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Advances of Brain Transcriptomics

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A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Neurogenomics".

Deadline for manuscript submissions: closed (20 July 2022) | Viewed by 22182

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Dr. Vladimir Babenko

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Guest Editor

Institute of Cytology and Genetics, 630090 Novosibirsk, Russia
Interests: brain transcriptiomics; alternative splicing; evolution of exon–intron structure; population genomics; next generation sequencing (NGS) methodologies
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Dr. Olga Redina

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Guest Editor

Institute of Cytology and Genetics, 630090 Novosibirsk, Russia
Interests: RNA-Seq; brain transcriptomics; hypertension animal models; stress induced arterial hypertension; qTLs (quantitative trait loci); molecular mechanisms of hypertension; behavior
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Advancements in RNA-Seq technology in the last decade have underlined its power for elucidating the brain gene networks responsible for various stressful factors, as well as pathologies like Alzheimer and Parkinson, and other neurological diseases including schizophrenia and depressive disorders. Single cell RNA-seq (scRNA-seq) allows for ascertaining various neurons and glia cell identities by elucidating the specific marker genes within them. This technology underlinees multiple novel stable cell colonies in the course of scRNA-seq analysis. Associative networks between cell colonies have been provided over the course of cells’ maturation, rendering an exhaustive picture of cell population development dynamics.

As a separate relevant issue, RNA-Seq provides the basis for cell/tissue specific alternative splicing (AS) elucidation with a high resolution. As it is known, the brain maintains the most expanded AS-mediated proteome variability, as well as AS-mediated transcription regulation, via nonsense mediated decay. The research of Barres Lab reported a 10-fold expansion of transcript diversity analyzing mouse brain transcriptomes (Yan et al., 2015). Currently, it is reported that the AS-specific profile is more specific and robust in certain instances than gene expression for neuronal identity (Ha et al., 2021). Multiple databases like ASCOT and Genome (for elucidating the tissue/cell specific AS profiles for each gene) are arising, underlining the research of brain transcriptome structural and expression variability as a top priority.

Additionally, there is a genetic based vs. acquired trait paradigm, which would be represented by both genetic studies based on animal model strains/breeds (e.g., tame foxes, aggressive strains of rats, etc.), and those that acquired the trait within single generation upon administering certain stress-related protocols.

In this Issue, we hope to address the spectra of physiological studies, including, but not limited to, animal models of social stress response and various brain disease related data/models using the abovementioned approaches and methods.

Dr. Vladimir Babenko
Dr. Olga Redina
Guest Editors

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Keywords

Brain transcriptome
Alternative splicing
Molecular basis of neurological diseases
Variability of brain proteome and plasticity
Brain disease marker genes/networks
Genetic basis of behavior
Marker gene networks in various brain regions based on RNA-Seq

Published Papers (11 papers)

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Editorial

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3 pages, 169 KiB

Open AccessEditorial

Advances of Brain Transcriptomics

by Olga E. Redina and Vladimir N. Babenko

Genes 2022, 13(10), 1831; https://0-doi-org.brum.beds.ac.uk/10.3390/genes13101831 - 11 Oct 2022

Cited by 2 | Viewed by 1089

Abstract

Advancements in RNA sequencing technology in past decade have underlined its power for elucidating the brain gene networks responsible for various stressful factors, as well as the pathologies associated with both genetically determined neurodegenerative diseases and those acquired during the lifespan [...] Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

Research

Jump to: Editorial

22 pages, 3418 KiB

Open AccessArticle

Identification of Hypothalamic Long Noncoding RNAs Associated with Hypertension and the Behavior/Neurological Phenotype of Hypertensive ISIAH Rats

by Larisa A. Fedoseeva, Nikita I. Ershov, Ivan A. Sidorenko, Arcady L. Markel and Olga E. Redina

Genes 2022, 13(9), 1598; https://0-doi-org.brum.beds.ac.uk/10.3390/genes13091598 - 07 Sep 2022

