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Molecular features driving cellular and regulatory complexity of human brain evolution [RNA-seq]

ABSTRACT: Genomic changes acquired in human evolution contribute to the unique abilities of human brain. However, characterizing the molecular underpinnings of human-specific traits is a multifaceted challenge due to the cellular heterogeneity of human brain and complex regulation of gene expression. Here, we performed single-nuclei RNA-sequencing (snRNA-seq) and single-nuclei ATAC-seq (snATAC-seq) in human, chimpanzee, and rhesus macaque brain tissue (brodmann area 23, posterior cingulate cortex). Human-specific changes were distinct among neuronal subtypes indicating that human brain evolution was accompanied by molecular alterations in finer cellular resolution. We also observed more human-specific alterations in epigenome compared to transcriptome. Interestingly, human-specific accessibility changes in neurons were not as concordant with gene expression changes in comparison to other species, partially explaining this discrepancy. These cis-regulatory elements were enriched for immediate early gene motifs, identifying accelerated evolution of activity regulated genes in humans. We also uncovered associations between human evolution and brain disease genes at the cell type level. Together, these results reveal multiple mechanisms for human brain evolution at cell type resolution and establish the first direct evidence for accelerated human-specificity of activity-dependent molecular changes.

ORGANISM(S): Pan troglodytes Homo sapiens Macaca mulatta

PROVIDER: GSE192773 | GEO | 2023/04/26

REPOSITORIES: GEO

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Molecular features driving cellular and regulatory complexity of human brain evolution [ATAC-seq]

Project description:Genomic changes acquired in human evolution contribute to the unique abilities of human brain. However, characterizing the molecular underpinnings of human-specific traits is a multifaceted challenge due to the cellular heterogeneity of human brain and complex regulation of gene expression. Here, we performed single-nuclei RNA-sequencing (snRNA-seq) and single-nuclei ATAC-seq (snATAC-seq) in human, chimpanzee, and rhesus macaque brain tissue (brodmann area 23, posterior cingulate cortex). Human-specific changes were distinct among neuronal subtypes indicating that human brain evolution was accompanied by molecular alterations in finer cellular resolution. We also observed more human-specific alterations in epigenome compared to transcriptome. Interestingly, human-specific accessibility changes in neurons were not as concordant with gene expression changes in comparison to other species, partially explaining this discrepancy. These cis-regulatory elements were enriched for immediate early gene motifs, identifying accelerated evolution of activity regulated genes in humans. We also uncovered associations between human evolution and brain disease genes at the cell type level. Together, these results reveal multiple mechanisms for human brain evolution at cell type resolution and establish the first direct evidence for accelerated human-specificity of activity-dependent molecular changes.

2023-04-26 | GSE192772 | GEO

Accelerated evolution of oligodendrocytes in human brain

Project description:Accelerated evolution of oligodendrocytes in human brain

| PRJNA510347 | ENA

Accelerated evolution of oligodendrocytes in human brain

Project description:Recent discussions of human brain evolution have largely focused on increased neuron numbers and changes in their connectivity and expression. However, it is increasingly appreciated that oligodendrocytes play important roles in cognitive function and disease. Whether both cell types follow distinctive evolutionary trajectories is not known. We examined the transcriptomes of neurons and oligodendrocytes in the frontal cortex of humans, chimpanzees, and rhesus macaques. We identified human-specific trajectories of gene expression in oligodendrocytes and show that oligodendrocytes have undergone accelerated gene expression evolution in the human lineage. The signature of acceleration is enriched for cell type-specific expression alterations in schizophrenia. These results underscore the importance of oligodendrocytes in human brain evolution.

2019-12-31 | GSE123936 | GEO

MicroRNA expression in primate postnatal brain through lifespan

2011-12-09 | GSE29356 | GEO

MicroRNA expression in primate postnatal brain through lifespan

Project description:While multiple studies have reported the accelerated evolution of brain gene expression in the human lineage, the mechanisms underlying such change remain poorly understood. Here we address this issue from a developmental perspective, by analyzing mRNA and microRNA (miRNA) expression in two brain regions within macaques, chimpanzees and humans throughout their lifespan. We find that developmental profiles of trans-regulators, such as miRNA, as well as their target genes, show the fastest rates of human-specific evolutionary change. Changes in expression of a few key regulators may be a major driving force behind human brain evolution. Human, chimpanzee and rhesus macaque post-mortem brain samples from the prefrontal cortex and cerebellar cortex were collected. The age ranges of the individuals in all three species covered the respective species' postnatal maturation period from infancy to old adulthood. RNA extracted from the dissected tissue was hybridized to B72.

