Comparative Characterization of Immune Response in Sheep with Caseous Lymphadenitis through Analysis of the Whole Blood Transcriptome
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals and Sampling Procedure
2.2. RNA Isolation, Library Preparation, and Sequencing of the Transcriptome
2.3. Transcriptome Data Processing, Differential Expression Analysis, and Gene Ontology Classification
2.4. Reverse-Transcriptase Real-Time qPCR Validation
3. Results
3.1. Sequencing Quality Overview
3.2. Characterization of the Ovine Whole Blood Transcriptome
3.3. Functional Significance of Unique and Common DEGs
3.3.1. Unique Genes with the Highest DE
3.3.2. Common Genes with the Highest DE
3.4. Enrichment of Gene Ontology (GO) Terms and Pathways in the Investigated Ovine Groups
3.4.1. Cellular Localization of Differentially Expressed Genes
3.4.2. Influenced Biological Processes and Role of DEGs in the Host Immune Response
3.4.3. Differential Gene Expression in Biological Pathways Influenced by C. pseudotuberculosis
3.5. Validation of RNA-Seq Data by RT–qPCR
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Group | Trimmed Reads | Mapped Reads | Mapped Reads % | Total Paired Reads | Uniquely MR | Uniquely MR % | Transcripts | Genes |
---|---|---|---|---|---|---|---|---|
EP | 34,454,888 | 26,542,080 | 77.02 | 25,825,876 | 14,965,299 | 56.34 | 27,430 | 12,230 |
EN | 30,881,461 | 24,175,800 | 78.29 | 23,691,710 | 13,300,932 | 55.02 | 26,730 | 12,080 |
CN | 30,495,644 | 19,935,851 | 63.64 | 19,501,543 | 11,341,457 | 57.03 | 26,753 | 11,932 |
Gene Name | Gene Symbol | FC | padj |
---|---|---|---|
CNxEP | |||
Killer cell lectin-like receptor subfamily B member 1 | KLRB1 | 7.74 | 1.46 × 10−4 |
Kelch-like family memeber 18 | KLHL18 | 6.62 | 1.53 × 10−2 |
Chloride voltage-gated channel Ka | CLCNKA | 5.35 | 1.98 × 10−2 |
Immunoglobulin superfamily DCC subclass member 3 | IGDCC3 | 5.11 | 7.60 × 10−5 |
Protein glucosyl galactosyl hydroxylysine glucosidase | PGGHG | 4.64 | 3.25 × 10−3 |
Asporin | ASPN | −6.71 | 1.84 × 10−2 |
Secreted protein acidic and cysteine rich | SPARC | −4.36 | 4.60 × 10−5 |
Secreted phosphoprotein 1 | SPP1 | −4.32 | 4.62 × 10−5 |
Solute carrier family 7 member 11 | SLC7A11 | −3.21 | 2.24 × 10−2 |
Twist family bHLH transcription factor 1 | TWIST1 | −3.14 | 1.84 × 10−2 |
CNxEN | |||
Zinc finger protein 227 | LOC101109384 | 3.45 | 1.99 × 10−3 |
Ankyrin repeat domain 7 | ANKRD7 | 2.82 | 7.95 × 10−4 |
Crystallin gamma S | CRYGS | 2.62 | 4.84 × 10−2 |
Antigen WC1.1 | WC1.1 | 2.42 | 2.12 × 10−3 |
Tripartite motif-containing 45 | TRIM45 | 2.42 | 2.50 × 10−2 |
Proteoglycan 4 | PRG4 | −7.44 | 3.33 × 10−3 |
