Transcriptome and Proteome Analysis Revealed Key Pathways Regulating Final Stage of Oocyte Maturation of the Turkey (Meleagris gallopavo)
Abstract
:1. Introduction
2. Results
2.1. Sequencing Results
2.2. Transcriptome of Inner Perivitelline Layer: Functional Annotation and Pathway Analysis
2.3. Proteome of Inner Perivitelline Layer: Functional Annotation and Pathway Analysis
2.4. Phylogenetic Analysis of Bird ZP Glycoproteins
2.5. Identification of Ubiquitinated Proteins and Immunohistochemical Detection of Ubiquitin in the IPVL and the GC layer
2.6. Immunohistochemical Detection of Cell Junction Proteins in GCs Surrounding the IPVL
2.7. Validation of Selected Genes by Quantitative Real-Time Reverse Transcriptase-Polymerase Chain Reaction (qRT-PCR)
3. Discussion
3.1. ZP Glycoproteins
3.2. Ubiquitination
3.3. Protein Synthesis
3.4. Sirtuin Signaling Pathway
3.5. Estrogen Receptor Signaling
3.6. Mitochondrial Oxidative Phosphorylation
3.7. The Cellular Response against Oxidative Stress
3.8. Cell-Cell Junction—Intercellular Interactions of GCs
4. Materials and Methods
4.1. Birds, Housing, and Tissue Collection
4.2. Tissue Morphology
4.3. RNA Isolation and the Evaluation of RNA Integrity
4.4. Library Preparation and Sequencing Procedures
4.5. Quality Control and Mapping Process
4.6. 2DE and Protein Identification by MALDI TOF/TOF
4.7. Functional Analysis
4.8. Phylogenetic Analysis
4.9. Immunohistochemistry
4.10. Identification of Ubiquitinated Proteins in the IPVL
4.11. Quantitative Real-Time Reverse Transcriptase PCR
Statistical Analysis
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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IPVL Samples | O1 | O2 | O3 | O4 | O5 | O6 |
---|---|---|---|---|---|---|
row reads | 1.03 × 108 | 1.18 × 108 | 1.05 × 108 | 1.16 × 108 | 1.2 × 108 | 1.01 × 108 |
trimmed reads | 1.02 × 108 | 1.16 × 108 | 1.03 × 108 | 1.14 × 108 | 1.19 × 108 | 0.99 × 108 |
mapped | 82307430 | 93758986 | 87048822 | 96081072 | 99511690 | 83720988 |
uniquely mapped | 80362334 | 91783236 | 84612194 | 93744112 | 97406022 | 81650560 |
mapped to coding regions (%) | 41.90 | 40.75 | 43.94 | 44.59 | 43.72 | 43.38 |
mapped to UTR (%) | 7.18 | 7.20 | 5.07 | 5.22 | 5.38 | 5.47 |
mapped to introns (%) | 5.30 | 5.14 | 7.13 | 7.61 | 7.70 | 7.51 |
mapped to intergenic regions (%) | 45.62 | 46.90 | 43.85 | 42.58 | 43.20 | 43.64 |
multi-mapped | 1,940,566 | 1,969,616 | 2,431,930 | 2,333,492 | 2,102,302 | 2,065,832 |
too many loci | 4530 | 6134 | 4698 | 3468 | 3366 | 4596 |
p Value | No Molecules | Functional Analysis | p Value | No Molecules |
---|---|---|---|---|
Trancriptome | Ingeniuty Canonical Pathways | Proteome | ||
1.05 × 1028 | 142 | Protein Ubiquitination Pathway | 9.18 × 108 | 15 |
1.35 × 1026 | 121 | EIF2 Signaling | 1.43 × 105 | 11 |
7.81 × 1020 | 86 | Regulation of eIF4 and p70S6K Signaling | 1.66 × 104 | 8 |
6.05 × 1018 | 128 | Sirtuin Signaling Pathway | 6.00 × 1011 | 11 |
8.65 × 1017 | 137 | Estrogen Receptor Signaling | 1.57 × 103 | 10 |
9.21 × 1017 | 86 | Mitochondrial Dysfunction | 1.89 × 1018 | 22 |
4.68 × 1015 | 89 | NRF2-mediated Oxidative Stress Response | 6.02 × 1012 | 17 |
1.32 × 1014 | 95 | mTOR Signaling | 4.83 × 103 | 7 |
9.55 × 1011 | 54 | Oxidative Phosphorylation | 1.20 × 1018 | 19 |
