Skip to main content
SpringerLink
Log in

Identification of the Differential Expression Profile of miRNAs in Longissimus dorsi Muscle of Dazu Black Goat

  • HUMAN GENETICS
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

MicroRNA (miRNA) was verified to display an important molecular regulatory role in the development of skeletal muscle. In this study, we identified the differentially expressed miRNAs from longissimus dorsi muscle of Dazu black goat at different stages (75 days embryonic stage [ET]) and 1 day after birth [DC]) to understand the regulatory role of miRNAs in the development of skeletal muscle. This work is expected to provide a theoretical basis for goat breeding in meat production. Results revealed a total of 218,161,800 clean tags from all the libraries; 546 significant differentially (p < 0.05) expressed miRNAs (DE_miRNAs) were identified, including 321 up-regulated and 225 down-regulated DE_miRNAs. Moreover, GO and KEGG analyses of the genes targeted by the DE_miRNAs revealed 59 and 345 significantly enriched GO terms and pathways associated with muscle development, respectively, such as the PI3K/Akt, Wnt. A total of 21 miRNAs from 546 DE_miRNAs were selected to estimate the agreement rate between miRNA-seq by RT-qPCR, and the results showed that the expressed pattern was completely unified from both. In brief, a series of miRNAs related to muscle development was identified in this study. This work provides valuable information to further understand the molecular regulatory mechanism of muscle development in goats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Kalds, P., Zhou, S., Cai, B., Liu, J., Wang, Y., Petersen, B., Sonstegard, T., Wang, X., and Chen, Y., Sheep and goat genome engineering: from random transgenesis to the CRISPR era, Front. Genet., 2019, p. 750. https://doi.org/10.3389/fgene.2019.00750

  2. Aiello, D., Patel, K., and Lasagna, E., The myostatin gene: an overview of mechanisms of action and its relevance to livestock animals, Anim. Genet., 2018, pp. 505—519. https://doi.org/10.1111/age.12696

  3. Widmann, M., Nie, A.M., and Munz, B., Physical exercise and epigenetic modifications in skeletal muscle, Sports Med., 2019, pp. 509—523. https://doi.org/10.1007/s40279-019-01070-4

  4. Hargreaves, M. and Spriet, L.L., Skeletal muscle energy metabolism during exercise, Nat. Metab., 2020, pp. 817—828. https://doi.org/10.1038/s42255-020-0251-4

  5. Silva, L.H.P., Rodrigues, R.T.S., Assis, D.E.F., Benedeti, P.D.B., Duarte, M.S. and Chizzotti, M.L., Explaining meat quality of bulls and steers by differential proteome and phosphoproteome analysis of skeletal muscle, J. Proteomics, 2019, pp. 51—66. https://doi.org/10.1016/j.jprot.2019.03.004

  6. Bartel, D.P., MicroRNAs: genomics, biogenesis, mechanism, and function, Cell, 2004, pp. 281—297. https://doi.org/10.1016/s0092-8674(04)00045-5

  7. Ling, Y.H., Sui, M.H., Zheng, Q., Wang, K.Y., Wu, H., Li, W.Y., Liu, Y., Chu, M.X., Fang, F.G., and Xu, L.N., miR-27b regulates myogenic proliferation and differentiation by targeting Pax3 in goat, Sci. Rep., 2018, p. 3909. https://doi.org/10.1038/s41598-018-22262-4

  8. Chen, X., Zhao, C., Dou, M., Sun, Y., Yu, T., Pang, W., and Yang G., Deciphering the miRNA transcriptome of Rongchang pig longissimus dorsi at weaning and slaughter time points, J. Anim. Physiol. Anim. Nutr. (Berlin), 2020, pp. 954—964. https://doi.org/10.1111/jpn.13314

