Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Proteomic Analysis of Bovine Muscle Satellite Cells during Myogenic Differentiation

  • Rajesh, Ramanna Valmiki (Division of Animal Genomics and Bioinformatics, National Institute of Animal science, Rural Development Administration) ;
  • Jang, Eun-Jeong (Division of Animal Genomics and Bioinformatics, National Institute of Animal science, Rural Development Administration) ;
  • Choi, In-Ho (Division of Animal Genomics and Bioinformatics, National Institute of Animal science, Rural Development Administration) ;
  • Heo, Kang-Nyeong (Division of Animal Genomics and Bioinformatics, National Institute of Animal science, Rural Development Administration) ;
  • Yoon, Du-Hak (Division of Animal Genomics and Bioinformatics, National Institute of Animal science, Rural Development Administration) ;
  • Kim, Tae-Hun (Division of Animal Genomics and Bioinformatics, National Institute of Animal science, Rural Development Administration) ;
  • Lee, Hyun-Jeong (Division of Animal Genomics and Bioinformatics, National Institute of Animal science, Rural Development Administration)
  • Received : 2010.09.29
  • Accepted : 2011.05.19
  • Published : 2011.09.01
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Abstract

The aim of this study was to analyze the proteome expression of bovine satellite cells from longissimus dorsi (LD), deep pectoral (DP) and semitendinosus (ST) muscle depots during in vitro myogenic differentiation. Proteomic profiling by twodimensional gel electrophoresis and mass spectrometry of differentiating satellite cells revealed a total of 38 proteins that were differentially regulated among the three depots. Among differentially regulated proteins, metabolic proteins like lactate dehydrogenase (LDH), malate dehydrogenase (MDH) were found to be up regulated in ST, while alpha-enolase (NNE) in LD and DP depot satellite cells were down regulated. Also, our analysis found that there was a prominent up regulation of cytoskeletal proteins like actin, actincapping protein and transgelin along with chaperone proteins like heat shock protein beta 1 (HSPB 1) and T-complex protein 1 (TCP-1). Among other up regulated proteins, LIM domain containing protein, annexin 2 and Rho GDP-dissociation inhibitor 1 (Rho GDI) are observed, which were already proven to be involved in the myogeneis. More interestingly, satellite cells from ST depot were found to have a higher myotube formation rate than the cells from the other two depots. Taken together, our results demonstrated that, proteins involved in glucose metabolism, cytoskeletal modeling and protein folding plays a key role in the myogenic differentiation of bovine satellite cells.

