Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Effect of Sex Steroid Hormones on Bovine Myogenic Satellite Cell Proliferation, Differentiation and Lipid Accumulation in Myotube

  • Lee, E.J. (School of Biotechnology, Yeungnam University) ;
  • Bajracharya, P. (School of Biotechnology, Yeungnam University) ;
  • Jang, E.J. (School of Biotechnology, Yeungnam University) ;
  • Chang, J.S. (Department of Agricultural Sciences, Korea National Open University) ;
  • Lee, H.J. (National Livestock Research Institute) ;
  • Hong, S.K. (National Livestock Research Institute) ;
  • Choi, I. (School of Biotechnology, Yeungnam University)
  • Received : 2009.04.10
  • Accepted : 2009.10.08
  • Published : 2010.05.01
Download PDF
⟨ Previous Next ⟩

Abstract

Myogenic satellite cells (MSCs) are adult stem cells that activate and differentiate into myotubes. These stem cells are multipotent as they transdifferentiate into adipocyte-like cells, nerve cells and osteocytes. The effects of steroid hormones ($E_2$ and testosterone) were studied as a further step toward understanding the mechanism of MSCs proliferation and differentiation. In this study, MSCs were grown continuously for 87 days, implying that there may be a group of MSCs that continue to proliferate rather than undergoing differentiation. Isolated MSCs were cultured in Dulbecco's Modified Eagle's Medium supplemented with adult male, female or castrated bovine serum to observe the effect of steroid hormones on MSC proliferation. Cell proliferation was the highest in cultures supplemented with male serum followed by female and castrated serum. The positive effect of male hormone on MSC proliferation was confirmed by the observation of testosterone-mediated increased proliferation of cells cultured in medium supplemented with castrated serum. Furthermore, steroid hormone treatment of MSCs increased lipid accumulation in myotubes. Oil-Red-O staining showed that 17${\beta}$-estradiol ($E_2$) treatment avidly increased lipid accumulation, followed by $E_2$+testosterone and testosterone alone. To our knowledge, this is the first report of lipid accumulation in myotubes due to steroids in the absence of an adipogenic environment, and the effect of steroid hormones on cell proliferation using different types of adult bovine serum, a natural hormonal system. In conclusion, we found that sex steroids affect MSCs proliferation and differentiation, and lipid accumulation in myotubes.