Secreted frizzled-related protein 1 | SFRP1 | −7.35 | 6.14 × 10−3 |
Tubulointerstitial nephritis antigen-like 1 | TINAGL1 | −4.53 | 4.98 × 10−5 |
Collagen type VI alpha 1 chain | COL6A1 | −4.06 | 3.62 × 10−2 |
Myeloperoxidase | MPO | −3.80 | 1.30 × 10−3 |
ENxEP | |||
Vascular cell adhesion protein 1 | VCAM1 | 7.50 | 2.68 × 10−2 |
Phospholipid phosphatase related 5 | PLPPR5 | 6.12 | 2.57 × 10−2 |
Group | EP | EN | |||
---|---|---|---|---|---|
Gene Name | Gene Symbol | FC | padj | FC | padj |
Same direction of expression | |||||
Hemicentin 1 | HMCN1 | 4.93 | 2.89 × 10−5 | 4.07 | 7.72 × 10−4 |
MHC class I polypeptide-related sequence B | MICB | 4.37 | 2.63 × 10−12 | 4.52 | 6.42 × 10−9 |
Lymphocyte antigen 6 family member G6C | LY6G6C | 3.77 | 1.30 × 10−4 | 4.08 | 7.84 × 10−6 |
Tyrosine protein phosphatase nonreceptor-type substrate 1 | PTPN1 | 3.59 | 4.17 × 10−3 | 3.91 | 6.92 × 10−3 |
Microfibril-associated protein 5 | MFAP5 | −9.26 | 8.45 × 10−6 | −6.63 | 9.73 × 10−4 |
Syndecan 2 | SDC2 | −8.35 | 3.52 × 10−4 | −5.72 | 1.00 × 10−2 |
Mesenteric estrogen-dependent adipogenesis | MEDAG | −7.34 | 2.83 × 10−4 | −8.93 | 1.36 × 10−4 |
Decorin | DCN | −6.76 | 1.39 × 10−4 | −5.51 | 2.31 × 10−3 |
Opposite direction of expression | |||||
Leukocyte immunoglobulin-like receptor subfamily A member 6 | LILRA6 | −1.72 | 9.82 × 10−4 | 3.08 | 8.59 × 10−6 |
GTPase IMAP family member 7 | GIMAP7 | −1.50 | 2.43 × 10−3 | 2.57 | 3.02 × 10−5 |
DEGs Ordered According to Their FC | Biological Processes | |
---|---|---|
EP | Upregulated | Downregulated |
KLRB1; DCN; IGDCC3; HMCN1; PRG3 | Antigen receptor-mediated SP | Humoral IR |
ADAMTS13; MICB; SPARC; SPP1; IL13 | B-cell receptor signaling pathway | Cytokine production |
LY6G6C; PTPN1; OLA-I; COL1A1; BTN2A2 | Response to other organisms | Calcium ion homeostasis |
GZMH; LAMB1; TNIP2; GATA6; SPIB | Adaptive IR somatic recomb. of IRCs built from Ig domains | Inflammatory response |
GIMAP8; NFKB2; C4BPA; GZMA; IBSP | Response to cytokine | Complement activation |
TNFRSF13C; SH2B2; PAX5; BLK; MT2A | Cell adhesion | |
CXCR6; JCHAIN; IFITM1; CXCL10; UBD | Lymphocyte activation | |
C3AR1; FCRL3; CDA; GHR; UBA7; CLECL1 | Innate IR | |
ADGRE3; CD1A; HSP90B1; LILRA6; OVAR | ||
BPI; ULBP1; CD1E; GIMAP7 | ||
EN | ||
PRG4; DCN; MICB; LY6G6C; HMCN1; PTPN1 | Positive regulation of NK cell-mediated cytotoxicity | Innate IR |
MPO; COL1A1; IL13; GZMB; GIMAP8 | Gamma-delta T-cell activation | Regulation of response to stress |
C4BPA; SERPINB4; BMPR1A; LAMB1 | I-kappaB kinase/NF-kappaB signaling | Regulation of protein metabolic process |
GIMAP1; LILRA6; DQB; CLEC4E; IL1RN | Response to stress | Apoptotic process |
