Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Investigation of single nucleotide polymorphisms in differentially expressed genes and proteins reveals the genetic basis of skeletal muscle growth differences between Tibetan and Large White pigs

  • Heli Xiong (Animal Nutrition and Swine Institute, Yunnan Academy of Animal Husbandry and Veterinary Sciences) ;
  • Yan Zhang (Animal Nutrition and Swine Institute, Yunnan Academy of Animal Husbandry and Veterinary Sciences) ;
  • Zhiyong Zhao (Animal Nutrition and Swine Institute, Yunnan Academy of Animal Husbandry and Veterinary Sciences)
  • Received : 2024.03.05
  • Accepted : 2024.06.07
  • Published : 2024.12.01
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Abstract

Objective: Skeletal muscle growth is an important economic trait for meat production, with notable differences between Tibetan pigs (TIBPs, a slow-growing breed) and Large White pigs (LWPs, a fast-growing breed). However, the genetic underpinnings of this disparity remain unclear. Methods: In the current study, we integrated differentially expressed genes (DEGs) and proteins (DEPs) from 60-day-old embryonic muscle tissue, along with whole-genome single nucleotide polymorphisms (SNPs) displaying absolute allele frequency differences (ΔAF) of 0.5 or more between the TIBP and LWP breeds, to unravel the genetic factors influencing skeletal muscle growth. Results: Our analysis revealed 3,499 DEGs and 628 DEPs with SNPs having a ΔAF equal to or greater than 0.5. Further functional analysis identified 145 DEGs and 23 DEPs involved in biological processes related to skeletal muscle development, and 22 DEGs and 3 DEPs implicated in the mechanistic target of rapamycin kinase signaling pathway, which is known for positively regulating protein synthesis. Among these genes, several DEGs and DEPs, enriched with TIPB-specific SNPs in regulatory or/and coding regions, showed marked ΔAF between the TIBP and LWP breeds, including MYF5, MYOF, ASB2, PDE9A, SDC1, PDGFRA, MYOM2, ACVR1, ZIC3, COL11A1, TGFBR1, EDNRA, TGFB2, PDE4D, PGAM2, GRK2, SCN4B, CACNA1S, MYL4, IGF1, and FOXO1. Additionally, genes such as CAPN3, MYOM2, and PGAM2, identified as both DEPs and DEGs related to skeletal muscle development, contained multiple TIBP-specific and LWP-predominant SNPs in regulatory and/or coding regions, underscoring significant ΔAF differences between the two breeds. Conclusion: This comprehensive investigation of SNPs in DEGs and DEPs identified a significant number of SNPs and genes related to skeletal muscle development during the prenatal stage. These findings not only shed light on potential causal genes for muscle divergence between the TIBP and LWP breeds but also offer valuable insights for pig breeding strategies aimed at enhancing meat production.

Keywords

Acknowledgement

We sincerely appreciate the researchers who shared tran-scriptome and proteome data of the 60-day-old embryonic muscle tissues from Tibetan and Large White pigs.

