DOI QR코드

DOI QR Code

Cloning and characterization of a cDNA encoding a paired box protein, PAX7, from black sea bream, Acanthopagrus schlegelii

  • Choi, Jae Hoon (Department of Fisheries Biology, Pukyong National University) ;
  • Han, Dan Hee (Department of Fisheries Biology, Pukyong National University) ;
  • Gong, Seung Pyo (Department of Fisheries Biology, Pukyong National University)
  • Received : 2021.12.03
  • Accepted : 2021.12.17
  • Published : 2021.12.31

Abstract

Paired box protein, PAX7, is a key molecule for the specification, maintenance and skeletal muscle regeneration of muscle satellite cells. In this study, we identified and characterized the cDNA and amino acid sequences of PAX7 from black sea bream (Acanthopagrus schlegelii) via molecular cloning and sequence analysis. A. schlegelii PAX7 cDNA was comprised of 1,524 bp encoding 507 amino acids and multiple sequence alignment analysis of the translated amino acids showed that it contained three domains including paired DNA-binding domain, homeobox domain and OAR domain which were well conserved across various animal species investigated. Pairwise Sequence Alignment indicated that A. schlegelii PAX7 had the same amino acid sequences with that of yellowfin seabream (A. latus) and 99.8% identity and similarity with that of gilt-head bream (Sparus aurata). Molecular phylogenetic analysis confirmed that A. schlegelii PAX7 formed a monophyletic group with those of teleost and most closely related with those of the fish that belong to Sparidae family including A. latus and S. aurata. In the investigation of its tissue specific mRNA expression, the expression was specifically identified in skeletal muscle tissue and a weak expression was also shown in gonad tissue. The cultured cells derived from skeletal muscle tissues expressed PAX7 mRNA at early passage but the expression was not observed after several times of subculture.

Keywords

Acknowledgement

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2021R1I1A3041760).