Keywords

References

  1. Allen, R. E. and L. L. Rankin. 1990. Regulation of satellite cells during skeletal muscle growth and development. Proc. Soc. Exp. Biol. Med. 194:81-86
  2. Allen, D. M., L. E. Chen, A. V. Seaber and J. R. Urbaniak. 1997. Calcitonin gene-related peptide and reperfusion injury. J. Orthop. Res. 15:243-248 https://doi.org/10.1002/jor.1100150213
  3. Arnold, A. M., J. M. Peralta and M. L. Thonney. 1996. Ontogeny of growth hormone, insulin-like growth factor-I, estradiol and cortisol in the growing lamb: effect of testosterone. J. Endocrinol. 150:391-399 https://doi.org/10.1677/joe.0.1500391
  4. Asakura, A., M. Komaki and M. Rudnicki. 2001. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68:245-253 https://doi.org/10.1046/j.1432-0436.2001.680412.x
  5. Asakura, A., P. Seale, A. Girgis-Gabardo and M. A. Rudnicki. 2002. Myogenic specification of side population cells in skeletal muscle. J. Cell Biol. 159:123-134 https://doi.org/10.1083/jcb.200202092
  6. Bischoff, R. and C. Heintz. 1994. Enhancement of skeletal muscle regeneration. Dev. Dyn. 201:41-54 https://doi.org/10.1002/aja.1002010105
  7. Boland, R., A. Vasconsuelo, L. Milanesi, A. C. Ronda and A. R. de Boland. 2008. 17beta-estradiol signaling in skeletal muscle cells and its relationship to apoptosis. Steroids 73:859-863 https://doi.org/10.1016/j.steroids.2007.12.027
  8. Buckingham, M., L. Bajard, T. Chang, P. Daubas, J. Hadchouel, S. Meilhac, D. Montarras, J. Hadchouel, S. Meilhac, D. Montarras, D. Rocancourt and F. Relaix. 2003. The formation of skeletal muscle: from somite to limb. J. Anat. 202:59-68 https://doi.org/10.1046/j.1469-7580.2003.00139.x
  9. Chen, J. C. and D. J. Goldhamer. 2003. Skeletal muscle stem cells. Reprod. Biol. Endocrinol. 13(1):101
  10. Choi, I., L. J. Gudas and B. S. Katzenellenbogen. 2000. Regulation of keratin 19 gene expression by estrogen in human breast cancer cells and identification of the estrogen responsive gene region. Mol. Cell Endocrinol. 164:225-237 https://doi.org/10.1016/S0303-7207(00)00197-0
  11. Cornelison, D. D. and B. J. Wold. 1997. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 191:270-283 https://doi.org/10.1006/dbio.1997.8721
  12. Costa, M. L., R. Escaleira, A. Cataldo, F. Oliveira and C. S. Mermelstein. 2004. Desmin: molecular interactions and putative functions of the muscle intermediate filament protein. Braz. J. Med. Biol. Res. 37:1819-1830 https://doi.org/10.1590/S0100-879X2004001200007
  13. Dehm, S. M. and D. J. Tindall. 2007. Androgen receptor structural and functional elements: role and regulation in prostate cancer. Mol. Endocrinol. 21:2855-2863 https://doi.org/10.1210/me.2007-0223
  14. Enns, D. L., S. Iqbal and P. M. Tiidus. 2008. Oestrogen receptors mediate oestrogen-induced increases in post-exercise rat skeletal muscle satellite cells. Acta. Physiol. 194:81-93 https://doi.org/10.1111/j.1748-1716.2008.01861.x
  15. Fux, C., B. Mitta, B. P. Kramer and M. Fussenegger. 2004. Dualregulated expression of C/EBP-alpha and BMP-2 enables differential differentiation of C2C12 cells into adipocytes and osteoblasts. Nucleic Acids Res. 2;32:e1 https://doi.org/10.1093/nar/gnh001
  16. Garriga, J., E. Adanero, J. Fernandez-Sola, A. Urbano-Marquez and R. Cusso. 2000. Ethanol inhibits skeletal muscle cell proliferation and delays its differentiation in cell culture. Alcohol and Alcohol. 35:236-241 https://doi.org/10.1093/alcalc/35.3.236
  17. Goodpaster, B. H. and D. E. Kelley. 1998. Role of muscle in triglyceride metabolism. Curr. Opin. Lipidol. 9:231-236 https://doi.org/10.1097/00041433-199806000-00008
  18. Gupta, V., S. Bhasin, W. Guo, R. Singh, R. Miki, P. Chauhan, K. Choong, T. Tchkonia, N. K. Lebrasseur, J. N. Flanagan, J. A. Hamilton, J. C. Viereck, N. S. Narula, J. L. Kirkland and R. Jasuja. 2008. Effects of dihydrotestosterone on differentiation and proliferation of human mesenchymal stem cells and preadipocytes. Mol. Cell. Endocrinol. 16:32-40 https://doi.org/10.1016/j.mce.2008.08.019