Cited by 2 | Viewed by 1284

Abstract

Long noncoding RNAs (lncRNAs) play an important role in the control of many physiological and pathophysiological processes, including the development of hypertension and other cardiovascular diseases. Nonetheless, the understanding of the regulatory function of many lncRNAs is still incomplete. This work is a continuation of our earlier study on the sequencing of hypothalamic transcriptomes of hypertensive ISIAH rats and control normotensive WAG rats. It aims to identify lncRNAs that may be involved in the formation of the hypertensive state and the associated behavioral features of ISIAH rats. Interstrain differences in the expression of seven lncRNAs were validated by quantitative PCR. Differential hypothalamic expression of lncRNAs LOC100910237 and RGD1562890 between hypertensive and normotensive rats was shown for the first time. Expression of four lncRNAs (Snhg4, LOC100910237, RGD1562890, and Tnxa-ps1) correlated with transcription levels of many hypothalamic genes differentially expressed between ISIAH and WAG rats (DEGs), including genes associated with the behavior/neurological phenotype and hypertension. After functional annotation of these DEGs, it was concluded that lncRNAs Snhg4, LOC100910237, RGD1562890, and Tnxa-ps1 may be involved in the hypothalamic processes related to immune-system functioning and in the response to various exogenous and endogenous factors, including hormonal stimuli. Based on the functional enrichment analysis of the networks, an association of lncRNAs LOC100910237 and Tnxa-ps1 with retinol metabolism and an association of lncRNAs RGD1562890 and Tnxa-ps1 with type 1 diabetes mellitus are proposed for the first time. Based on a discussion, it is hypothesized that previously functionally uncharacterized lncRNA LOC100910237 is implicated in the regulation of hypothalamic processes associated with dopaminergic synaptic signaling, which may contribute to the formation of the behavioral/neurological phenotype and hypertensive state of ISIAH rats. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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12 pages, 18545 KiB

Open AccessArticle

Transcriptome Profile of a New Mouse Model of Spinocerebellar Ataxia Type 14 Implies Changes in Cerebellar Development

by Szilvia E. Mezey, Josef P. Kapfhammer and Etsuko Shimobayashi

Genes 2022, 13(8), 1417; https://0-doi-org.brum.beds.ac.uk/10.3390/genes13081417 - 09 Aug 2022

Cited by 2 | Viewed by 1854

Abstract

The autosomal dominant inherited spinocerebellar ataxias (SCAs) are a group of neurodegenerative disorders characterized by cerebellar atrophy and loss of Purkinje neurons. Spinocerebellar ataxia type 14 (SCA14) is a rare variant of SCAs caused by missense mutations or deletions in the PRKCG gene encoding the protein kinase C γ (PKCγ). Although mutated PKCγs are responsible for SCA14, it is still unclear exactly how mutated PKCγs are involved in SCA14 pathogenesis. Therefore, it is important to study how PKCγ signaling is altered in the cerebellum, which genes or signaling pathways are affected, and how this leads to neurological disease. In this study, we used a mouse line carrying a knock-in pseudo-substrate domain mutation in PKCγ (PKCγ-A24E) as an SCA14 model and performed RNA sequencing (RNA-seq) analysis at an early developmental timepoint (postnatal day 15) to investigate changes in the gene profile compared to wildtype mice. We analyzed both heterozygous (Het) PKCγ-A24E mice and homozygous (Homo) PKCγ-A24E mice for transcriptomic changes. The Het PKCγ-A24E mice reflects the situation observed in human SCA14 patient, while Homo PKCγ-A24E mice display stronger phenotypes with respect to Purkinje cell development and behavior. Our findings highlight an abundance of modifications affecting genes involved in developmental processes, suggesting that at least a part of the final phenotype is shaped by altered cerebellar development and is not only caused by changes in mature animals. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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20 pages, 1052 KiB

Open AccessArticle

Prefrontal Cortex Response to Prenatal Insult and Postnatal Opioid Exposure

by Haley E. Rymut, Laurie A. Rund, Bruce R. Southey, Rodney W. Johnson, Jonathan V. Sweedler and Sandra L. Rodriguez-Zas

Genes 2022, 13(8), 1371; https://0-doi-org.brum.beds.ac.uk/10.3390/genes13081371 - 30 Jul 2022

Cited by 3 | Viewed by 1752

Abstract

The influence of proinflammatory challenges, such as maternal immune activation (MIA) or postnatal exposure to drugs of abuse, on brain molecular pathways has been reported. On the other hand, the simultaneous effects of MIA and drugs of abuse have been less studied and sometimes offered inconsistent results. The effects of morphine exposure on a pig model of viral-elicited MIA were characterized in the prefrontal cortex of males and females using RNA-sequencing and gene network analysis. Interacting and main effects of morphine, MIA, and sex were detected in approximately 2000 genes (false discovery rate-adjusted p-value < 0.05). Among the enriched molecular categories (false discovery rate-adjusted p-value < 0.05 and −1.5 > normalized enrichment score > 1.5) were the cell adhesion molecule pathways associated with inflammation and neuronal development and the long-term depression pathway associated with synaptic strength. Gene networks that integrate gene connectivity and expression profiles displayed the impact of morphine-by-MIA interaction effects on the pathways. The cell adhesion molecules and long-term depression networks presented an antagonistic effect between morphine and MIA. The differential expression between the double-challenged group and the baseline saline-treated Controls was less extreme than the individual challenges. The previous findings advance the knowledge about the effects of prenatal MIA and postnatal morphine exposure on the prefrontal cortex pathways. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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18 pages, 7512 KiB

