- Volume 24 Issue 9
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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
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.
- 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
- 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.
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- 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
- 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.
- 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
- 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.
- 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
- 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
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
- 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
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
- 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
- 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
- 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
- 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.
- 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.
- 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
- 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
- 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
- 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
- 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
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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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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