  19. Hasty, P., A. Bradley, J. H. Morris, D. G. Edmondson, J. M. Venuti, E. N. Olson and W. H. Klein. 1993. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 5:501-506 https://doi.org/10.1038/364501a0
  20. Hawke, T. J. and D. J. Garry. 2001. Myogenic satellite cells:physiology to molecular biology. J. Appl. Physiol. 91:534-551
  21. Heine, P. A., J. A. Taylor, G. A. Iwamoto, D. B. Lubahn and P. S. Cooke. 2000. Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc. Natl. Acad. Sci. USA. 7:12729-12734
  22. Hu, E., P. Tontonoz and B. M. Spiegelman. 1995. Transdifferentiation of myoblasts by the adipogenic transcription factors PPAR gamma and C/EBP alpha. Proc. Natl. Acad. Sci. USA. 10:9856-9860
  23. Hulver, M. W., J. R. Berggren, R. N. Cortright and Dudek. 2003. Skeletal muscle lipid metabolism with obesity. Am. J. Physiol. Endocrinol. Metab. 284:E741-E747 https://doi.org/10.1152/ajpendo.00514.2002
  24. Inoue, K., S. Yamasaki, T. Fushiki, Y. Okada and E. Sugimoto. 1994. Androgen receptor antagonist suppresses exerciseinduced hypertrophy of skeletal muscle. Eur. J. Appl. Physiol. Occup. Physiol. 69:88-91 https://doi.org/10.1007/BF00867933
  25. Ishido, M., K. Kami and M. Masuhara. 2004. Localization of MyoD, myogenin and cell cycle regulatory factors in hypertrophying rat skeletal muscles. Acta. Physiol. Scand. 180:281-289 https://doi.org/10.1046/j.0001-6772.2003.01238.x
  26. Johnson, B. J., P. T. Anderson, J. C. Meiske and W. R. Dayton. 1996. Effect of a combined trenbolone acetate and estradiol implant on steroid hormone levels, feedlot performance, carcass characteristics and carcass composition of feedlot steers. J. Anim. Sci. 74:363-371
  27. Kahlert, S., C. Groh$\acute{a}$, R. H. Karas, K. L$\ddot{o}$bbert, L. Neyses and H. Vetter. 1997. Effects of estrogen on skeletal myoblast growth. Biochem. Biophys. Res. Commun. 17:373-378 https://doi.org/10.1016/0006-291X(64)90014-2
  28. Kamanga-Sollo, E., M. E. White, K. Y. Chung, B. J. Johnson and W. R. Dayton. 2008a. Potential role of G-protein-coupled receptor 30 (GPR30) in estradiol-17$\beta$-stimulated IGF-I mRNA expression in bovine statellite cell cultures. Domest. Anim Endocrinol. 35:254-262 https://doi.org/10.1016/j.domaniend.2008.06.001
  29. Kamanga-Sollo, E., M. E. White, M. R. Hathaway, K. Y. Chung, B. J. Johnson and W. R. Dayton. 2008b. Roles of IGF-1 and the estrogen, androgen and IGF-1 receptors in estradiol-17β- and trenbolone acetate-stimulated proliferation of cultured bovine satellite cells. Domest. Anim. Endocrinol. 35: 88-97 https://doi.org/10.1016/j.domaniend.2008.02.003
  30. Kook, S. H., K. C. Choi, Y. O. Son, K. Y. Lee, I. H. Hwang, H. J. Lee, J. S. Chang, I. H. Choi and J. C. Lee. 2006. Satellite cells isolated from adult Hanwoo muscle can proliferate and differentiate into myoblasts and adipose-like cells. Mol. Cells 22:239-245
  31. Lee, D. K. 2002. Androgen receptor enhances myogenin expression and accelerates differentiation. Biochem. Biophys. Res. Commun. 294:408-413 https://doi.org/10.1016/S0006-291X(02)00504-1
  32. Lee, E. J., J. Choi, J. H. Hyun, K. H. Cho, I. H. Hwang, H. J. Lee, J. S. Chang and I. Choi. 2007. Steroid effects on cell proliferation, differentiation and steroid receptor gene expression in adult bovine muscle satellite cells. Asian-Aust. J. Anim. Sci. 20:501-510
  33. McKeehan, W. L., P. S. Adams and M. P. Rosser. 1984. Direct mitogenic effects of insulin, epidermal growth factor, glucocorticoid, cholera toxin, unknown pituitary factors and possibly prolactin, but not androgen, on normal rat prostate epithelial cells in serum-free, primary cell culture. Cancer Res. 44:1998-2010