  9. Chen, M., Zhang, S., Xu, Z., Gao, J., Mishra, S.K., Zhu, Q., Zhao, X., Wang, Y., Yin, H., Fan, X., Zeng, B., Yang, M., Yang, D., Ni, Q., Li, Y., Zhang, M. and Li, D., MiRNA profiling in pectoral muscle throughout pre- to post-natal stages of chicken development, Front. Genet., 2020, p. 570. https://doi.org/10.3389/fgene.2020.00570

  10. Ling, Y., Xu, L., Zhu, L., Sui, M., Zheng, Q., Li, W., Liu, Y., Fang, F., and Zhang, X., RNA-seq reveals miRNA role shifts in seven stages of skeletal muscles in goat fetuses and kids, Front. Genet., 2020, p. 684. https://doi.org/10.3389/fgene.2020.00684

  11. Zhang, W., Tong, H., Zhang, Z., Shao, S., Liu, D., Li, S., and Yan, Y., Transcription factor EGR1 promotes differentiation of bovine skeletal muscle satellite cells by regulating MyoG gene expression, J. Cell. Physiol., 2018, pp. 350—362. https://doi.org/10.1002/jcp.25883

  12. Zhang, W., Wang, S.Y., Deng, S.Y., Gao, L., Yang, L.W., Liu, X.N., and Shi, G.Q., MiR-27b promotes sheep skeletal muscle satellite cell proliferation by targeting myostatin gene, J. Genet., 2018, pp. 1107—1117.

  13. Song, C., Yang, J., Jiang, R., Yang, Z., Li, H., Huang, Y., Lan, X., Lei, C., Ma, Y., Qi. X., and Chen, H., miR-148a-3p regulates proliferation and apoptosis of bovine muscle cells by targeting KLF6, J. Cell. Physiol., 2019. https://doi.org/10.1002/jcp.28232

  14. Zhang, X., Cai, S., Chen, L., Yuan, R., Nie, Y., Ding, S., Fang, Y., Zhu, Q., Chen, K., Wei, H., Chen, Y., and Mo, D., Integrated miRNA-mRNA transcriptomic analysis reveals epigenetic-mediated embryonic muscle growth differences between Wuzhishan and Landrace pigs1, J. Anim. Sci., 2019, pp. 1967—1978. https://doi.org/10.1093/jas/skz091

  15. Gu, B., Liu, H., Han, Y., Chen, Y., and Jiang, H., Integrated analysis of miRNA and mRNA expression profiles in 2-, 6-, and 12-month-old Small Tail Han sheep ovaries reveals that oar-miR-432 downregulates RPS6KA1 expression, Gene, 2019, pp. 76—90. https://doi.org/10.1016/j.gene.2019.02.095

  16. Tesfaye, D., Gebremedhn, S., Salilew-Wondim, D., Hailay, T., Hoelker, M., Grosse-Brinkhaus, C., and Schellander, K., MicroRNAs: tiny molecules with a significant role in mammalian follicular and oocyte development, Reproduction, 2018, pp. R121—R135. https://doi.org/10.1530/REP-17-0428

  17. Chu, M., Zhao, Y., Yu, S., Hao, Y., Zhang, P., Feng, Y., Zhang, H., Ma, D., Liu, J., Cheng, M., Li, L., Shen, W., Cao, H., Li, Q., and Min, L., miR-15b negatively correlates with lipid metabolism in mammary epithelial cells, Am. J. Physiol.—Cell Physiol., 2018, vol. 314, no. 1, pp. C43—C52. https://doi.org/10.1152/ajpcell.00115.2017

    Article  CAS  PubMed  Google Scholar 

  18. Wang, H., Shi, H., Luo, J., Yi, Y., Yao, D., Zhang, X., Ma, G., and Loor, J.J., MiR-145 regulates lipogenesis in goat mammary cells via targeting INSIG1 and epigenetic regulation of lipid-related genes, J. Cell. Physiol., 2017, pp. 1030—1040. https://doi.org/10.1002/jcp.25499

  19. Ivanova, E., Le Guillou, S., Hue-Beauvais, C., and Le Provost, F., Epigenetics: new insights into mammary gland biology, Genes (Basel), 2021. https://doi.org/10.3390/genes12020231