References

  1. Zappaterra M, Gioiosa S, Chillemi G, Zambonelli P, Davoli R. Muscle transcriptome analysis identifies genes involved in ciliogenesis and the molecular cascade associated with intramuscular fat content in Large White heavy pigs. PLoS ONE 2020;15:e0233372. https://doi.org/10.1371/journal.pone.0233372
  2. Dwyer CM, Fletcher JM, Stickland NC. Muscle cellularity and postnatal growth in the pig. J Anim Sci 1993;71:3339-43. https://doi.org/10.2527/1993.71123339x
  3. Stickland NC, Handel SE. The numbers and types of muscle fibres in large and small breeds of pigs. J Anat 1986;147:181-9.
  4. Zhao X, Mo DL, Li AN, et al. Comparative analyses by sequencing of transcriptomes during skeletal muscle development between pig breeds differing in muscle growth rate and fatness. PLoS ONE 2011;6:e19774. https://doi.org/10.1371/journal.pone.0019774
  5. Picard B, Lefaucheur L, Berri C, Duclos MJ. Muscle fibre ontogenesis in farm animal species. Reprod Nutr Dev 2002;42:415-31. https://doi.org/10.1051/rnd:2002035
  6. Bharathy N, Ling BMT, Taneja R. Epigenetic regulation of skeletal muscle development and differentiation. In: Kundu TK, editor. Epigenetics: development and disease. Subcellular biochemistry. Dordrecht, The Netherlands: Springer; 2013. pp. 139-50. https://doi.org/10.1007/978-94-007-4525-4_7
  7. Brand-Saberi B, Christ B. Genetic and epigenetic control of muscle development in vertebrates. Cell Tissue Res 1999;296:199-212. https://doi.org/10.1007/s004410051281
  8. Ludolph DC, Konieczny SF. Transcription factor families: muscling in on the myogenic program. FASEB J 1995;9:1595. https://doi.org/10.1096/fasebj.9.15.8529839
  9. Oksbjerg N, Gondret F, Vestergaard M. Basic principles of muscle development and growth in meat-producing mammals as affected by the insulin-like growth factor (IGF) system. Domest Anim Endocrinol 2004;27:219-40. https://doi.org/10.1016/j.domaniend.2004.06.007
  10. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 2013;280:4294-314. https://doi.org/10.1111/febs.12253
  11. Schiaffino S, Reggiani C, Akimoto T, Blaauw B. Molecular mechanisms of skeletal muscle hypertrophy. J Neuromuscul Dis 2021;8:169-83. https://doi.org/10.3233/jnd-200568
  12. Zhang X, Chen Y, Pan J, et al. iTRAQ-based quantitative proteomic analysis reveals the distinct early embryo myofiber type characteristics involved in landrace and miniature pig. BMC Genomics 2016;17:137. https://doi.org/10.1186/s12864-016-2464-1
  13. Cagnazzo M, te Pas MFW, Priem J, et al. Comparison of prenatal muscle tissue expression profiles of two pig breeds differing in muscle characteristics. J Anim Sci 2006;84:1-10. https://doi.org/10.2527/2006.8411
  14. Davoli R, Braglia S, Russo V, Varona L, te Pas MFW. Expression profiling of functional genes in prenatal skeletal muscle tissue in Duroc and Pietrain pigs. J Anim Breed Genet 2011;128:15-27. https://doi.org/10.1111/j.1439-0388.2010.00867.x
  15. Wang LY, Li XX, Ma J, Zhang YW, Zhang H. Integrating genome and transcriptome profiling for elucidating the mechanism of muscle growth and lipid deposition in Pekin ducks. Sci Rep 2017;7:3837. https://doi.org/10.1038/s41598-017-04178-7
  16. Shang P, Wang ZX, Chamba YZ, Zhang B, Zhang H, Wu C. A comparison of prenatal muscle transcriptome and proteome profiles between pigs with divergent growth phenotypes. J Cell Biochem 2019;120:5277-86. https://doi.org/10.1002/jcb.27802
  17. Kolberg L, Raudvere U, Kuzmin I, Vilo J, Peterson H. gprofiler2 -- an R package for gene list functional enrichment analysis and namespace conversion toolset g:profiler. F1000Res 2020;9:709. https://doi.org/10.12688/f1000research.24956.2
  18. Yang CC, Gong AF. Integrated bioinformatics analysis for differentially expressed genes and signaling pathways identification in gastric cancer. Int J Med Sci 2021;18:792-800. https://doi.org/10.7150/ijms.47339
  19. Thomson DM. The role of AMPK in the regulation of skeletal muscle size, hypertrophy, and regeneration. Int J Mol Sci 2018;19:3125. https://doi.org/10.3390/ijms19103125
  20. Yoshida T, Delafontaine P. Mechanisms of IGF-1-mediated regulation of skeletal muscle hypertrophy and atrophy. Cells 2020;9:1970. https://doi.org/10.3390/cells9091970