Open AccessArticle

Transcriptome Analysis Identifies Key Metabolic Changes in the Brain of Takifugu rubripes in Response to Chronic Hypoxia

by Fengqin Shang, Yun Lu, Yan Li, Bing Han, Renjie Wei, Shengmei Liu, Ying Liu, Yang Liu and Xiuli Wang

Genes 2022, 13(8), 1347; https://0-doi-org.brum.beds.ac.uk/10.3390/genes13081347 - 27 Jul 2022

Cited by 10 | Viewed by 1928

Abstract

The brain is considered to be an extremely sensitive tissue to hypoxia, and the brain of fish plays an important role in regulating growth and adapting to environmental changes. As an important aquatic organism in northern China, the economic yield of Takifugu rubripes is deeply influenced by the oxygen content of seawater. In this regard, we performed RNA-seq analysis of T. rubripes brains under hypoxia and normoxia to reveal the expression patterns of genes involved in the hypoxic response and their enrichment of metabolic pathways. Studies have shown that carbohydrate, lipid and amino acid metabolism are significant pathways for the enrichment of differentially expressed genes (DEGs) and that DEGs are significantly upregulated in those pathways. In addition, some biological processes such as the immune system and signal transduction, where enrichment is not significant but important, are also discussed. Interestingly, the DEGs associated with those pathways were significantly downregulated or inhibited. The present study reveals the mechanism of hypoxia tolerance in T. rubripes at the transcriptional level and provides a useful resource for studying the energy metabolism mechanism of hypoxia response in this species. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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17 pages, 1639 KiB

Open AccessArticle

Terpenoid Backbone Biosynthesis among Pig Hippocampal Pathways Impacted by Stressors

by Haley E. Rymut, Laurie A. Rund, Bruce R. Southey, Rodney W. Johnson and Sandra L. Rodriguez-Zas

Genes 2022, 13(5), 814; https://0-doi-org.brum.beds.ac.uk/10.3390/genes13050814 - 02 May 2022

Cited by 8 | Viewed by 2098

Abstract

Neurogenomic changes induced by maternal immune activation (MIA) during gestation and the social stress of weaning can alter brain plasticity in the hippocampus of offspring. The present study furthers the understanding of how these stressors impact hippocampus gene networks. The hippocampus transcriptome was profiled in pigs that were either exposed to MIA or not and were weaned or nursed. Overall, 1576 genes were differentially expressed (FDR-adjusted p-value < 0.05 and |log2 (fold change between pig groups)| > 1.2) in response to the main and interacting effects of MIA, weaning, and sex. Functional analysis identified 17 enriched immunological and neurological pathways in the Kyoto Encyclopedia of Genes and Genomes database. The enrichment of the terpenoid backbone biosynthesis pathway was characterized by genes under-expressed in MIA relative to non-MIA exposed, males relative to females, and weaned relative to nursed pigs. On the other hand, the enrichment of drug addiction pathways was characterized by gene over-expression in MIA relative to non-exposed pigs. Our results indicate that weaning and sex can modify the effects of MIA on the offspring hippocampus. This knowledge can aid in precise identification of molecular targets to reduce the prolonged effects of pre- and postnatal stressors. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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24 pages, 10113 KiB

Open AccessArticle

Dorsal Striatum Transcriptome Profile Profound Shift in Repeated Aggression Mouse Model Converged to Networks of 12 Transcription Factors after Fighting Deprivation

by Vladimir Babenko, Olga Redina, Dmitry Smagin, Irina Kovalenko, Anna Galyamina, Roman Babenko and Natalia Kudryavtseva

Genes 2022, 13(1), 21; https://0-doi-org.brum.beds.ac.uk/10.3390/genes13010021 - 22 Dec 2021

