Dorsal Striatum Transcriptome Profile Profound Shift in Repeated Aggression Mouse Model Converged to Networks of 12 Transcription Factors after Fighting Deprivation
<p>Timescale of experiments. A20—mice with 20 days of consecutive wins in daily agonistic interactions; AD—A20 mice after subsequent 14 days of fight deprivation; Control—mice without agonistic interactions.</p> "> Figure 2
<p>PCA biplot outlines distinct alteration of TF programs (3 DEG clusters) between AD (blue), A20 (red) and control (green) groups. Green shaded area is control group.</p> "> Figure 3
<p>GO annotation of 12 TFs split into three corresponding clusters (<b>A</b>–<b>C</b>) (<a href="#genes-13-00021-f002" class="html-fig">Figure 2</a>). Overall PPI enrichment <span class="html-italic">p</span>-value (7 edges vs. 1 exp): 5.23 × 10<sup>−6</sup>. Green shaded area (<b>A</b>) is a control-group-associated cluster (<a href="#genes-13-00021-f002" class="html-fig">Figure 2</a>). Color coding: yellow—KW-0010: activator, 7 genes; FDR < 2.4 × 10<sup>−6</sup>; red—central nervous system projection neuron axonogenesis; 2 genes; FDR < 0.03; pink—GO:0035257; nuclear hormone receptor binding; 3 genes; FDR < 0.015; blue—GO:0071376 cellular response to corticotropin-releasing hormone stimulus; 2 genes; FDR < 0.0024; green—behavioral abnormalities of Zic1 and Zic2 mutant mice; PMID: 11699604. The image was created with the string-db.org service.</p> "> Figure 4
<p>Eleven connected co-varied genes spanning 5 DEGs (<span class="html-italic">Egr1</span>, <span class="html-italic">Etv5</span>, <span class="html-italic">Fosl2</span>, <span class="html-italic">Nr4a1</span>, <span class="html-italic">Nr4a2</span>) presented in <a href="#genes-13-00021-f003" class="html-fig">Figure 3</a>A. GO color coding corresponds to the plot above (gene numbers attached to bars). The DEGs in this set feature control group and are decreased in AD and A20 groups (<a href="#genes-13-00021-f002" class="html-fig">Figure 2</a>).</p> "> Figure 5
<p>Eight circadian rhythm genes subset expanded from <span class="html-italic">Arntl</span> DEG and annotated by string-db suite (<a href="#genes-13-00021-f003" class="html-fig">Figure 3</a>A).</p> "> Figure 6
<p>Circadian rhythm TF set (8 genes; <a href="#genes-13-00021-f005" class="html-fig">Figure 5</a>) PCA biplot featuring a control-group-associated <span class="html-italic">Arntl</span> DEG (<a href="#genes-13-00021-f003" class="html-fig">Figure 3</a>A) along with experimentally confirmed (string-db) connected genes <span class="html-italic">Npas2, Clock</span> (green shaded area) that are attenuated in affected species due to repressive action of cAMP-associated <span class="html-italic">Per1</span> expression in aggressive mice. <span class="html-italic">H0:</span> random distribution of species across plot’s 2 halves: <span class="html-italic">p</span> < 0.0024; binomial test. Each gene statistically significantly correlates with at least 2 other genes (<span class="html-italic">p</span> < 0.05) except for <span class="html-italic">Clock</span> (<a href="#genes-13-00021-t002" class="html-table">Table 2</a>). Curved arrow depicts group-related sequential gene expression dynamics cycle: C->A20->AD->C. Underlined gene names indicate DEGs in any of the 3-way comparisons. Enlarged underlined genes feature differential expression in 2 comparisons: <span class="html-italic">Arntl</span> (C_AD, C_A20)<span class="html-italic">; Per2</span> (AD_A20, C_A20).</p> "> Figure 7
<p>Twenty-seven genes recovered by string-db.org as Zic1/2-associated TF network and associated with AD subgroup (<a href="#genes-13-00021-f002" class="html-fig">Figure 2</a> and <a href="#genes-13-00021-f003" class="html-fig">Figure 3</a>B). <span class="html-italic">Armadillo</span> (<span class="html-italic">Ctnnb1)</span> gene (catenin β 1) is the most connected gene in the center. GO color coding is assigned as in histogram plot above (number of genes is attached as bar labels therein).</p> "> Figure 8