  20. Ma, T., Li, J., Li, J., Wu, S., Xiangba, Jiang, H., and Zhang, Q., Expression of miRNA-203 and its target gene in hair follicle cycle development of Cashmere goat, Cell Cycle, 2021, pp. 204—210. https://doi.org/10.1080/15384101.2020.1867789

  21. Nocelli, C., Cappelli, K., Capomaccio, S., Pascucci, L., Mercati, F., Pazzaglia, I., Mecocci, S., Antonini, M., and Renieri, C., Shedding light on cashmere goat hair follicle biology: from morphology analyses to transcriptomic landascape, BMC Genomics, 2020, p. 458. https://doi.org/10.1186/s12864-020-06870-x

  22. China National Commission of Animal Genetic Resources, Animal Genetic Resources in China: Sheep and Goat, Beijing: Chinese Agricultural Press, 2011.

    Google Scholar 

  23. Na, R., Zeng, Y., Han, Y., Liu, C., Yang, B., and He, Y., Identification of differentially expressed microRNAs in ovulatory and subordinate follicles in Dazu black goats, Anim. Biotechnol., 2021, pp. 1—7. https://doi.org/10.1080/10495398.2021.1895185

  24. Wang, L.J., Sun, X.W., Guo, F.Y., Zhao, Y.J., Zhang, J.H., and Zhao, Z.Q., Transcriptome analysis of the uniparous and multiparous goats ovaries Reprod. Domest. Anim., 2016, pp. 877—885. https://doi.org/10.1111/rda.12750

  25. E, G.X., Zhao, Y.J., and Huang, Y.F., Selection signatures of litter size in Dazu black goats based on a whole genome sequencing mixed pools strategy, Mol. Biol. Rep., 2019, pp. 5517—5523. https://doi.org/10.1007/s11033-019-04904-6

  26. Alvarez, R., Vera, L., Pongor, S., Marino-Ramirez, L., and Landsman, D., TPM Calculator: one-step software to quantify mRNA abundance of genomic features, Bioinformatics, 2019, pp. 1960—1962. https://doi.org/10.1093/bioinformatics/bty896

  27. Sui, M., Zheng, Q., Wu, H., Zhu, L., Ling, Y., Wang, L., Fang, F., Liu, Y., Zhang, Z., Chu, M., and Zhang, Y., The expression and regulation of miR-1 in goat skeletal muscle and satellite cell during muscle growth and development, Anim. Biotechnol., 2020, pp. 455—462. https://doi.org/10.1080/10495398.2019.1622555

  28. Mok, G.F., Lozano-Velasco, E., Maniou, E., Viaut, C., Moxon, S., Wheeler, G., and Munsterberg, A., miR-133-mediated regulation of the Hedgehog pathway orchestrates embryo myogenesis, Development, 2018. https://doi.org/10.1242/dev.159657

  29. Wüst, S., Dröse, S., Heidler, J., Wittig, I., Klockner, I., Franko, A., Bonke, E., Günther, S., Gärtner, U., Boettger, T., and Braun, T., Metabolic maturation during muscle stem cell differentiation is achieved by miR-1/133a-mediated inhibition of the Dlk1-Dio3 Mega gene cluster, Cell Metab., 2018, pp. 1026—1039. https://doi.org/10.1016/j.cmet.2018.02.022

  30. Nicolai, S., Pieraccioli, M., Smirnov, A., Pitolli, C., Anemona, L., Mauriello, A., Candi, E., Annicchiarico-Petruzzelli, M., Shi, Y., Wang, Y., Melino, G., and Raschellà, G., ZNF281/Zfp281 is a target of miR-1 and counteracts muscle differentiation, Mol. Oncol., 2020, pp. 294—308. https://doi.org/10.1002/1878-0261.12605

