DOI QR코드

DOI QR Code

Differential Proteome Expression of In vitro Proliferating Bovine Satellite Cells from Longissimus Dorsi, Deep Pectoral and Semitendinosus Muscle Depots in Response to Hormone Deprivation and Addition

  • Rajesh, Ramanna Valmiki (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, R.D.A.) ;
  • Kim, Seong-Kon (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, R.D.A.) ;
  • Park, Mi-Rim (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, R.D.A.) ;
  • Park, Min-Ah (Dept. of Agricultural Science, Korea National Open University) ;
  • Jang, Eun-Joung (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, R.D.A.) ;
  • Hong, Seung-Gu (Nutrition and Physiology Team, National Institute of Animal Science, R.D.A.) ;
  • Chang, Jong-Soo (Dept. of Agricultural Science, Korea National Open University) ;
  • Yoon, Du-Hak (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, R.D.A.) ;
  • Kim, Tae-Hun (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, R.D.A.) ;
  • Lee, Hyun-Jeong (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, R.D.A.)
  • Received : 2009.12.02
  • Accepted : 2009.12.21
  • Published : 2009.12.01

Abstract

The aim of this study was to analyze the proteome of proliferating bovine satellite cells from longissimus dorsi, deep pectoral and semitendinosus muscle depots which had been subjected to hormonal deprivation or addition in culture. For hormone deprivation or addition studies, the cells were either grown in 10% charcoal-dextran stripped fetal bovine serum (CD-FBS) or in 10% FBS supplemented medium. Further to analyze the effect of insulin like growth factor (IGF-1) and testosterone (TS), the cells were grown in 10% CD-FBS containing IGF-1 (10 ng/ml) or TS (10 nM). Results have shown that hormone deprivation had a negative impact on proliferation of the cells from each of the muscle depots. In case of IGF-1 and TS addition, the proliferation levels were low compared with that of the cells grown in 10% FBS. Hence, to gain the insights of the proteins that are involved in such divergent levels of proliferation, the proteome of such satellite cells proliferating under the above mentioned conditions were analyzed using 2D-DIGE and MALDI-ToF/ToF. Thirteen proteins during hormone deprivation and nine proteins from hormone addition were found to be differentially expressed in all the cultures of the cells from the three depots. Moreover, the results highlighted in this study offer a role for each differentially expressed protein with respect to its effect on positive or negative regulation of cell proliferation.