Keywords

References

  1. Ahmed, M. and P. Bergsten. 2005. Glucose-induced changes of multiple mouse islet proteins analysed by two-dimensional gel electrophoresis and mass spectrometry. Diabetologica 48:477-485. https://doi.org/10.1007/s00125-004-1661-7
  2. Allen, R. E. and L. L. Rankin. 1990. Regulation of satellite cells during skeletal muscle growth and development. Proc. Soc. Exp. Biol. Med. 94:81-86.
  3. Barjoti, C., V. Laplace-Marieze, L. Gannoun-Zaki, G. Mckoy, M. Le Briand, P. Vigneroni and F. Bacou. 1998. Expression of lactate dehydrogenase, myosin heavy chain and myogenic regulatory factor genes in rabbit embryonic muscle cell cultures. J. Muscle Res. Cell. Motil. 19:343-351. https://doi.org/10.1023/A:1005389418903
  4. Bhasin, S., L. Woodhouse, R. Casaburi, A. B. Singh, D. Bhasin and N. Berman. 2001. Testosterone dose-response relationships in healthy young men. Am. J. Physiol. Endocrinol. Metab. 281:E1172-1181.
  5. Bouley, J., B. Meunier, C. Chambon, S. De Smet, J. F. Hocquette and B. Picard. 2005. Proteomic analysis of bovine skeletal muscle hypertrophy. Proteomics 5:490-500. https://doi.org/10.1002/pmic.200400925
  6. Bracha1, A. L., A. Ramanathan, S. Huang, D. EIngber and S. L. Schreiber. 2010. Carbon metabolism-mediated myogenic differentiation. Nat. Chem. Biol. 6:202-204. https://doi.org/10.1038/nchembio.301
  7. Bryan, B. A., D. Li, X. Wu and M. Liu. 2005. The Rho family of small GTPases: Crucial regulators of skeletal myogenesis. Cell. Mol. Life Sci. 62:1547-1555. https://doi.org/10.1007/s00018-005-5029-z
  8. Campion, D. R. 1984. The muscle satellite cell: a review. Int. Rev. Cytol. 87:225-251. https://doi.org/10.1016/S0074-7696(08)62444-4
  9. Chaze, T., B. Meunier, C. Chambon, C. Jurie and B. Picard. 2008. In vivo proteome dynamics during early bovine myogenesis. Proteomics 8:4236-4248. https://doi.org/10.1002/pmic.200701101
  10. Cooper, R. N., S. Tajbakhsh, V. Mouly, G. Cossu, M. Buckingham and G. S. Butler-Browne. 1999. In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J. Cell Sci. 112:2895-2901.
  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. Doumit, M. E. and R. A. Merkel. 1992. Conditions for the isolation and culture of porcine myogenic satellite cells. Tissue Cell 24:253-262. https://doi.org/10.1016/0040-8166(92)90098-R
  13. Dovas, A. and J. R. Couchman. 2005. RhoGDI: Multiple functions in the regulation of Rho family GTPase activities. Biochem. J. 390:1-9. https://doi.org/10.1042/BJ20050104
  14. Fischer, D., J. Matten, J. Reimann, C. Bonnemann and R. Schroder. 2002. Expression, localization and functional divergence of alphaB-crystallin and heat shock protein 27 in core myopathies and neurogenic atrophy. Acta Neuropathol. 104:297-304.
  15. Grounds, M. D., K. L. Garrett, M. C. Lai, W. E. Wright and M. W. Beilharz. 1992. Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res. 267:99-104. https://doi.org/10.1007/BF00318695
  16. Halevy, O., A. Krispin, Y. Leshem, J. P. MCMurthy and S. Yahav. 2001. Early-age heat exposure affects skeletal muscle satellite cell proliferation and differentiation in chicks. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R302-R309.
  17. Hamelin, M., T. Sayd, C. Chambon, J. Bouix, B. Bibé, D. Milenkovic, H. Leveziel, M. Georges, A. Clop, P. Marinova and E. Laville. 2006. Proteomic analysis of ovine muscle hypertrophy. J. Anim. Sci. 84:3266-3276. https://doi.org/10.2527/jas.2006-162
  18. Hellmann, U., C. Wemstedt, J. Gonez and C. H. Heldin. 1995. Improvement of an "In-gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 224:451-455. https://doi.org/10.1006/abio.1995.1070
  19. Houbak, M. B., P. Ertbjerg and M. Therkildsen. 2008. In vitro study to evaluate the degradation of bovine muscle proteins post-mortem by proteasome and $\mu$-calpain. Meat Sci. 79:77-85. https://doi.org/10.1016/j.meatsci.2007.08.003
  20. Jia, X., K. Hollung, M. Therkildsen, K. I. Hildrum and E. Bendixen. 2006. Proteome analysis of early post-mortem changes in two bovine muscle types: M. longissimus dorsi and M. semitendinosus. Proteomics 6:936-944. https://doi.org/10.1002/pmic.200500249
  21. Kamanga-Sollo, E., M. E. White, M. R. Hathaway, K. Y. Chung, B. J. Johnson and W. R. Dayton. 2008. Roles of IGF-1 and the estrogen, androgen and IGF-1 receptors in estradiol-17$\beta$ and trenbolone acetate-stimulated proliferation of cultures bovine satellite cells. Domest. Anim. Endocrinol. 35:88-97. https://doi.org/10.1016/j.domaniend.2008.02.003
  22. Kim, N. K., S. Cho, S. H. Lee, H. R. Park, C. S. Lee, Y. M. Cho, Y. H. Choy, D. Yoon, S. K. Im and E. W. Park. 2008. Proteins in longissimus muscle of Korean native cattle and their relationship to meat quality. Meat Sci. 80:1068-1073. https://doi.org/10.1016/j.meatsci.2008.04.027