GIMAP7; TRIM45; DNM1; GZMH; HMGB2 | Apoptotic process | Locomotion |
PRG3; SOX13; C3AR1; GZMA; ULBP2 | Calcium ion homeostasis | |
WC1.1; CCL14; DNM3; NLRP2; TNFSF10 | ||
GCA; KIR3DP1; LILRA5; BLK; UBD; PILRB | ||
SERPINB9; CD226; FCER1A; ADGRE1; OLA-I | ||
CLEC2D; TNFRSF25; GHSR; PSPC1; BPI |
Gene Set | Description | Size | Overlap | ER | p-Value | FDR |
---|---|---|---|---|---|---|
EP | ||||||
R-HSA-2173782 | Binding and uptake of ligands by scavenger receptors | 42 | 6 | 14.2 | 3.48 × 10−6 | 0.01 |
R-HSA-3000178 | ECM proteoglycans | 76 | 6 | 7.9 | 1.10 × 10−4 | 0.06 |
R-HSA-1474244 | Extracellular matrix organization | 301 | 11 | 3.6 | 2.11 × 10−4 | 0.06 |
R-HSA-1480926 | O2/CO2 exchange in erythrocytes | 13 | 3 | 21.0 | 2.62 × 10−4 | 0.06 |
R-HSA-198933 | Immunoregulatory interactions between a lymphoid and a nonlymphoid cell | 132 | 8 | 5.3 | 3.56 × 10−4 | 0.08 |
R-HSA-1280215 | Cytokine signaling in the immune system | 688 | 16 | 2.3 | 1.33 × 10−3 | 0.25 |
R-HSA-168256 | Immune system | 1997 | 32 | 1.60 | 3.35 × 10−3 | 0.40 |
EN | ||||||
hsa04115 | p53 signal pathway | 72 | 7 | 6.2 | 1.23 × 10−4 | 0.04 |
R-HSA-198933 | Immunoregulatory interactions between al and a nonlymphoid cell | 132 | 7 | 3.7 | 2.73 × 10−3 | 0.11 |
R-HSA-1793185 | Chondroitin sulfate/dermatan sulfate metabolism | 50 | 4 | 9.3 | 8.80 × 10−4 | 0.19 |
R-HSA-1480926 | O2/CO2 exchange in erythrocytes | 13 | 3 | 18.5 | 4.99 × 10−4 | 0.29 |
hsa04110 | Cell cycle | 124 | 7 | 3.6 | 3.22 × 10−3 | 0.34 |
R-HSA-5633008 | TP53 Regulates the transcription of cell death genes | 44 | 4 | 7.3 | 2.15 × 10−3 | 0.41 |
R-HSA-3000170 | Syndecan interactions | 27 | 3 | 8.9 | 4.49 × 10−3 | 0.65 |
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Kyselová, J.; Tichý, L.; Sztankóová, Z.; Marková, J.; Kavanová, K.; Beinhauerová, M.; Mušková, M. Comparative Characterization of Immune Response in Sheep with Caseous Lymphadenitis through Analysis of the Whole Blood Transcriptome. Animals 2023, 13, 2144. https://doi.org/10.3390/ani13132144
Kyselová J, Tichý L, Sztankóová Z, Marková J, Kavanová K, Beinhauerová M, Mušková M. Comparative Characterization of Immune Response in Sheep with Caseous Lymphadenitis through Analysis of the Whole Blood Transcriptome. Animals. 2023; 13(13):2144. https://doi.org/10.3390/ani13132144
Chicago/Turabian StyleKyselová, Jitka, Ladislav Tichý, Zuzana Sztankóová, Jiřina Marková, Kateřina Kavanová, Monika Beinhauerová, and Michala Mušková. 2023. "Comparative Characterization of Immune Response in Sheep with Caseous Lymphadenitis through Analysis of the Whole Blood Transcriptome" Animals 13, no. 13: 2144. https://doi.org/10.3390/ani13132144