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Muscle differentiation induced up-regulation of calcium-related gene expression in quail myoblasts

  • Park, Jeong-Woong (Institute of Green-Bio Science and Technology, Seoul National University) ;
  • Lee, Jeong Hyo (Institute of Green-Bio Science and Technology, Seoul National University) ;
  • Kim, Seo Woo (Graduate School of International Agricultural Technology, Seoul National University) ;
  • Han, Ji Seon (Graduate School of International Agricultural Technology, Seoul National University) ;
  • Kang, Kyung Soo (Bio Division, Medikinetics, Inc.) ;
  • Kim, Sung-Jo (Division of Cosmetics and Biotechnology, Hoseo University) ;
  • Park, Tae Sub (Institute of Green-Bio Science and Technology, Seoul National University)
  • Received : 2018.04.16
  • Accepted : 2018.05.29
  • Published : 2018.09.01

Abstract

Objective: In the poultry industry, the most important economic traits are meat quality and carcass yield. Thus, many studies were conducted to investigate the regulatory pathways during muscle differentiation. To gain insight of muscle differentiation mechanism during growth period, we identified and validated calcium-related genes which were highly expressed during muscle differentiation through mRNA sequencing analysis. Methods: We conducted next-generation-sequencing (NGS) analysis of mRNA from undifferentiated QM7 cells and differentiated QM7 cells (day 1 to day 3 of differentiation periods). Subsequently, we obtained calcium related genes related to muscle differentiation process and examined the expression patterns by quantitative reverse-transcription polymerase chain reaction (qRT-PCR). Results: Through RNA sequencing analysis, we found that the transcription levels of six genes (troponin C1, slow skeletal and cardiac type [TNNC1], myosin light chain 1 [MYL1], MYL3, phospholamban [PLN], caveolin 3 [CAV3], and calsequestrin 2 [CASQ2]) particularly related to calcium regulation were gradually increased according to days of myotube differentiation. Subsequently, we validated the expression patterns of calcium-related genes in quail myoblasts. These results indicated that TNNC1, MYL1, MYL3, PLN, CAV3, CASQ2 responded to differentiation and growth performance in quail muscle. Conclusion: These results indicated that calcium regulation might play a critical role in muscle differentiation. Thus, these findings suggest that further studies would be warranted to investigate the role of calcium ion in muscle differentiation and could provide a useful biomarker for muscle differentiation and growth.