<p>PCA plot of 27 genes from <a href="#genes-13-00021-f007" class="html-fig">Figure 7</a> gene network of AD-specific <span class="html-italic">Wnt</span>-associated (<span class="html-italic">Ctnnb1</span>, <span class="html-italic">Prkcd</span>, <span class="html-italic">Fzd8</span>, <span class="html-italic">Fzd9</span>; [<a href="#B31-genes-13-00021" class="html-bibr">31</a>]) TF program; see also <a href="#genes-13-00021-f002" class="html-fig">Figure 2</a> and <a href="#genes-13-00021-f003" class="html-fig">Figure 3</a>. Bold underlined gene names indicate 9 DEGs within this network.</p> "> Figure 9
<p>Neighborhood recovery of <span class="html-italic">Zeb2</span> neighborhood inferred by string-db.org resource (11 genes) implies “repression of transcription” GO function of genes set. All but one (<span class="html-italic">Arhgap</span>) genes are transcriptional repressors; 8 genes belong to nucleus compartment (TFs); 4 genes (<span class="html-italic">Cdh1</span>, <span class="html-italic">Cdh2</span>, <span class="html-italic">Ctbp1</span>, <span class="html-italic">Ctbp2</span>) are associated with glutamatergic synapse.</p> "> Figure 10
<p>Total of 1009 DEGs across AD and A20 groups. A20 group maintained around 170 increased DEGs, while 839 DEGs featured attenuated expression in the A20 DS.</p> "> Figure 11
<p>(<b>a</b>) “Semaphorin-plexin signaling” GO DEG set (4 genes); <span class="html-italic">H0:</span> random distribution of samples across 2 plot halves, <span class="html-italic">p</span>-value < 0.00065 (binomial test); (<b>b</b>) JAK/STAT gene projection inferred from string-db.org seeded by <span class="html-italic">Jak2, Irs1</span> DEGs; <span class="html-italic">H0:</span> random distribution of samples across 2 plot halves, <span class="html-italic">p</span>-value < 0.0045 (binomial test). Underlined gene names signify DEGs. Encircled is A20 group.</p> "> Figure 12
<p>RNA-binding DEG subcluster within 149 cAMP-mediated positive A20 DEG cluster (<a href="#genes-13-00021-f010" class="html-fig">Figure 10</a>). <span class="html-italic">Drd1</span> included, underlining significant correlation with these DEGs. <span class="html-italic">Per2, Rbm15</span> are known transcriptional repressors (see the text). <span class="html-italic">H0:</span> random distribution of samples across 2 plot halves, <span class="html-italic">p</span>-value < 0.0045 (binomial test). Underlined gene names signify DEGs.</p> "> Figure 13
<p>PCA plot based on 33 specific cAMP-mediated balanced gene subset compiled in (Babenko et al., 2020) featuring A20 and AD groups. Marker gene set is shown in bold. Blue-shaded arrow signifies dopamine vs. glutamate uptake gradient. Yellow-shaded arrow signifies D1 passive/active states phasing [<a href="#B11-genes-13-00021" class="html-bibr">11</a>]. Blue-shaded oval underlines opioid synthesis (<span class="html-italic">Penk, Pdyn). H0:</span> random distribution of 5-fold AD sample with only 1 alien species in a plot; left half is <span class="html-italic">p</span>-value < 0.016 (binomial distribution). Blue dots are AD samples; dark blue dots are aggressive samples. Underlined gene names indicate DEGs.</p> "> Figure 14
<p>FPKM values of 5 dopamine- and opioid-specific genes across 18 samples.</p> "> Figure 15
<p>Flowchart of DEG inferred events from aggressive to control groups.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Experimental Procedures
Modeling Repeated Aggression in Male Mice
2.3. RNA-Seq Data Collection and Processing
2.4. Statistical Analysis
3. Results
3.1. Detecting DEGs in Three Pairwise Comparisons
3.2. C_AD Comparison
3.2.1. Expansion of TF Clusters by Co-Variation Analysis
3.2.2. Control Six-TF DEGs Assessment
3.2.3. Circadian Rhythm DEG Analysis
3.2.4. Cluster Two Expansion
3.2.5. Third Cluster Featuring Joint A20/AD Species
3.3. A20 vs. AD Comparison