8.33 × 106 | 31 | Remodeling of Epithelial Adherens Junctions | 9.18 × 1011 | 10 |
1.80 × 105 | 22 | BAG2 Signaling Pathway | 3.05 × 1010 | 9 |
Gluconeogenesis I | 4.50 × 109 | 7 | ||
4.38 × 107 | 79 | Actin Cytoskeleton Signaling | 3.62 × 108 | 14 |
Molecular and Cellular Function | ||||
7.31 × 1010–3.36 × 1070 | 760 | Protein Synthesis | 2.91 × 105–1.47 × 1016 | 68 |
1.86 × 1014–2.18 × 1068 | 376 | RNA Post-Transcriptional Modification | ||
9.96 × 1010–1.18 × 1053 | 1728 | Cell Death and Survival | 5.64 × 105–4.34 × 1024 | 127 |
1.32 × 1018–1.68 × 1040 | 380 | Protein Degradation | ||
8.39 × 1010–4.77 × 1034 | 1048 | Molecular Transport | ||
Post-Transcriptional Modification | 5.05 × 105–2.93 × 1022 | 43 | ||
Protein Folding | 5.05 × 105–4.02 × 1021 | 22 | ||
Cellular Compromise | 1.71 × 106–2.20 × 1015 | 46 | ||
Physiological System Development and Function | ||||
1.15 × 1012–6.47 × 1059 | 1242 | Organismal Survival | 9.44 × 1010–9.44 × 1010 | 76 |
1.81 × 1010–3.72 × 1024 | 1012 | Embryonic Development | 4.43 × 107–8.27 × 109 | 23 |
3.60 × 1010–3.72 × 1024 | 1413 | Organismal Development | 3.55 × 105–8.27 × 109 | 55 |
1.86 × 1011–3.72 × 1024 | 371 | Tissue Morphology | ||
5.78 × 1010–1.06 × 1019 | 542 | Connective Tissue Development and Function | ||
Tissue Development | 1.13 × 105–6.47 × 1059 | 52 | ||
Organ Development | 2.73 × 106–8.27 × 109 | 30 | ||
Score | Top Networks | Score | ||
28 | 35 | Molecular Transport, RNA Post-Transcriptional Modification, RNA Trafficking | ||
28 | 35 | Protein Synthesis. RNA Damage and Repair | ||
28 | 35 | Post-Translational Modification, Protein Degradation, Protein Synthesis | ||
Cellular Assembly and Organization, RNA Post-Transcriptional Modification | 57 | 29 | ||
Cell Death and Survival, Drug Metabolism. Small Molecule Biochemistry | 46 | 25 | ||
Gene Expression, Post-Translational Modification, Protein Folding | 39 | 22 | ||
Cell Death and Survival, Gene Expression Protein Synthesis | 32 | 19 |
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Słowińska, M.; Paukszto, Ł.; Pardyak, L.; Jastrzębski, J.P.; Liszewska, E.; Wiśniewska, J.; Kozłowski, K.; Jankowski, J.; Bilińska, B.; Ciereszko, A. Transcriptome and Proteome Analysis Revealed Key Pathways Regulating Final Stage of Oocyte Maturation of the Turkey (Meleagris gallopavo). Int. J. Mol. Sci. 2021, 22, 10589. https://doi.org/10.3390/ijms221910589
Słowińska M, Paukszto Ł, Pardyak L, Jastrzębski JP, Liszewska E, Wiśniewska J, Kozłowski K, Jankowski J, Bilińska B, Ciereszko A. Transcriptome and Proteome Analysis Revealed Key Pathways Regulating Final Stage of Oocyte Maturation of the Turkey (Meleagris gallopavo). International Journal of Molecular Sciences. 2021; 22(19):10589. https://doi.org/10.3390/ijms221910589
Chicago/Turabian StyleSłowińska, Mariola, Łukasz Paukszto, Laura Pardyak, Jan P. Jastrzębski, Ewa Liszewska, Joanna Wiśniewska, Krzysztof Kozłowski, Jan Jankowski, Barbara Bilińska, and Andrzej Ciereszko. 2021. "Transcriptome and Proteome Analysis Revealed Key Pathways Regulating Final Stage of Oocyte Maturation of the Turkey (Meleagris gallopavo)" International Journal of Molecular Sciences 22, no. 19: 10589. https://doi.org/10.3390/ijms221910589