Keywords

References

  1. Van Kaam JB, Groenen MA, Bovenhuis H, et al. Whole genome scan in chickens for quantitative trait loci affecting growth and feed efficiency. Poult Sci 1999;78:15-23. https://doi.org/10.1093/ps/78.1.15
  2. Yaffe D. Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci USA 1968;61;477-83. https://doi.org/10.1073/pnas.61.2.477
  3. Arnold HH, Winter B. Muscle differentiation: more complexity to the network of myogenic regulators. Curr Opin Genet Dev 1998;8:539-44. https://doi.org/10.1016/S0959-437X(98)80008-7
  4. Kim SW, Lee JH, Park BC, Park TS. Myotube differentiation in clustered regularly interspaced short palindromic repeat/Cas9-mediated MyoD knockout quail myoblast cells. Asian-Australas J Anim Sci 2017;30:1029-36.
  5. Kim SW, Lee JH, Park TS. Functional analysis of SH3 domain containing ring finger 2 during the myogenic differentiation of quail myoblast cells. Asian-Australas J Anim Sci 2017;30:1183-9.
  6. Kerst B, Mennerich D, Schuelke M. et al. Heterozygous myogenic factor 6 mutation associated with myopathy and severe course of Becker muscular dystrophy. Neuromuscul Disord 2000;10:572-7. https://doi.org/10.1016/S0960-8966(00)00150-4
  7. Miner JH, Wold B. Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc Natl Acad Sci USA 1990;87:1089-93. https://doi.org/10.1073/pnas.87.3.1089
  8. Buckingham M, Rigby PW. Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev Cell 2014:28:225-38. https://doi.org/10.1016/j.devcel.2013.12.020
  9. Lansdown AB. Calcium: a potential central regulator in wound healing in the skin. Wound Repair Regen 2002;10:271-85. https://doi.org/10.1046/j.1524-475X.2002.10502.x
  10. Tharin S, Hamel PA, Conway EM, et al. Regulation of calcium binding proteins calreticulin and calsequestrin during differentiation in the myogenic cell line L6. J Cell Physiol 1996;166:547-60. https://doi.org/10.1002/(SICI)1097-4652(199603)166:3<547::AID-JCP9>3.0.CO;2-P
  11. Ledoux J, Werner ME, Brayden J, et al. Calcium-activated potassium channels and the regulation of vascular tone. Physiology 2006;21:69-78. https://doi.org/10.1152/physiol.00040.2005
  12. Ohtsuki I, Maruyama K, Ebashi S. Regulatory and cytoskeletal proteins of vertebrate skeletal muscle. Adv Protein Chem 1986; 38:1-67.
  13. Rees DD, Frederiksen DW. Calcium regulation of porcine aortic myosin. J Biol Chem 1981;256:357-64.
  14. Orrenius S, Zhivotovsky B, Nicotera P. Calcium: Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003;4:552-65. https://doi.org/10.1038/nrm1150
  15. Westerblad H, Bruton JD, Katz A. Skeletal muscle: energy metabolism, fiber types, fatigue and adaptability. Exp Cell Res 2010;316:3093-9. https://doi.org/10.1016/j.yexcr.2010.05.019
  16. Musaro A, McCullagh KJ, Naya FJ, et al. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 1999;400:581-5. https://doi.org/10.1038/23060
  17. Kay BK, Shah AJ, Halstead WE. Expression of the Ca2+-binding protein, parvalbumin, during embryonic development of the frog, Xenopus laevis. J Cell Biol 1987;104:841-7. https://doi.org/10.1083/jcb.104.4.841
  18. Schwartz LM, Kay BK. Differential expression of the $Ca^{2+}$-binding protein parvalbumin during myogenesis in Xenopus laevis. Dev Biol 1988;128:441-52. https://doi.org/10.1016/0012-1606(88)90306-5
  19. Heizmann CW, Strehler EE. Chicken parvalbumin. Comparison with parvalbumin-like protein and three other components (Mr= 8,000 to 13,000). J Biol Chem 1979;254:4296-303.
  20. Froemming GR, Ohlendieck K. Oligomerisation of $Ca^{2+}$-regulatory membrane components involved in the excitationcontraction-relaxation cycle during postnatal development of rabbit skeletal muscle. Biochim Biophys Acta Protein Structure and Molecular Enzymology 1998;1387:226-38. https://doi.org/10.1016/S0167-4838(98)00126-5
  21. Billeter R, Quitschke W, Paterson BM. Approximately 1 kilobase of sequence 5'to the two myosin light-chain 1f/3f gene cap sites is sufficient for differentiation-dependent expression. Mol Cell Biol 1988;8:1361-5. https://doi.org/10.1128/MCB.8.3.1361
  22. 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
  23. Bitard-Feildel T, Kemena C, Greenwood JM, Bornberg-Bauer E. Domain similarity based orthology detection. BMC Bioinformatics 2015;16:154. https://doi.org/10.1186/s12859-015-0570-8
  24. Parton RG, Way M, Zorzi N, et al. Caveolin-3 associates with developing T-tubules during muscle differentiation. J Cell Biol 1997;136:137-54. https://doi.org/10.1083/jcb.136.1.137
  25. Fliegel L, Ohnishi M, Carpenter MR, et al. Amino acid sequence of rabbit fast-twitch skeletal muscle calsequestrin deduced from cDNA and peptide sequencing. Proc Natl Acad Sci USA 1987;84:1167-71. https://doi.org/10.1073/pnas.84.5.1167
  26. Devlin RB, Emerson Jr, CP. Coordinate regulation of contractile protein synthesis during myoblast differentiation. Cell 1978;13:599-611. https://doi.org/10.1016/0092-8674(78)90211-8

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