3.3.1. Differentially Expressed Genes between Groups
3.3.2. Elaborating on A20-Associated Positive DEG Cluster
3.3.3. Dopamine-Mediated cAMP Signaling Cascade Balanced Gene Projection in A20 vs. AD Comparison
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
DEGs | differentially expressed genes |
FPKM | fragments per kilobase of transcript per million mapped reads |
GO | Gene Ontology |
KEGG | Kyoto Encyclopedia of Genes and Genomes Pathway Database |
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Number of DEGs (FDR < 0.05) | Number of Non-Zero Expressed Gene Pairs | |
---|---|---|
Control vs. A20 | 1030 | 24,321 |
Control vs. AD | 62 | 23,924 |
A20 vs. AD | 1009 | 23,763 |
Variables | Nr1d1 | Cry2 | Per1 | Npas2 | Arntl | Cry1 | Clock | Per2 |
---|---|---|---|---|---|---|---|---|
Nr1d1 | 1 | 0.603 | 0.312 | −0.247 | −0.620 | −0.288 | −0.305 | 0.025 |
Cry2 | 0.603 | 1 | 0.656 | −0.087 | −0.392 | 0.179 | −0.138 | 0.447 |
Per1 | 0.312 | 0.656 | 1 | −0.226 | −0.474 | 0.297 | 0.126 | 0.669 |
Npas2 | −0.247 | −0.087 | −0.226 | 1 | 0.552 | 0.510 | 0.223 | 0.065 |
Arntl | −0.620 | −0.392 | −0.474 | 0.552 | 1 | 0.325 | 0.369 | −0.067 |
Cry1 | −0.288 | 0.179 | 0.297 | 0.510 | 0.325 | 1 | 0.323 | 0.786 |
Clock | −0.305 | −0.138 | 0.126 | 0.223 | 0.369 | 0.323 | 1 | 0.274 |
Per2 | 0.025 | 0.447 | 0.669 | 0.065 | –0.067 | 0.786 | 0.274 | 1 |
Family | Min (q_Value) | Max (q_Value) | Stddev (q_Value) | # DEGs per Family |
---|---|---|---|---|
Slc | 1.35 × 10−3 | 3.63 × 10−2 | 1.05 × 10−2 | 29 |
Kcn | 1.35 × 10−3 | 4.92 × 10−2 | 1.31 × 10−2 | 22 |
Tme | 1.35 × 10−3 | 4.88 × 10−2 | 1.50 × 10−2 | 17 |
Zfp | 1.35 × 10−3 | 4.97 × 10−2 | 1.38 × 10−2 | 15 |
Col | 1.35 × 10−3 | 4.39 × 10−2 | 1.28 × 10−2 | 10 |
Arh | 1.35 × 10−3 | 4.88 × 10−2 | 1.66 × 10−2 | 8 |
Ptp | 1.35 × 10−3 | 2.59 × 10−2 | 1.04 × 10−2 | 7 |
Map | 1.35 × 10−3 | 2.31 × 10−2 | 7.40 × 10−3 | 7 |
Gpr | 1.35 × 10−3 | 2.10 × 10−2 | 7.21 × 10−3 | 7 |
Kif | 1.35 × 10−3 | 2.24 × 10−2 | 7.86 × 10−3 | 6 |
Cac | 1.35 × 10−3 | 4.56 × 10−2 | 1.89 × 10−2 | 6 |
Tri | 1.35 × 10−3 | 3.10 × 10−2 | 1.30 × 10−2 | 6 |
Ank | 1.35 × 10−3 | 4.56 × 10−2 | 1.51 × 10−2 | 6 |
Fam | 1.35 × 10−3 | 1.37 × 10−2 | 4.58 × 10−3 | 6 |
Cdk | 1.35 × 10−3 | 4.45 × 10−2 | 1.72 × 10−2 | 5 |
Rgs | 1.35 × 10−3 | 4.67 × 10−2 | 1.57 × 10−2 | 5 |
Prr | 1.35 × 10−3 | 3.76 × 10−2 | 1.38 × 10−2 | 5 |
Aka | 1.35 × 10−3 | 2.51 × 10−2 | 9.33 × 10−3 | 5 |
Ple | 1.35 × 10−3 | 4.78 × 10−2 | 1.94 × 10−2 | 5 |
Cep | 1.35 × 10−3 | 4.63 × 10−3 | 1.28 × 10−3 | 5 |
Adc | 1.35 × 10−3 | 4.63 × 10−3 | 1.39 × 10−3 | 5 |
Doc | 1.35 × 10−3 | 9.39 × 10−3 | 3.13 × 10−3 | 5 |
Variables | Darpp-32 | Penk | Drd2 | Drd1 | Pdyn |
---|---|---|---|---|---|
Darpp-32 | 1 | 0.858 | 0.914 | 0.863 | 0.723 |
Penk | 0.858 | 1 | 0.925 | 0.838 | 0.867 |
Drd2 | 0.914 | 0.925 | 1 | 0.886 | 0.777 |
Drd1 | 0.863 | 0.838 | 0.886 | 1 | 0.717 |
Pdyn | 0.723 | 0.867 | 0.777 | 0.717 | 1 |
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Babenko, V.; Redina, O.; Smagin, D.; Kovalenko, I.; Galyamina, A.; Babenko, R.; Kudryavtseva, N. Dorsal Striatum Transcriptome Profile Profound Shift in Repeated Aggression Mouse Model Converged to Networks of 12 Transcription Factors after Fighting Deprivation. Genes 2022, 13, 21. https://doi.org/10.3390/genes13010021
Babenko V, Redina O, Smagin D, Kovalenko I, Galyamina A, Babenko R, Kudryavtseva N. Dorsal Striatum Transcriptome Profile Profound Shift in Repeated Aggression Mouse Model Converged to Networks of 12 Transcription Factors after Fighting Deprivation. Genes. 2022; 13(1):21. https://doi.org/10.3390/genes13010021
Chicago/Turabian StyleBabenko, Vladimir, Olga Redina, Dmitry Smagin, Irina Kovalenko, Anna Galyamina, Roman Babenko, and Natalia Kudryavtseva. 2022. "Dorsal Striatum Transcriptome Profile Profound Shift in Repeated Aggression Mouse Model Converged to Networks of 12 Transcription Factors after Fighting Deprivation" Genes 13, no. 1: 21. https://doi.org/10.3390/genes13010021