Animal Bioscience

  • 제37권11호
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  • Pages.1848-1862
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  • 2024
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  • 2765-0189(pISSN)
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  • 2765-0235(eISSN)
아세아태평양축산학회 (Asian Australasian Association of Animal Production Societies)
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Asparagine synthetase regulates the proliferation and differentiation of chicken skeletal muscle satellite cells

  • Hangfeng Jin (Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University) ;
  • Han Wang (Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University) ;
  • Jianqing Wu (Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University) ;
  • Moran Hu (Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University) ;
  • Xiaolong Zhou (Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University) ;
  • Songbai Yang (Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University) ;
  • Ayong Zhao (Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University) ;
  • Ke He (Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine of Zhejiang A&F University)
  • 투고 : 2024.04.25
  • 심사 : 2024.07.10
  • 발행 : 2024.11.01
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초록

Objective: Asparagine synthetase (ASNS) is an aminotransferase responsible for the biosynthesis of aspartate by using aspartic acid and glutamine. ASNS is highly expressed in fast-growing broilers, but few studies have reported the regulatory role of ASNS in muscle development. Methods: To explore the function of ASNS in chicken muscle development, the expression of ASNS in different chicken breeds and tissues were first performed by real-time quantitative reverse transcription polymerase chain reaction (RT-PCR). Then, using real-time quantitative RT-PCR, western blot, EdU assay, cell cycle assay and immunofluorescence, the effects of ASNS on the proliferation and differentiation of chicken skeletal muscle satellite cell (SMSC) were investigated. Finally, potential mechanisms by which ASNS influences chicken muscle fiber differentiation were identified through RNA-Seq. Results: The mRNA expression pattern of ASNS in muscles mirrors trends in muscle fiber cross-sectional area, average daily weight gain, and muscle weight across different breeds. ASNS knockdown inhibited SMSC proliferation, while overexpression showed the opposite. Moreover, ASNS attenuated SMSC differentiation by activating the adenosine 5'-monophosphate (AMP)-activated protein kinase (AMPK) pathway. Additionally, 5-aminoimidazole-4-carboxamide1-β-D-ribofuranoside (AICAR) treatment suppressed the cell differentiation induced by siRNA-ASNS. RNA-Seq identified 1,968 differentially expressed genes (DEGs) during chicken SMSC differentiation when overexpression ASNS. Gene ontology (GO) enrichment analysis revealed that these DEGs primarily participated in 8 biological processes, 8 cellular components, and 4 molecular functions. Kyoto encyclopedia of genes and genomes (KEGG) pathway analysis identified several significantly enriched signaling pathways, such as the JAK-STAT signaling pathway, tumor necrosis factor signaling pathway, toll-like receptor signaling pathway, and PI3K-Akt signaling pathway. Conclusion: ASNS promotes proliferation while inhibits the differentiation of chicken SMSCs. This study provides a theoretical basis for studying the role of ASNS in muscle development.

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과제정보

This work was supported by the 'Pioneer' and 'Leading Goose' R&D Program of Zhejiang (2022C04014), the Technology Extension Project from Department of Agriculture and Rural Affairs of Zhejiang Province (H20230331) and Livestock Industry Technology Team Project of Zhejiang Province (H20240263). Han would like to thank the support of China Scholarship Council (No. 201908330130).