Cited by 5 | Viewed by 2470

Abstract

Both aggressive and aggression-deprived (AD) species represent pathologic cases intensely addressed in psychiatry and substance abuse disciplines. Previously, we reported that AD mice displayed a higher aggressive behavior score than the aggressive group, implying the manifestation of a withdrawal effect. We employed an animal model of chronic social conflicts, curated in our lab for more than 30 years. In the study, we pursued the task of evaluating key events in the dorsal striatum transcriptome of aggression experienced mice and AD species compared to controls using RNA-Seq profiling. Aggressive species were subjected to repeated social conflict encounters (fights) with regular positive (winners) experience in the course of 20 consecutive days (A20 group). This led to a profoundly shifted transcriptome expression profile relative to the control group, outlined by more than 1000 differentially expressed genes (DEGs). RNA-Seq cluster analysis revealed that elevated cyclic AMP (cAMP) signaling cascade and associated genes comprising 170 differentially expressed genes (DEGs) in aggressive (A20) species were accompanied by a downturn in the majority of other metabolic/signaling gene networks (839 DEGs) via the activation of transcriptional repressor DEGs. Fourteen days of a consecutive fighting deprivation period (AD group) featured the basic restoration of the normal (control) transcriptome expression profile yielding only 62 DEGs against the control. Notably, we observed a network of 12 coordinated DEG Transcription Factor (TF) activators from 62 DEGs in total that were distinctly altered in AD compared to control group, underlining the distinct transcription programs featuring AD group, partly retained from the aggressive encounters and not restored to normal in 14 days. We found circadian clock TFs among them, reported previously as a withdrawal effect factor. We conclude that the aggressive phenotype selection with positive reward effect (winning) manifests an addiction model featuring a distinct opioid-related withdrawal effect in AD group. Along with reporting profound transcriptome alteration in A20 group and gaining some insight on its specifics, we outline specific TF activator gene networks associated with transcriptional repression in affected species compared to controls, outlining Nr1d1 as a primary candidate, thus offering putative therapeutic targets in opioid-induced withdrawal treatment. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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8 pages, 657 KiB

Open AccessCommunication

Differential Analysis of A-to-I mRNA Edited Sites in Parkinson’s Disease

by Denis V. Pozdyshev, Anastasia A. Zharikova, Maria V. Medvedeva and Vladimir I. Muronetz

Genes 2022, 13(1), 14; https://0-doi-org.brum.beds.ac.uk/10.3390/genes13010014 - 22 Dec 2021

Cited by 7 | Viewed by 2812

Abstract

Parkinson’s disease (PD) is a widespread neuronal degenerative disorder with unexplored etiology. It is associated with various pathological events. In particular, the prefrontal cortex Brodmann area 9 (BA9) region is affected in PD. This frontal lobe brain region plays an important role in cognitive, motor, and memory-related functions. BA9 develops Lewy bodies in PD patients and shows essential changes in transcriptome and proteome, connected with mitochondria related pathways, protein folding pathways, and metallothioneins. Recently, altered adenosine to inosine mRNA editing patterns have been detected in various neurological pathologies. In this article, we present an investigation of differences in A-to-I RNA editing levels and specificity of mRNA editing sites in brain tissues of healthy and PD patients based on RNA sequencing data. Overall, decreased editing levels in the brains of PD patients were observed, potential editing sites with altered editing during PD were identified, and the role of different adenosine deaminases in this process was analyzed. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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12 pages, 945 KiB

Open AccessArticle

Gene Regulation Analysis Reveals Perturbations of Autism Spectrum Disorder during Neural System Development

by Dan Li, Joshua Xu and Mary Qu Yang

Genes 2021, 12(12), 1901; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12121901 - 27 Nov 2021

Cited by 4 | Viewed by 2124

Abstract

Autism spectrum disorder (ASD) is a neurodevelopmental disorder that impedes patients’ cognition, social, speech and communication skills. ASD is highly heterogeneous with a variety of etiologies and clinical manifestations. The prevalence rate of ASD increased steadily in recent years. Presently, molecular mechanisms underlying ASD occurrence and development remain to be elucidated. Here, we integrated multi-layer genomics data to investigate the transcriptome and pathway dysregulations in ASD development. The RNA sequencing (RNA-seq) expression profiles of induced pluripotent stem cells (iPSCs), neural progenitor cells (NPCs) and neuron cells from ASD and normal samples were compared in our study. We found that substantially more genes were differentially expressed in the NPCs than the iPSCs. Consistently, gene set variation analysis revealed that the activity of the known ASD pathways in NPCs and neural cells were significantly different from the iPSCs, suggesting that ASD occurred at the early stage of neural system development. We further constructed comprehensive brain- and neural-specific regulatory networks by incorporating transcription factor (TF) and gene interactions with long 5 non-coding RNA(lncRNA) and protein interactions. We then overlaid the transcriptomes of different cell types on the regulatory networks to infer the regulatory cascades. The variations of the regulatory cascades between ASD and normal samples uncovered a set of novel disease-associated genes and gene interactions, particularly highlighting the functional roles of ELF3 and the interaction between STAT1 and lncRNA ELF3-AS 1 in the disease development. These new findings extend our understanding of ASD and offer putative new therapeutic targets for further studies. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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18 pages, 1240 KiB