  34. Meyer, H. H. and M. Rapp. 1985. Estrogen receptor in bovine skeletal muscle. J. Anim. Sci. 60:294-300
  35. Mooradian, A. D., J. E. Morley and S. G. Korenman. 1987. Biological actions of androgens. Endocr. Rev. 8:1-28 https://doi.org/10.1210/edrv-8-1-1
  36. Moss, F. P. and C. P. Leblond. 1971. Satellite cells as the source of nuclei in muscles of growing rats. Anat. Rec. 170:421-435 https://doi.org/10.1002/ar.1091700405
  37. Ricketts, M. L., D. D. Moore, W. J. Banz, O. Mezei and N. F. Shay. 2005. Molecular mechanisms of action of the soy isoflavones includes activation of promiscuous nuclear receptors. A review. J. Nutir. Biochem. 16: 321-330 https://doi.org/10.1016/j.jnutbio.2004.11.008
  38. Singh, N. K., H. S. Chae, I. H. Hwang, Y. M. Yoo, C. N. Ahn, S. H. Lee, H. J. Lee, H. J. Park and H. Y. Chung. 2007. Transdifferentiation of porcine satellite cells to adipoblasts with ciglitizone. J. Anim. Sci. 85:1126-1135 https://doi.org/10.2527/jas.2006-524
  39. Sinha-Hikim, I., S. M. Roth, M. I. Lee and S. Bhasin. 2003. Testosterone-induced muscle hypertrophy is associated with an increase in satellite cell number in healthy, young men. Am. J. Physiol. Endocrinol. Metab. 285:E197-205
  40. Snochowski, M., T. Saartok, E. Dahlberg, E. Eriksson J. A. Gustafsson. 1981. Androgen and glucocorticoid receptors in human skeletal muscle cytosol. J. Steroid Biochem. 14:765-771 https://doi.org/10.1016/0022-4731(81)90013-3
  41. Tajbakhsh, S., D. Rocancourt and M. Buckingham. 1996. Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature 21:266-270 https://doi.org/10.1038/021266a0
  42. Vasconsuelo, A., L. Milanesi and R. Boland. 2008. 17Betaestradiol abrogates apoptosis in murine skeletal muscle cells through estrogen receptors: role of the phosphatidylinositol 3- kinase/Akt pathway. Endocrinology 196(2):385-397 https://doi.org/10.1677/JOE-07-0250
  43. Van Barneveld, R. J. 2003. Modern pork production - Balancing efficient growth and feed conversion with product quality requirements and consumer demands. Asia Pac. J. Clin. Nutr. 12 Supp1:S31
  44. Veldhuis, J. D., J. N. Roemmich, E. J. Richmond, A. D. Rogol, J. C. Lovejoy, M. Sheffield-Moore, N. Mauras and C. Y. Bowers. 2005. Endocrine control of body composition in infancy, childhood, and puberty. Endocr. Rev. 26:114-146 https://doi.org/10.1210/er.2003-0038
  45. Wheeler, T. L., L. V. Cundiff and R. M. Koch. 1994. Effect of marbling degree on beef palatability in Bos taurus and Bos indicus cattle. J. Anim. Sci. 72:3145-151
  46. Zammit, P. S., J. J. Carvajal, J. P. Golding, J. E. Morgan, D. Summerbell, J. Zolnerciks, T. A. Partridge, P. W. Rigby and J. R. Beauchamp. 2004. Myf5 expression in satellite cells and spindles in adult muscle is controlled by separate genetic elements. Dev. Biol. 273:454-465 https://doi.org/10.1016/j.ydbio.2004.05.038
  47. Zammit, P. and J. Beauchamp. 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

Cited by

  1. Gene expression profiles analyzed by DNA sequencing of cDNA clones constructed from porcine preadipocytes and adipocytes vol.34, pp.2, 2012, https://doi.org/10.1007/s13258-011-0075-4
  2. Effect of porcine placenta steroid extract on myogenic satellite cell proliferation, transdifferentiation, and lipid accumulation vol.48, pp.5, 2012, https://doi.org/10.1007/s11626-012-9512-1
  3. A metabolomics study of the inhibitory effect of 17-beta-estradiol on osteoclast proliferation and differentiation vol.11, pp.2, 2015, https://doi.org/10.1039/C4MB00528G
  4. Meeting the meat: delineating the molecular machinery of muscle development vol.58, pp.1, 2016, https://doi.org/10.1186/s40781-016-0100-x
  5. Effects and Mechanisms of Phthalates’ Action on Reproductive Processes and Reproductive Health: A Literature Review vol.17, pp.18, 2010, https://doi.org/10.3390/ijerph17186811