2011-12-09 | E-GEOD-29356 | biostudies-arrayexpress

Accelerated functional evolution of regulatory lncRNAs in the human lineage

Project description:Long noncoding RNA sequences evolve relatively rapidly, but it is unclear whether this is due to relaxed constraint or accelerated evolution. Here, we trace the recent evolutionary history of human lncRNAs, using genomes of multiple individuals from all great ape species to map fixed lineage-specific nucleotide variants. We find that the lower conservation of lncRNAs compared to protein coding genes partially arises from lncRNA’s more recent evolutionary origin. We identify more than one hundred lncRNAs that show some evidence of accelerated evolution in at least one primate species, including 17 in human. Several of these display transcriptional regulatory activity in an RNA-specific reporter assay. By experimentally reconstructing the ancestral lncRNA sequence, we find that this activity has been altered by human-specific nucleotide substitutions. Functional analysis of accelerated lncRNAs with specific expression in blood suggests lncRNAs have participated in adaptive regulatory changes in the immune system during recent human evolution. Together our results provide evidence that accelerated evolution of lncRNAs may have contributed, through regulatory changes, to human-specific phenotypes.

2018-11-30 | GSE80554 | GEO

3D Genome of macaque fetal brain reveals evolutionary innovations during primate corticogenesis

Project description:Elucidating the regulatory mechanisms of human brain evolution is essential to understanding human cognition and mental disorders. We generated multi-omics profiles and constructed a high-resolution map of 3D genome architecture of rhesus macaque during corticogenesis. By comparing the 3D genomes of human, macaque and mouse brains, we identified many human-specific chromatin structure changes, including 499 topologically associating domains (TADs) and 1,266 chromatin loops. The human-specific loops are significantly enriched in enhancer-enhancer interactions and the regulated genes show human-specific expression changes in the subplate, a transient zone of the developing brain critical for neural circuit formation and plasticity. Notably, many human-specific sequence changes are located in the human-specific TAD boundaries and loop anchors, which may lead to the formation of new transcription factor binding sites and chromatin structures in human. Collectively, the presented data highlight the value of comparative 3D genome analyses in dissecting the regulatory mechanisms of brain development and evolution.

2020-12-15 | GSE163177 | GEO

Transcriptome map of the human brain at the single-cell resolution

Project description:The human brain is about three times larger than the brain of our closest relatives, chimpanzees and bonobos. However, increased size alone fails to explain cognitive abilities unique to humans. Functional changes acquired in the human lineage are likely mediated by divergent gene expression and cell composition in brain regions. Here we generated a map of the human brain transcriptome by assessing the gene expression levels in 33 distinct regions representing all major brain structures from four adult cognitively healthy human individuals, three chimpanzees, three bonobos, and three rhesus macaques. We further conducted single-nuclei RNA-sequencing (SN-seq) experiment in three of the 33 brain regions in four species: two regions showing excess of the human-specific differences, cingulate anterior cortex and cerebellar gray matter, as well as one region showing no such excess, caudate nucleus. We determined cell type specificity of human-specific differences observed in the bulk tissue analysis, and identified species-specific expression differences directly using SN-seq data. This data resource forms a comprehensive baseline for studies of normal and abnormal human brain function and evolution.

2020-01-30 | GSE127898 | GEO

Transcriptome map of the human brain at the single-cell resolution

2020-01-30 | GSE127774 | GEO

Evolution of human-specific microRNA miR-941 [cerebellum gene expression]

Project description:miRNA-mediated gene expression silencing has previously been shown to be important for a variety of physiological and pathological processes. Here, we have explored the role of one bona fide human-specific miRNA (miR-941) in evolution of the human-specific expression and function. Using combination of high-throughput sequencing (GSE26545), miRNA transfection and large-scale PCR of various human populations, we have shown that emergence and rapid expansion of miR-941 might take place on the human evolutionary linage between six and one million years ago. Functionally, miR-941 could be associated with hedgehog and insulin signaling pathways, and thus might potentially play a role in evolution of human longevity. Human-specific effects of miR-941 regulation are detectable in human brain and affect genes involved in neurotransmitter signaling. Furthermore, emergence of miR-941 on the human evolutionary linage was accompanied by the accelerated loss of its binding sites. Taken together, these results strongly implicate the contribution of miR-941 in evolution of the human-specific phenotype. Cerebellum mRNA samples from 5 human, 5 chimpanzee and 1 rhesus macaque for Affymetrix Human Exon 1.0 ST Arrays were prepared following the standard GeneChip Whole Transcript (WT) Sense Target Labelling Assay.

2012-12-20 | E-GEOD-35619 | biostudies-arrayexpress

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