Open AccessArticle

Correlation of Expression Changes between Genes Controlling 5-HT Synthesis and Genes Crh and Trh in the Midbrain Raphe Nuclei of Chronically Aggressive and Defeated Male Mice

by Olga E. Redina, Vladimir N. Babenko, Dmitry A. Smagin, Irina L. Kovalenko, Anna G. Galyamina and Natalia N. Kudryavtseva

Genes 2021, 12(11), 1811; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12111811 - 18 Nov 2021

Cited by 5 | Viewed by 1658

Abstract

Midbrain raphe nuclei (MRNs) contain a large number of serotonergic neurons associated with the regulation of numerous types of psychoemotional states and physiological processes. The aim of this work was to study alterations of the MRN transcriptome in mice with prolonged positive or negative fighting experience and to identify key gene networks associated with the regulation of serotonergic system functioning. Numerous genes underwent alterations of transcription in the MRNs of male mice that either manifested aggression or experienced social defeat in daily agonistic interactions. The expression of the Tph2 gene encoding the rate-limiting enzyme of the serotonin synthesis pathway correlated with the expression of many genes, 31 of which were common between aggressive and defeated mice and were downregulated in the MRNs of mice of both experimental groups. Among these common differentially expressed genes (DEGs), there were genes associated with behavior, learning, memory, and synaptic signaling. These results suggested that, in the MRNs of the mice, the transcriptome changes associated with serotonergic regulation of various processes are similar between the two groups (aggressive and defeated). In the MRNs, more DEGs correlating with Tph2 expression were found in defeated mice than in the winners, which is probably a consequence of deeper Tph2 downregulation in the losers. It was shown for the first time that, in both groups of experimental mice, the changes in the transcription of genes controlling the synthesis and transport of serotonin directly correlate with the expression of genes Crh and Trh, which control the synthesis of corticotrophin- and thyrotropin-releasing hormones. Our findings indicate that CRH and TRH locally produced in MRNs are related to serotonergic regulation of brain processes during a chronic social conflict. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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16 pages, 2931 KiB

Open AccessArticle

Reduced Expression of Slc Genes in the VTA and NAcc of Male Mice with Positive Fighting Experience

by Dmitry A. Smagin, Vladimir N. Babenko, Olga E. Redina, Irina L. Kovalenko, Anna G. Galyamina and Natalia N. Kudryavtseva

Genes 2021, 12(7), 1099; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12071099 - 20 Jul 2021

Cited by 4 | Viewed by 2141

Abstract

A range of several psychiatric medications targeting the activity of solute carrier (SLC) transporters have proved effective for treatment. Therefore, further research is needed to elucidate the expression profiles of the Slc genes, which may serve as markers of altered brain metabolic processes and neurotransmitter activities in psychoneurological disorders. We studied the Slc differentially expressed genes (DEGs) using transcriptomic profiles in the ventral tegmental area (VTA), nucleus accumbens (NAcc), and prefrontal cortex (PFC) of control and aggressive male mice with psychosis-like behavior induced by repeated experience of aggression accompanied with wins in daily agonistic interactions. The majority of the Slc DEGs were shown to have brain region-specific expression profiles. Most of these genes in the VTA and NAcc (12 of 17 and 25 of 26, respectively) were downregulated, which was not the case in the PFC (6 and 5, up- and downregulated, respectively). In the VTA and NAcc, altered expression was observed for the genes encoding the transporters of neurotransmitters as well as inorganic and organic ions, amino acids, metals, glucose, etc. This indicates an alteration in transport functions for many substrates, which can lead to the downregulation or even disruption of cellular and neurotransmitter processes in the VTA and NAcc, which are attributable to chronic stimulation of the reward systems induced by positive fighting experience. There is not a single Slc DEG common to all three brain regions. Our findings show that in male mice with repeated experience of aggression, altered activity of neurotransmitter systems leads to a restructuring of metabolic and neurotransmitter processes in a way specific for each brain region. We assume that the scoring of Slc DEGs by the largest instances of significant expression co-variation with other genes may outline a candidate for new prognostic drug targets. Thus, we propose that the Slc genes set may be treated as a sensitive genes marker scaffold in brain RNA-Seq studies. Full article

(This article belongs to the Special Issue Advances of Brain Transcriptomics)

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