical interneurons from primates (Extended Data Fig.…”

Section: Introductionmentioning

confidence: 99%

Innovations in Primate Interneuron Repertoire

Krienen

Goldman

Zhang

et al. 2019

Preprint

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26Primates and rodents, which descended from a common ancestor more than 90 million years 27 ago, exhibit profound differences in behavior and cognitive capacity. Modifications, 28 specializations, and innovations to brain cell types may have occurred along each lineage. We 29 used Drop-seq to profile RNA expression in more than 184,000 individual telencephalic 30 interneurons from humans, macaques, marmosets, and mice. Conserved interneuron types 31 varied significantly in abundance and RNA expression between mice and primates, but varied 32 much more modestly among primates. In adult primates, the expression patterns of dozens of 33 genes exhibited spatial expression gradients among neocortical interneurons, suggesting that 34 adult neocortical interneurons are imprinted by their local cortical context. In addition, we found 35 that an interneuron type previously associated with the mouse hippocampus-the "ivy cell", which 36 has neurogliaform characteristics-has become abundant across the neocortex of humans, 37 macaques, and marmosets. The most striking innovation was subcortical: we identified an 38 abundant striatal interneuron type in primates that had no molecularly homologous cell population 39 in mouse striatum, cortex, thalamus, or hippocampus. These interneurons, which expressed a 40 unique combination of transcription factors, receptors, and neuropeptides, including the 41 neuropeptide TAC3, constituted almost 30% of striatal interneurons in marmosets and humans. 42Understanding how gene and cell-type attributes changed or persisted over the evolutionary 43 divergence of primates and rodents will guide the choice of models for human brain disorders and 44 mutations and help to identify the cellular substrates of expanded cognition in humans and other 45 primates. 46 47 53 54 Brain structures, circuits, and cell types have acquired adaptations and new functions along 55 specific evolutionary lineages. Numerous examples of modifications to specific cell types within 56 larger conserved brain systems have been discovered, including hindbrain circuits that control 57 species-specific courtship calls in frogs 3 , the evolution of trichromatic vision in primates 4 , and 58 neurons that have converted from motor to sensory processing to produce a novel swimming 59 behavior in sand crabs 5 . Evolution can modify brain structures through a wide range of 60 mechanisms, including increasing or reducing production of cells of a given type, altering the 61 molecular and cellular properties of shared cell types, reallocating or redeploying cell types to 62 new locations in the brain, or inventing entirely new cell types (Fig. 1a). 63 64 Single-cell RNA sequencing, which systematically measures gene expression in thousands of 65 individual cells, has recently enabled detailed comparisons of cell types and expression patterns 66 between homologous brain structures separated by millions of years of evolution 4,6,7 (non-single 67 cell approaches have also yielded important insights in this domain, e.g. 8 ). For example...

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Evolution of Osteocrin as an activity-regulated factor in the primate brain

Cited by 109 publications

References 45 publications

Rem2 signaling affects neuronal structure and function in part by regulation of gene expression

Rem2 signaling affects neuronal structure and function in part by regulation of gene expression

Evolutionary conservation and conversion of Foxg1 function in brain development

Innovations in Primate Interneuron Repertoire

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