  21. Lebrasseur NK, Cote GM, Miller TA, Fielding RA, Sawyer DB. Regulation of neuregulin/ErbB signaling by contractile activity in skeletal muscle. Am J Physiol Cell Physiol 2003;284:C1149-55. https://doi.org/10.1152/ajpcell.00487.2002
  22. Majmundar AJ, Lee DSM, Skuli N, et al. HIF modulation of Wnt signaling regulates skeletal myogenesisin vivo. Development 2015;142:2405-12. https://doi.org/10.1242/dev.123026
  23. Guo Y, Wang M, Ge J, et al. Bioactive biodegradable poly-citrate nanoclusters enhances the myoblast differentiation and in vivo skeletal muscle regeneration via p38 MAPK signaling pathway. Bioact Mater 2020;5:486-95. https://doi.org/10.1016/j.bioactmat.2020.04.004
  24. Park JW, Lee JH, Han JS, Shin SP, Park TS. Muscle differentiation induced by p53 signaling pathway-related genes in myostatin-knockout quail myoblasts. Mol Biol Rep 2020;47:9531-40. https://doi.org/10.1007/s11033-020-05935-0
  25. Adolf IC, Almars A, Dharsee N, et al. HLA-G and single nucleotide polymorphism (SNP) associations with cancer in African populations: implications in personal medicine. Genes Dis 2021;9:1220-33. https://doi.org/10.1016/j.gendis.2021.06.004
  26. Hecht M, Bromberg Y, Rost B. News from the protein mutability landscape. J Mol Biol 2013;425:3937-48. https://doi.org/10.1016/j.jmb.2013.07.028
  27. Bartoszewski R, Kroliczewski J, Piotrowski A, et al. Codon bias and the folding dynamics of the cystic fibrosis transmembrane conductance regulator. Cell Mol Biol Lett 2016;21:23. https://doi.org/10.1186/s11658-016-0025-x
  28. Garcia-Guerra L, Vila-Bedmar R, Carrasco-Rando M, et al. Skeletal muscle myogenesis is regulated by G protein-coupled receptor kinase 2. J Mol Cell Biol 2014;6:299-311. https://doi.org/10.1093/jmcb/mju025
  29. Davey JR, Watt KI, Parker BL, et al. Integrated expression analysis of muscle hypertrophy identifies Asb2 as a negative regulator of muscle mass. JCI Insight 2016;1:e85477. https://doi.org/10.1172/jci.insight.85477
  30. Helinska A, Krupa M, Archacka K, et al. Myogenic potential of mouse embryonic stem cells lacking functional Pax7 tested in vitro by 5-azacitidine treatment and in vivo in regenerating skeletal muscle. Eur J Cell Biol 2017;96:47-60. https://doi.org/10.1016/j.ejcb.2016.12.001
  31. Chan SSK, Hagen HR, Swanson SA, et al. Development of bipotent cardiac/skeletal myogenic progenitors from MESP1+ mesoderm. Stem Cell Rep 2016;6:26-34. https://doi.org/10.1016/j.stemcr.2015.12.003
  32. Stanley A, Tichy ED, Kocan J, Roberts DW, Shore EM, Mourkioti F. Dynamics of skeletal muscle-resident stem cells during myogenesis in fibrodysplasia ossificans progressiva. NPJ Regen Med 2022;7:5. https://doi.org/10.1038/s41536-021-00201-8
  33. Zhang Y, Beketaev I, Ma YL, Wang J. Sumoylation-deficient phosphoglycerate mutase 2 impairs myogenic differentiation. Front Cell Dev Biol 2022;10:1052363. https://doi.org/10.3389/fcell.2022.1052363
  34. Xu M, Chen X, Chen D, Yu B, Huang Z. FoxO1: a novel insight into its molecular mechanisms in the regulation of skeletal muscle differentiation and fiber type specification. Oncotarget 2017;8:10662-74. https://doi.org/10.18632/oncotarget.12891
  35. Zhang L, Zhou Q, Zhang J, et al. Liver transcriptomic and proteomic analyses provide new insight into the pathogenesis of liver fibrosis in mice. Genomics 2023;115:110738. https://doi.org/10.1016/j.ygeno.2023.110738
  36. Chen L, Tang F, Gao H, Zhang X, Li X, Xiao D. CAPN3: a muscle-specific calpain with an important role in the pathogenesis of diseases (Review). Int J Mol Med 2021;48:203. https://doi.org/10.3892/ijmm.2021.5036
  37. Lamber EP, Guicheney P, Pinotsis N. The role of the M-band myomesin proteins in muscle integrity and cardiac disease. J Biomed Sci 2022;29:18. https://doi.org/10.1186/s12929-022-00801-6
  38. Pearson AM. Muscle growth and exercise. Crit Rev Food Sci Nutr 1990;29:167-96. https://doi.org/10.1080/10408399009527522
  39. Rehfeldt C, Te Pas MFW, Wimmers K, et al. Advances in research on the prenatal development of skeletal muscle in animals in relation to the quality of muscle-based food. I. regulation of myogenesis and environmental impact. Animal 2011;5:703-17. https://doi.org/10.1017/s1751731110002089