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Integrated analysis of miRNA and mRNA transcriptomic reveals antler growth regulatory network

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Abstract

The growth of antler is driven by endochondral ossification in the growth center of the apical region. Antler grows faster than cancer tissues, but it can be stably regulated and regenerated periodically. To elucidate the molecular mechanisms of how antler grows rapidly without carcinogenesis, in this study, we used RNA-seq technology to evaluate the changes of miRNA and mRNA profiles in antler at four different developmental stages, including 15, 60, 90, and 110 days. We identified a total of 55004 unigenes and 246 miRNAs of which, 10182, 13258, 10740 differentially expressed (DE) unigenes and 35, 53, 27 DE miRNAs were identified in 60-day vs. 15-day, 90-day vs. 60-day, and 110-day vs. 90-day. GO and KEGG pathway analysis indicated that DE unigenes and DE miRNA were mainly associated with chondrogenesis, osteogenesis and inhibition of oncogenesis, that were closely related to antler growth. The interaction networks of mRNA–mRNA and miRNA–mRNA related to chondrogenesis, osteogenesis and inhibition of oncogenesis of antler were constructed. The results indicated that mRNAs (COL2A1, SOX9, WWP2, FGFR1, SPARC, LOX, etc.) and miRNAs (miR-145, miR-199a-3p, miR-140, miR-199a-5p, etc.) might have key roles in chondrogenesis and osteogenesis of antler. As well as mRNA (TP53, Tpm3 and ATP1A1, etc.) and miRNA (miR-106a, miR-145, miR-1260b and miR-2898, etc.) might play important roles in inhibiting the carcinogenesis of antler. In summary, we constructed the mRNA–mRNA and miRNA–mRNA regulatory networks related to chondrogenesis, osteogenesis and inhibition of oncogenesis of antler, and identified key candidate mRNAs and miRNAs among them. Further developments and validations may provide a reference for in-depth analysis of the molecular mechanism of antler growth without carcinogenesis.

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Acknowledgements

The authors would like to thank staff from the Institute of Special Economic Animals and Plants and State Key Laboratory for Molecular Biology of Special Economical Animals, Chinese Academy of Agricultural Sciences, for help in sika deer tissue collection. Illumina sequencing was performed at the Novogene Bioinformatics Technology Co., Ltd., Beijing, China. This study was funded by National Natural Science Foundation of China (Grant/Award number: 32002171).

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Authors and Affiliations

  1. College of Animal Medicine/College of Animal Science and Technology, Jilin Agricultural University, 2888 Xincheng Street, Changchun, 130118, China

    Boyin Jia, Linlin Zhang & Yifan Zhang

  2. College of Vocational and Technical Education, Changchun Sci-Tech University, 1699 Donghua Street, Changchun, 130606, China

    Chenxia Ge

  3. Institute of Wild Economic Animals and Plants and State Key Laboratory for Molecular Biology of Special Economical Animals, Chinese Academy of Agricultural Sciences, 4899 Juye Street, Changchun, 130112, China

    Fuhe Yang

  4. Laboratory of Production and Product Application of Sika Deer of Jilin Province, Jilin Agricultural University, 2888 Xincheng Street, Changchun, 130118, China

    Rui Du

  5. Institute of Antler Science and Product Technology, Changchun Sci-Tech University, 1345 Pudong Road, Changchun, 130000, China

    Hengxing Ba

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  1. Boyin Jia
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  2. Linlin Zhang
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  3. Yifan Zhang
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  4. Chenxia Ge
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  6. Rui Du
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Correspondence to Rui Du or Hengxing Ba.

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Ethical approval

Antler tips were collected from anesthetized sika deer in strict accordance approved by the ethics committee of Jilin Agricultural University.

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Communicated by Stefan Hohmann.

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Suppl. Fig. 1 Characterization of miRNA-seq mapped reads from the small RNA sequencing of antler. (TIF 131 KB)

Suppl. Fig. 2 The top 20 GO categories of DE unigenes in each comparable group. (TIF 1317 KB)

Suppl. Fig. 3 The top 20 enriched KEGG pathways of DE unigenes in each comparable group. (TIF 566 KB)

Suppl. Fig. 4 The top 20 enriched GO terms for the potential genes targeted by DE miRNAs. (TIF 1698 KB)

Suppl. Fig.5 The top 20 enriched KEGG pathways for the potential genes targeted by DE miRNAs. (TIF 465 KB)

Supplementary Data 1. Summary of transcriptome data. (XLS 20 KB)

Supplementary Data 2. FPKM statistical of antler transcriptome in sika deer. (XLS 21 KB)

Supplementary Data 3. Summary of miRNAome data. (XLS 19 KB)

Supplementary Data 4. Statistical information of small RNAs mapping to reference sequence. (XLS 21 KB)

Supplementary Data 5. Small RNAs annotation. (XLSX 13 KB)

Supplementary Data 6. Identification of known miRNAs and novel miRNAs. (XLSX 19 KB)

Supplementary Data 7. The lists of DE unigenes. (XLS 1949 KB)

Supplementary Data 8. GO categories of differential unigenes in four growth periods. (XLS 3167 KB)

Supplementary Data 9. KEGG pathways of differential unigenes in four growth periods. (XLS 1425 KB)

Supplementary Data 10. Interaction networks of DE unigenes in each comparable group. (XLS 309 KB)

Supplementary Data 11. Known miRNA four growth periods. (XLS 45 KB)

Supplementary Data 12. The lists of DE miRNAs. (XLS 28 KB)

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Jia, B., Zhang, L., Zhang, Y. et al. Integrated analysis of miRNA and mRNA transcriptomic reveals antler growth regulatory network. Mol Genet Genomics 296, 689–703 (2021). https://doi.org/10.1007/s00438-021-01776-z

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  • DOI: https://doi.org/10.1007/s00438-021-01776-z

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