  31. Bjorkman, K.K., Buvoli, M., Pugach, E.K., Polmear, M.M., and Leinwand, L.A., miR-1/206 downregulates splicing factor Srsf9 to promote C2C12 differentiation, Skelet Muscle, 2019, p. 31. https://doi.org/10.1186/s13395-019-0211-4

  32. Zhang, J., Hua, C., Zhang, Y., Wei, P., Tu, Y., and Wie, T., KAP1-associated transcriptional inhibitory complex regulates C2C12 myoblasts differentiation and mitochondrial biogenesis via miR-133a repression, Cell Death Dis., 2020, p. 732. https://doi.org/10.1038/s41419-020-02937-5

  33. Carvalho, E.B., Gionbelli, M.P., Rodrigues, R.T.S., Bonilha, S.F. M., Newbold, C.J., Guimaraes, S.E.F., Silva, W., Verardo, L.L., Silva, F.F., Detmann, E., and Duarte, M.S., Differentially expressed mRNAs, proteins and miRNAs associated to energy metabolism in skeletal muscle of beef cattle identified for low and high residual feed intake, BMC Genomics, 2019, p. 501. https://doi.org/10.1186/s12864-019-5890-z

  34. Wang, Y., Mei, C., Su, X., Wang, H., Yang, W., and Zan, L., MEF2A regulates the MEG3-DIO3 miRNA mega cluster-targeted PP2A signaling in bovine skeletal myoblast differentiation, Int. J. Mol. Sci., 2019. https://doi.org/10.3390/ijms20112748

  35. Chaweewannakorn, C., Tsuchiya, M., Koide, M., Hatakeyama, H., Tanaka, Y., Yoshida, S., Sugawara, S., Hagiwara, Y., Sasaki, K., and Kanzaki, M., Roles of IL-1alpha/beta in regeneration of cardiotoxin-injured muscle and satellite cell function, Am. J. Physiol. Regul. Integr. Comp. Physiol., 2018, pp. R90—R103. https://doi.org/10.1152/ajpregu.00310.2017

  36. Li, F., Yin, C., Ma, Z., Yang, K., Sun, L., Duan, C., Wang, T., Hussein, A., Wang, L., Zhu, X., Gao, P., Xi, Q., Zhang, Y., Shu, G., Wang, S., and Jiang, Q., PHD3 mediates denervation skeletal muscle atrophy through Nf-kappaB signal pathway, FASEB J., 2021. e21444. https://doi.org/10.1096/fj.202002049R

  37. Huang, J., Wang, K., Shiflett, L.A., Brotto, L., Bonewald, L.F., Wacker, M.J., Dallas, S.L. and Brotto, M., Fibroblast growth factor 9 (FGF9) inhibits myogenic differentiation of C2C12 and human muscle cells, Cell Cycle, 2019, pp. 3562—3580. https://doi.org/10.1080/15384101.2019.1691796

  38. Yang, Z., Qu, Z., Yi, M., Lv, Z., Wang, Y., Shan, Y., Ran, N., and Liu, X., MiR-204-5p inhibits transforming growth factor-beta1-induced proliferation and extracellular matrix production of airway smooth muscle cells by regulating Six1 in asthma, Int. Arch. Allergy Immunol., 2020, pp. 239—248. https://doi.org/10.1159/000505064

  39. Maire, P., Dos Santos, M., Madani, R., Sakakibara, I., Viaut, C., and Wurmser, M., Myogenesis control by SIX transcriptional complexes, Semin. Cell Dev. Biol., 2020, pp. 51—64. https://doi.org/10.1016/j.semcdb.2020.03.003

  40. Ma, J., Xu, G., Wan, L., and Wang, N., Molecular cloning, sequence analysis and tissue-specific expression of Akirin2 gene in Tianfu goat, Gene, 2015, pp. 9—15. https://doi.org/10.1016/j.gene.2014.09.030

  41. Macqueen, D.J., Bower, N.I., and Johnston, I.A., Positioning the expanded akirin gene family of Atlantic salmon within the transcriptional networks of myogenesis, Biochem. Biophys. Res. Commun., 2010, pp. 599—605. https://doi.org/10.1016/j.bbrc.2010.08.110