  23. Kim, N. K., S. H. Lee, Y. M. Cho, E. S. Son, K. Y. Kim, C. S. Lee, D. Yoon, S. K. Im, S. J. Oh and E. W. Park. 2009. Proteome analysis of the m. longissimus dorsi between fattening stages in Hanwoo steer. BMB Rep. 42:433-438. https://doi.org/10.5483/BMBRep.2009.42.7.433
  24. Kislinger, T., A. O. Gramolini, Y. Pan, K. Rahman, D. H. MacLennan and A. Emili. 2005. Proteome dynamics during C2C12 myoblast differentiation. Mol. Cell Proteomics 4:887-901. https://doi.org/10.1074/mcp.M400182-MCP200
  25. Kong, Y., M. J. Flick, A. J. Kudla and S. F. Konieczny. 1996. Muscle LIM protein promotes myogenesis by enhancing the activity of MyoD. Mol. Cell. Biol. 17:4750-4760.
  26. 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.
  27. Landry, F., C. R. Lombardo and J. W. Smith. 2000. A method for application of samples to Matrix-Assisted Laser Desorption Ionization Time-of-Flight targets that enhances peptide detection. Anal. Biochem. 279:1-8. https://doi.org/10.1006/abio.1999.4468
  28. Laville, E., T. Sayd, M. Morzel, S. Blinet, C. Chambon, J. Lepetit, G. Renand and J. F. Hocquette. 2009. Proteome changes during meat aging in tough and tender beef suggest the importance of apoptosis and protein solubility for beef aging and tenderization. J. Agric. Food Chem. 57:10755-10764. https://doi.org/10.1021/jf901949r
  29. Lehnert, S. A., A. Reverter, K. A. Byrne, Y. Wang, G. S. Nattrass, N. J. Hudson and P. L. Greenwood. 2007. Gene expression studies of developing bovine longissimus muscle from two different beef cattle breeds. BMC Dev. Biol. 7:95-108. https://doi.org/10.1186/1471-213X-7-95
  30. Lennon, N. J., A. Kho, B. J. Bacskai, S. L. Perlmutter, B. T. Hyman and R. H. Brown Jr. 2003. Dysferlin Interacts with Annexins A1 and A2 and Mediates Sarcolemmal Woundhealing. J. Biol. Chem. 278:50466-50473. https://doi.org/10.1074/jbc.M307247200
  31. 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
  32. Peterson, C. A., M. Cho, F. Rastinejad and H. M. Blau. 1992. $\beta$-Enolase is a marker of human myoblast heterogeneity prior to differentiation. Dev. Biol. 151:626-629. https://doi.org/10.1016/0012-1606(92)90201-Q
  33. Picard, B., C. Berri, L. Lefaucheur, C. Molette, T. Sayd and C. Terlouw. 2010. Skeletal muscle proteomics in live stock. Brief Funct Genomic Proteomic bfg.oxfordjournals.org/cgi/content/full/elq005v1
  34. Rajesh, R. V., S. K. Kim, M. R. Park, M. A. Park, E. J. Jang, S. G. Hong, J. S. Chang, D. Yoon, T. H. Kim and H. J. Lee. 2009. Differential proteome expression of in vitro proliferating bovine satellite cells from Longissimuss dorsi, Deep pectoral and Semitendinosus muscle depots in response to hormone deprivation and addition. Korean Journal of Animal Science and Technology 51:459-470. https://doi.org/10.5187/JAST.2009.51.6.459
  35. Rudnicki, M. A., P. N. J. Schnegelsberg, R. H. Stead, T. Braun, H. H. Arnold and R. Jaenisch. 1993. MyoD or Myf5 is required for the formation of skeletal muscle. Cell 75:1351-1359. https://doi.org/10.1016/0092-8674(93)90621-V
  36. Schmidt, A. and M. N. Hall. 1998. Signaling to the actin cytoskeleton. Annu. Rev. Cell Dev. Biol. 14:305-338. https://doi.org/10.1146/annurev.cellbio.14.1.305
  37. Seale, P. and M. A. Rudnicki. 2000. A new look at the origin, function, and ''Stem-Cell'' status of muscle satellite cells. Dev. Biol. 218:115-124. https://doi.org/10.1006/dbio.1999.9565
  38. Shibata, M., K. Matsumoto, M. Oe, M. Ohnishi-Kameyama, K. Ojima, I. Nakajima, S. Muroya and K. Chikuni. 2009. Differential expression of the skeletal muscle proteome in grazed cattle. J. Anim. Sci. 87:2700-2708. https://doi.org/10.2527/jas.2008-1486
  39. Smith, C. K., M. J. Janney and R. E. Allen. 1994. Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J. Cell. Physiol. 159:379-385. https://doi.org/10.1002/jcp.1041590222
  40. Sternlicht, H., G. W. Farr, M. L. Sternlicht, J. K. Driscoll, K. Willison and M. B. Yaffe. 1993. The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc. Natl. Acad. Sci. USA. 90:9422-9426. https://doi.org/10.1073/pnas.90.20.9422
  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 384:266-270. https://doi.org/10.1038/384266a0
  42. Tannu, N. S., V. K. Rao, R. M. Chaudhary, F. Giorgianni, A. E. Saeed, Y. Gao and R. Raghow. 2004. Comparative proteomes of the proliferating C2C12 myoblasts and fully differentiated myotubes reveal the complexity of the skeletal muscle differentiation program. Mol. Cell Proteomics 3:1065-1082. https://doi.org/10.1074/mcp.M400020-MCP200
  43. Thompson, H. S., E. B. Maynard, E. R. Morales and S. P. Scordilis. 2003. Exercise-induced HSP27, HSP70 and MAPK responses in human skeletal muscle. Acta Physiol. Scand. 178:61-72. https://doi.org/10.1046/j.1365-201X.2003.01112.x

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