참고문헌

  1. Daughtry M, Berio E, Shen Z, et al. Satellite cell-mediated breast muscle regeneration decreases with broiler size. Poult Sci 2017;96:3457-64. https://doi.org/10.3382/ps/pex068
  2. Lomelino CL, Andring JT, McKenna R, Kilberg MS. Asparagine synthetase: function, structure, and role in disease. J Biol Chem 2017;292:19952-8. https://doi.org/10.1074/jbc.R117.819060
  3. Brown D, Ryan K, Daniel Z, et al. The Beta-adrenergic agonist, ractopamine, increases skeletal muscle expression of asparagine synthetase as part of an integrated stress response gene program. Sci Rep 2018;8:15915. https://doi.org/10.1038/s41598-018-34315-9
  4. Gao GL, Wang HW, Zhao XZ, et al. Feeding conditions and breed affect the level of DNA methylation of the mitochondrial uncoupling protein 3 gene in chicken breast muscle. J Anim Sci 2015;93:1522-34. https://doi.org/10.2527/jas.2014-8431
  5. Fang K, Chu Y, Zhao Z, et al. Enhanced expression of asparagine synthetase under glucose-deprived conditions promotes esophageal squamous cell carcinoma development. Int J Med Sci 2020;17:510-6. https://doi.org/10.7150/ijms.39557
  6. Deng L, Yao P, Li L, et al. P53-mediated control of aspartate-asparagine homeostasis dictates LKB1 activity and modulates cell survival. Nat Commun 2020;11:1755. https://doi.org/10.1038/s41467-020-15573-6
  7. Ye C, Zhang D, Zhao L, et al. CaMKK2 suppresses muscle regeneration through the inhibition of myoblast proliferation and differentiation. Int J Mol Sci 2016;17:1695. https://doi.org/10.3390/ijms17101695
  8. Kui H, Ran B, Yang M, et al. Gene expression profiles of specific chicken skeletal muscles. Sci Data 2022;9:552. https://doi.org/10.1038/s41597-022-01668-w
  9. Wang H, Hu M, Ding Z, et al. Phosphoglycerate dehydrogenase positively regulates the proliferation of chicken muscle cells. Poult Sci 2022;101:101805. https://doi.org/10.1016/j.psj.2022.101805
  10. Livak KJ, Schmittgen T. Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCt method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  11. Halevy O, Piestun Y, Allouh MZ, et al. Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 2004;231:489-502. https://doi.org/10.1002/dvdy.20151
  12. Zhai C, Huff-Lonergan EJ, Lonergan SM, Nair MN, Huff-Lonergan E. Housekeeping proteins in meat quality research: are they reliable markers for internal controls in western blot? a mini review. Meat Muscle Biol 2022;6:11551. http://doi.org/10.22175/mmb.11551
  13. Tan X, Liu R, Li W, et al. Assessment the effect of genomic selection and detection of selective signature in broilers. Poult Sci 2022;101:101856. https://doi.org/10.1016/j.psj.2022.101856
  14. Visnjic D, Lalic H, Dembitz V, Tomic B, Smoljo T. AICAr, a widely used AMPK activator with important AMPK-independent effects: a systematic review. Cells 2021;10:1095. https://doi.org/10.3390/cells10051095
  15. Mutryn MF, Brannick EM, Fu W, Lee WR, Abasht B. Characterization of a novel chicken muscle disorder through differential gene expression and pathway analysis using RNA-sequencing. BMC Genomics 2015;16:399. https://doi.org/10.1186/s12864-015-1623-0
  16. Hammond J. Animal breeding in relation to nutrition and environmental conditions. Biol Rev 1947;22:195-213. https://doi.org/10.1111/j.1469-185X.1947.tb00330.x
  17. Tsai WC, Yu TY, Lin LP, et al. Platelet rich plasma releasate promotes proliferation of skeletal muscle cells in association with upregulation of PCNA, cyclins and cyclin dependent kinases. Platelets 2017;28:491-7. https://doi.org/10.1080/09537104.2016.1227061
  18. Li H, Zhou F, Du W, et al. Knockdown of asparagine synthetase by RNAi suppresses cell growth in human melanoma cells and epidermoid carcinoma cells. Biotechnol Appl Biochem 2016;63:328-33. https://doi.org/10.1002/bab.1383
  19. Yang H, He X, Zheng Y, et al. Down-regulation of asparagine synthetase induces cell cycle arrest and inhibits cell proliferation of breast cancer. Chem Biol Drug Des 2014;84:578-84. https://doi.org/10.1111/cbdd.12348
  20. Brearley MC, Li C, Daniel Z, Loughna P, Parr T, Brameld JM. Changes in expression of serine biosynthesis and integrated stress response genes during myogenic differentiation of C2C12 cells. Biochem Biophys Rep 2019;20:100694. https://doi.org/10.1016/j.bbrep.2019.100694
  21. Williamson DL, Butler DC, Alway SE. AMPK inhibits myoblast differentiation through a PGC-1alpha-dependent mechanism. Am J Physiol Endocrinol Metab 2009;297:E304-14. https://doi.org/10.1152/ajpendo.91007.2008
  22. Barnes T, Sebastiano KMD, Vlavcheski F, Quadrilatero J, Tsiani EL, Mourtzakis M. Glutamate increases glucose uptake in L6 myotubes in a concentration- and time-dependent manner that is mediated by AMPK. Appl Physiol Nutr Metab 2018;43:1307-13. https://doi.org/10.1139/apnm-2018-0174
  23. Hu Z, Xu H, Lu Y, et al. MUSTN1 is an indispensable factor in the proliferation, differentiation and apoptosis of skeletal muscle satellite cells in chicken. Exp Cell Res 2021;407:112833. https://doi.org/10.1016/j.yexcr.2021.112833
  24. Burguiere AC, Nord H, von Hofsten J. Alkali-like myosin light chain-1 (myl1) is an early marker for differentiating fast muscle cells in zebrafish. Dev Dyn 2011;240:1856-63. https://doi.org/10.1002/dvdy.22677
  25. Ju Y, Li J, Xie C, et al. Troponin T3 expression in skeletal and smooth muscle is required for growth and postnatal survival: characterization of Tnnt3(tm2a(KOMP)Wtsi) mice. Genesis 2013;51:667-75. https://doi.org/10.1002/dvg.22407
  26. Aminizadeh S, Masoumi-Ardakani Y, Shahouzehi B. The effects of PDK4 inhibition on AMPK protein levels and PGC-1α gene expression following endurance training in skeletal muscle of Wistar rats. Ukr Biochem J 2018;90:89-96. https://doi.org/10.15407/ubj90.06.089
  27. Zhao TQ, Li Y, Zhang M, Zhao MC, Cao X, Hou SZ. Glycyrrhizic acid protects glomerular podocytes induced by high glucose by modulating SNARK/AMPK signaling pathway. Curr Med Sci 2023;43:696-707. https://doi.org/10.1007/s11596-023-2765-y
  28. Gustafsson T, Rundqvist H, Norrbom J, Rullman E, Jansson E, Sundberg CJ. The influence of physical training on the angiopoietin and VEGF-A systems in human skeletal muscle. J Appl Physiol 2007;103:1012-20. https://doi.org/10.1152/japplphysiol.01103.2006
  29. Ji Y, Li M, Chang M, et al. Inflammation: roles in skeletal muscle atrophy. Antioxidants 2022;11:1686. https://doi.org/10.3390/antiox11091686
  30. Han S, Cui C, He H, et al. FHL1 regulates myoblast differentiation and autophagy through its interaction with LC3. J Cell Physiol 2020;235:4667-78. https://doi.org/10.1002/jcp.29345
  31. Chenette DM, Cadwallader AB, Antwine TL, et al. Targeted mRNA decay by RNA binding protein AUF1 regulates adult muscle stem cell fate, promoting skeletal muscle integrity. Cell Rep 2016;16:1379-90. https://doi.org/10.1016/j.celrep.2016.06.095
  32. Zhang L, Zhang Y, Zhou M, et al. Role and mechanism underlying FoxO6 in skeletal muscle in vitro and in vivo. Int J Mol Med 2021;48:143. https://doi.org/10.3892/ijmm.2021.4976