  42. Rao, V.V., Sangiah, U., Mary, K.A., Akira, S., and Mohanty, A., Role of Akirin1 in the regulation of skeletal muscle fiber-type switch, J. Cell. Biochem., 2019. https://doi.org/10.1002/jcb.28406

  43. Chen, X., Luo, Y., Huang, Z., Jia, G., Liu, G., and Zhao, H., Akirin2 regulates proliferation and differentiation of porcine skeletal muscle satellite cells via ERK1/2 and NFATc1 signaling pathways, Sci. Rep., 2017, p. 45156. https://doi.org/10.1038/srep45156

  44. Sun, W., Huang, H., Ma, S., Gan, X., Zhu, M., Liu, H., Li, L., and Wang, J., Akirin2 could promote the proliferation but not the differentiation of duck myoblasts via the activation of the mTOR/p70S6K signaling pathway, Int. J. Biochem. Cell Biol., 2016, pp. 298—307. https://doi.org/10.1016/j.biocel.2016.08.032

  45. Wang, Y., Yan, X., Liu, H., Hu, S., Hu, J., Li, L., and Wang, J., Effect of thermal manipulation during embryogenesis on the promoter methylation and expression of myogenesis-related genes in duck skeletal muscle, J. Therm. Biol., 2019, pp. 75—81. https://doi.org/10.1016/j.jtherbio.2018.12.023

  46. Taylor, M.V. and Hughes, S.M., Mef2 and the skeletal muscle differentiation program, Semin. Cell Dev. Biol., 2017, pp. 33—44. https://doi.org/10.1016/j.semcdb.2017.11.020

  47. Anderson, C.M., Hu, J., Barnes, R.M., Heidt, A.B., Cornelissen, I., and Black, B.L., Myocyte enhancer factor 2C function in skeletal muscle is required for normal growth and glucose metabolism in mice, Skelet Muscle, 2015, p. 7. https://doi.org/10.1186/s13395-015-0031-0

  48. Ninfali, C., Siles, L., Darling, D.S., and Postigo, A., Regulation of muscle atrophy-related genes by the opposing transcriptional activities of ZEB1/CtBP and FOXO3, Nucleic Acids Res., 2018, pp. 10697—10708. https://doi.org/10.1093/nar/gky835

  49. Li, G., Luo, W., Abdalla, B.A., Ouyang, H., Yu, J., Hu, F., Nie, Q., and Zhang, X., miRNA-223 upregulated by MYOD inhibits myoblast proliferation by repressing IGF2 and facilitates myoblast differentiation by inhibiting ZEB1, Cell Death Dis., 2017. e3094. https://doi.org/10.1038/cddis.2017.479

  50. Girardi F., and Le Grand, F., Wnt signaling in skeletal muscle development and regeneration, Prog. Mol. Biol. Transl. Sci., 2018, pp. 157—179. https://doi.org/10.1016/bs.pmbts.2017.11.026

  51. von Maltzahn, J., Bentzinger, C.F, and Rudnicki, M.A., Wnt7a-Fzd7 signalling directly activates the Akt/mTOR anabolic growth pathway in skeletal muscle, Nat. Cell Biol., 2011, pp. 186—191. https://doi.org/10.1038/ncb2404

  52. Lacour, F., Vezin, E., Bentzinger, C.F., Sincennes, M.C., Giordani, L., Ferry, A., Mitchell, R., Patel, K., Rudnicki, M.A., Chaboissier, M.C., Chassot, A.A., Le Grand, F., R-spondin1 controls muscle cell fusion through dual regulation of antagonistic Wnt signaling pathways, Cell Rep., 2017, pp. 2320—2330. https://doi.org/10.1016/j.celrep.2017.02.036

  53. Ma, H., Wu, Y., and Zhang, H., Notch signaling in bone formation and related skeletal diseases, Zhonghua Yi Xue Yi Chuan Xue Za Zhi, 2015, pp. 274—279. https://doi.org/10.3760/cma.j.issn.1003-9406.2015.02.027