References

  1. Aloisio GM, Nakada Y, Saatcioglu HD, Pena CG, Baker MD, Tarnawa ED, Mukherjee J, Manjunath H, Bugde A, Sengupta AL, Amatruda JF, Cuevas I, Castrillon DH. 2014. PAX7 expression defines germline stem cells in the adult testis. J. Clin. Invest. 124:3929-3944. https://doi.org/10.1172/JCI75943
  2. Berberoglu MA, Gallagher TL, Morrow ZT, Talbot JC, Hromowyk KJ, Tenente IM, Amacher SL. 2017. Satellite-like cells contribute to pax7-dependent skeletal muscle repair in adult zebrafish. Dev. Biol. 424:162-180. https://doi.org/10.1016/j.ydbio.2017.03.004
  3. Bischoff R and Heintz C. 1994. Enhancement of skeletal muscle regeneration. Dev. Dyn. 201:41-54. https://doi.org/10.1002/aja.1002010105
  4. Brzoska E, Przewozniak M, Grabowska I, Moraczewski J. 2009. Pax3 and Pax7 expression during myoblast differentiation in vitro and fast and slow muscle regeneration in vivo. Cell Biol. Int. 33:483-492. https://doi.org/10.1016/j.cellbi.2008.11.015
  5. Chapalamadugu KC, Murdoch BM, Robison BD, Murdoch GK. 2015. Oncorhynchus mykiss pax7 sequence variations with comparative analyses against other teleost species. Springerplus 4:263. https://doi.org/10.1186/s40064-015-1030-7
  6. Choi KH, Yoon JW, Kim M, Jeong J, Ryu M, Park S, Lee CK. 2020. Optimization of culture conditions for maintaining pig muscle stem cells in vitro. Food Sci. Anim. Resour. 40:659-667. https://doi.org/10.5851/kosfa.2020.e39
  7. Ding S, Wang F, Liu Y, Li S, Hu P. 2017. Characterization and isolation of highly purified porcine satellite cells. Cell Death Discov. 3:17003. https://doi.org/10.1038/cddiscovery.2017.3
  8. Du X, Wu S, Wei Y, Yu X, Ma F, Zhai Y, Yang D, Zhang M, Liu W, Zhu H, Wu J, Liao M, Li N, Bai C, Hua J. 2021. PAX7 promotes CD49f-positive dairy goat spermatogonial stem cells' self-renewal. J. Cell. Physiol. 236:1481-1493. https://doi.org/10.1002/jcp.29954
  9. Dumont NA, Rudnicki MA. 2015. Intrinsic and extrinsic mechanisms regulating satellite cell function. Development 142:1572-1581. https://doi.org/10.1242/dev.114223
  10. Fan Q, Li D, Cai L, Qiu X, Zhao Z, Wu J, Lu Y. 2019. A novel mutation in the OAR domain of PITX3 associated with congenital posterior subcapsular cataract. BMC Med. Genet. 20:42. https://doi.org/10.1186/s12881-019-0782-2
  11. Codina M, Capilla E, Jimenez-Amilburu V, Navarro I, Du SJ, Gutierrez J; Garcia de la serrana D. 2014. Characterisation and expression of myogenesis regulatory factors during in vitro myoblast development and in vivo fasting in the gilthead sea bream (Sparus aurata). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 167:90-99. https://doi.org/10.1016/j.cbpa.2013.10.020
  12. Halevy O, Piestun Y, Allouh MZ, Rosser BW, Rinkevich Y, Reshef R, Rozenboim I, Yablonka-Reuveni Z. 2004. Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev. Dyn. 231:489-502. https://doi.org/10.1002/dvdy.20151
  13. Huang JD, Chang CF. 2002. The morphology of gonadal tissue and male germ cells in the protandrous black porgy, Acanthopagrus schlegeli. Zool. Stud. 41:216-227.
  14. Jun S and Desplan C. 1996. Cooperative interactions between paired domain and homeodomain. Development 122:2639-2650. https://doi.org/10.1242/dev.122.9.2639
  15. Kwon HC, Zhang CI, Shin YJ, Kim KH, Seo YI. 2009. Maturation and spawning of black seabream Acanthopagrus schlegeli in the southern sea of Korea. Korean J. Ichthyol. 21:93-99.
  16. Mayran A, Drouin J. 2015. Pax factors in transcription and epigenetic remodelling. Semin. Cell Dev. Biol. 44:135-144. https://doi.org/10.1016/j.semcdb.2015.07.007
  17. Montarras D, Buckingham M. 2013. Lying low but ready for action: the quiescent muscle satellite cell. FEBS J. 280:4036-4050. https://doi.org/10.1111/febs.12372
  18. Nicklas S, Otto A, Wu X, Miller P, Stelzer S, Wen Y, Kuang S, Wrogemann K, Patel K, Schwamborn JC. 2012. TRIM32 regulates skeletal muscle stem cell differentiation and is necessary for normal adult muscle regeneration. PLoS One 7:e30445. https://doi.org/10.1371/journal.pone.0030445
  19. Pawlikowski B, Lee L, Kramer RH. 2009. Analysis of human muscle stem cells reveals a differentiation-resistant progenitor cell population expressing Pax7 capable of self-renewal. Dev. Dyn. 238:138-149. https://doi.org/10.1002/dvdy.21833
  20. Pelletier A, Mayran A, Gouhier A, Omichinski JG, Drouin J. 2021. Pax7 pioneer factor action requires both paired and homeo DNA binding domains. Nucleic Acids Res. 49:7424-7436. https://doi.org/10.1093/nar/gkab561
  21. Ramirez-Espinosa JJ, Gonzalez-Davalos L, Shimada A, Pina E, Mora O. 2016. Bovine (Bos taurus) bone marrow mesenchymal cell differentiation to adipogenic and myogenic lineages. Cells Tissues Organs 201:51-64. https://doi.org/10.1159/000440878
  22. Rudnicki MA and Jaenisch R. 1995. The MyoD family of transcription factors and skeletal myogenesis. Bioessays 17:203-209. https://doi.org/10.1002/bies.950170306
  23. Seger C, Hargrave M, Wang X, Chai RJ, Ingham PW. 2011. Analysis of Pax7 expressing myogenic cells in zebrafish muscle development, injury, and models of disease. Dev. Dyn. 240:2440-2451. https://doi.org/10.1002/dvdy.22745
  24. Shi X and Garry DJ. 2006. Muscle stem cells in development, regeneration, and disease. Genes Dev. 20:1692-1708. https://doi.org/10.1101/gad.1419406
  25. Underhill DA and Gros P. 1997. The paired-domain regulates DNA binding by the homeodomain within the intact Pax-3 protein. J. Biol. Chem. 272:14175-14182. https://doi.org/10.1074/jbc.272.22.14175
  26. von Maltzahn J, Jones AE, Rudnicki MA. 2013. Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 110:16474-16479. https://doi.org/10.1073/pnas.1307680110
  27. Wang L, Zhang W, Gladstone S, Ng WK, Shao Q. 2019. Effects of isoenergetic diets with varying protein and lipid levels on the growth, feed utilization, metabolic enzymes activities, antioxidative status and serum biochemical parameters of black sea bream (Acanthopagrus schlegelii). Aquaculture 513:734397. https://doi.org/10.1016/j.aquaculture.2019.734397
  28. Weber CM, Martindale MQ, Unguez GA. 2012. Activation of Pax7-positive cells in a non-contractile tissue contributes to regeneration of myogenic tissues in the electric fish S. macrurus. PLoS One 7:e36819. https://doi.org/10.1371/journal.pone.0036819
  29. Wu GC, Chang CF. 2021. Molecular and cellular regulation on sex change in hermaphroditic fish, with a special focus on protandrous black porgy, Acanthopagrus schlegelii. Mol. Cell. Endocrinol. 520:111069. https://doi.org/10.1016/j.mce.2020.111069
  30. Zammit P and Beauchamp J. 2001. The skeletal muscle satellite cell: stem cell or son of stem cell? Differentiation 68:193-204. https://doi.org/10.1046/j.1432-0436.2001.680407.x
  31. Zaret KS and Carroll JS. 2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25:2227-2241. https://doi.org/10.1101/gad.176826.111
  32. Zhou F, Shao Q, Xiao J, Peng X, Ngandzali BO, Ng WK. 2011. Effects of dietary arginine and lysine levels on growth performance, nutrient utilization and tissue biochemical profile of black sea bream, Acanthopagrus schlegelii, fingerlings. Aquaculture 319:72-80. https://doi.org/10.1016/j.aquaculture.2011.06.001