  54. Verma, M., Asakura, Y., Murakonda, B.S.R., Pengo, T., Latroche, C., Chazaud, B., McLoon, L.K., and Asakura, A., Muscle satellite cell cross-talk with a vascular niche maintains quiescence via VEGF and notch signaling, Cell Stem Cell, 2018, pp. 530—543. https://doi.org/10.1016/j.stem.2018.09.007

  55. Luo, Z., Shang, X., Zhang, H., Wang, G., Massey, P.A., Barton, S.R., Kevil, C.G., and Dong, Y., Notch signaling in osteogenesis, osteoclastogenesis, and angiogenesis, Am. J. Pathol., 2019, pp. 1495—1500. https://doi.org/10.1016/j.ajpath.2019.05.005

  56. Chi, B., Liu, G., Xing, L., and Tian, F., Research progress of Hedgehog signaling pathway in regulating bone formation and osteogenic differentiation of bone mesenchymal stem cells, Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi, 2016, pp. 1545—1550. https://doi.org/10.7507/1002-1892.20160318

  57. Voronova, A., Coyne, E., Al Madhoun, A., Fair, J.V., Bosiljcic, N., St-Louis, C., Li, G., Thurig, S., Wallace, V.A., Wiper-Bergeron, N., and Skerjanc, I.S., Hedgehog signaling regulates MyoD expression and activity, J. Biol. Chem., 2013, vol. 288, no. 6, pp. 4389—4404. https://doi.org/10.1074/jbc.M112.400184

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by the Chongqing Overseas Student Entrepreneurship Innovation Support Plan (grant number no. cx2019132); the Fundamental Research Funds for the Central Universities (grant no. XDJK2019B049); National Natural Science Foundation of China (grant no. 32102544); the Chongqing Science and Technology Innovation Special Project (grant number no. cstc2017shms-zdyfX0059).

Author information

Author notes

    Authors and Affiliations

    1. College of Animal Science and Technology, Chongqing Key Laboratory of Forage and Herbivore, Chongqing Engineering Research Centre for Herbivores Resource Protection and Utilization, Southwest University, 400716, Chongqing, China

      S.-Q. Zeng, Ch.-L. Liu, Ch.-Na. Huang, W.-J. Si, Ch.-B. Liu, L.-X. Ren, W.-Y. Zhang, Y.-M. He, Y. Yuan, H.-Y. Zhang, Y.-G. Han, R.-S. Na, G.-X. E & Y.-F. Huang

    Authors
    1. S.-Q. Zeng
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Ch.-L. Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Ch.-Na. Huang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. W.-J. Si
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Ch.-B. Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. L.-X. Ren
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. W.-Y. Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Y.-M. He
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Y. Yuan
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. H.-Y. Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    11. Y.-G. Han
      View author publications

      You can also search for this author in PubMed Google Scholar

    12. R.-S. Na
      View author publications

      You can also search for this author in PubMed Google Scholar

    13. G.-X. E
      View author publications

      You can also search for this author in PubMed Google Scholar

    14. Y.-F. Huang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Contributions

    S.-Q. Zeng and Ch.-L. Liu contributed equally to this work.

    Corresponding authors

    Correspondence to G.-X. E or Y.-F. Huang.

    Ethics declarations

    Conflict of interest. The authors declare that they have no conflicts of interest.

    Statement on the welfare of animals. The relevant experimental procedures of animals in this study followed the Animal Experiment Ethics Committee of Southwest University [2007 no. 3] and passed the China Animal Protection Law.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Zeng, SQ., Liu, CL., Huang, CN. et al. Identification of the Differential Expression Profile of miRNAs in Longissimus dorsi Muscle of Dazu Black Goat. Russ J Genet 58, 1385–1392 (2022). https://doi.org/10.1134/S102279542211014X

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1134/S102279542211014X

    Keywords:

    Search

    Navigation