Keywords

References

  1. Abraham, M. R., Jahangir, A., Alekseev, A. E. and Terzic, A. 1999. Channelopathies of inwardly rectifying potassium channels. J. 13:1901-1910. https://doi.org/10.1096/fasebj.13.14.1901
  2. Allen, R. E. and Boxhorn, L. K. 1987. Inhibition of skeletal muscle satellite cell differentiation by transforming growth factor-$\beta$. J. Cell. Physiol. 133:567-573. https://doi.org/10.1002/jcp.1041330319
  3. Allen, R. E. and Rankin, L. L. 1990. Regulation of satellite cells during skeletal muscle growth and development. Proc. Soc. Exp. Biol. Med. 94:81-86.
  4. Allen, R. E., Sheeha, S. M., Taylor, R. G., Kendall, T. L. and Rice, G. M. 1995. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J. Cell. Physiol. 165: 307312.
  5. Apple, J. K., Dikeman, M. E., Simms, D. D. and Kuhl, G. 1991. Effects of synthetic hormone implants, singularly or in combinations, on performance, carcass traits, and longissimus muscle palatability of Holstein steers. J. Ani. Sci. 69:4437-4448. https://doi.org/10.2527/1991.69114437x
  6. Azmitia, E. C. 2001. Modern views on an ancient chemical: Serotonin effects on cell proliferation, maturation, and apoptosis. Brain Res. Bull. 56:413-424. https://doi.org/10.1016/S0361-9230(01)00614-1
  7. Bailey, S. R., Polan, J. L., Munoz, O. C., Agrawal, M. C., and Goswami, N. J. 2004. Proliferation and β-tubulin for human aortic endothelial cells within gas-plasma scaffolds. Cardiovasc. Radiat. Med. 5:119-124. https://doi.org/10.1016/j.carrad.2004.08.001
  8. Bhasin, S., Woodhouse, L., Casaburi, R., Singh, A. B., Bhasin, D. and Berman, N. 2001. Testosterone dose-response relationships in healthy young men. Am. J. Physiol. Endocrinol. Metab. 281:E1172-1181. https://doi.org/10.1152/ajpendo.2001.281.6.E1172
  9. Blishchenko, E. Y., Sazonova, O. V., Kalinina, O. A., Yatskin, O. N.,. Philippova, M. M., Surovoy, A. Y., Karelin, A. A., and Ivanov, V. T. 2002. Family of hemorphins: co-relations between aminoacidsequences and effects in cell cultures, Peptides 23:903-910. https://doi.org/10.1016/S0196-9781(02)00017-7
  10. Bock, J., Szabo, I., Jekle, A. and Gulbinsa, E. 2002. Actinomycin D-induced apoptosis involves the potassium channel Kv1.3. Biochem. Biophys. Res. Commun. 295:526-531. https://doi.org/10.1016/S0006-291X(02)00695-2
  11. Braden, C., McFarland, Jerry Stewart, Jr., Hamza, A., Nordal, R., Davidson, D. J., Henkin, J. and Gladson., C. L. 2009. Plasminogen Kringle 5 induces apoptosis of brain microvessel endothelial cells: sensitization by radiation and requirement for GRP78 and LRP1. Cancer Res. 69:5537-5545. https://doi.org/10.1158/0008-5472.CAN-08-4841
  12. Brenda, Y. T., Salumbides, C., Wang, David Z. Qian, Simon Williams, Burd, C. G. and Emr, S. D. 1998. Phosphatidylinositol (3)-phosphate signaling mediated by specific binding to ring FYVE finger domains. Mol. Cell. 2:157-162. https://doi.org/10.1016/S1097-2765(00)80125-2
  13. Byun, Y., Chen, F., Chang, R., Trivedi, M., Green, K. J. and Cryns, V. L. 2001. Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis, Cell Death Differ. 8:43-450.
  14. Callebert, J., Esteve, J. M., Herve, P., Peoch, K., Tournois, C., Drouet, L., Launay, J. M. and Maroteaux, L. 2006. Evidence for a control of plasma serotonin levels by 5-hydroxytryptamine (2B) receptors in mice. J. Pharmacol. Exp. Ther. 317:724-731. https://doi.org/10.1124/jpet.105.098269
  15. 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
  16. Cooper, R. N., Tajbakhsh, S., Mouly, V., Cossu, G., Buckingham, M. and Butler-Browne, G. S. 1999. In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J. Cell. Sci. 112:2895-2901.
  17. Dodson, M. V., McFarland, D. C., Grant, A. L., Doumit, M. E. and Velleman, S. G. 1996. Extrinsic regulation of domestic animal-derived satellite cells. Domest. Anim. Endocrinol. 13:107-26. https://doi.org/10.1016/0739-7240(95)00062-3
  18. Doumit, M. E. and Merkel, R. A. 1992. Conditions for the isolation and culture of porcine myogenic satellite cells. Tissue and cell. 24:253-262. https://doi.org/10.1016/0040-8166(92)90098-R
  19. Doumit, M. E., Cook, D. R. and Merkel, R. A. 1996 Testosterone up-regulates androgen receptors and decreases differentiation of porcine myogenic satellite cells in vitro. Endocrinology 137:1385-1394. https://doi.org/10.1210/en.137.4.1385
  20. Florini, J. R. and Magri, K. A. 1989. Effects of growth factors on myogenic differentiation. Am. J. Physiol. 256:701-711. https://doi.org/10.1152/ajpcell.1989.256.4.C701
  21. Folkman, J. 2006. Antiangiogenesis in cancer therapy-endostatin and its mechanisms of action. Exp. Cell. Res. 312:594-607. https://doi.org/10.1016/j.yexcr.2005.11.015
  22. Goodman, A., Goode, B. L., Matsudaira, P. and Fink, G, R. 2003. The Saccharomyces cerevisiae calponin/transgelin homolog Scp1 functions with fimbrin to regulate stability and organization of the actin cytoskeleton. Mol. Biol. Cell. 14: 2617-29. https://doi.org/10.1091/mbc.E03-01-0028
  23. Greene, E. A. and Allen RE. 1991. Growth factor regulation of bovine satellite cell growth in vitro. J. Ani. Sci. 69:146-152. https://doi.org/10.2527/1991.691146x
  24. Halevy, O., Krispin, A., Leshem, Y., MCMurthy, J. P. and Yahav, S. 2001. Early-age heat exposure affects skeletal muscle satellite cell proliferation and differentiation in chicks. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 281: R302-R309. https://doi.org/10.1152/ajpregu.2001.281.1.R302
  25. Hansen-Smith, F. M., Picou, D. and Golden, M. N. H. 1979. Muscle satellite cells in malnourished and nutritionally rehabilitated children. Neurol. Sci. 41:207-221. https://doi.org/10.1016/0022-510X(79)90040-6
  26. Hayden, J. M., Williams, J. E. and Collier, R. J. 1993. Plasma growth hormone, insulin-like growth factor, insulin, and thyroid hormone association with body protein and fat accretion in steers undergoing compensatory gain after dietary energy restriction. J. Anim. Sci. 71:3327-3338. https://doi.org/10.2527/1993.71123327x
  27. Hellmann, U., Wemstedt, C., Gonez, J. and Heldin, C. H. 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
  28. Herschler, R. C., Olmsted, A. W., Edwards, A. J., Hale, T., Montgomery, R. L., Preston, S. J. and Sheldon, J. J. 1995. Production responses to various doses and ratio of estradiol benzoate and trenbolone acetate implants in steers and heifers. J. Ani. Sci. 69:2452-2462.
  29. Hill, D. J., Crace, S. P., Nissley, Morell, D., Holder, A. T. and Milner. R. D. G. 1985. Fetal rat myoblasts release both rat somatomedin-C (SM-C)-in-like growth factor I QGF-I) and multiplication-stimulating activity in vitro: partial characterization and biological activity of myoblastderived SM-C/IGF-I. Endocrinology 117:2061. https://doi.org/10.1210/endo-117-5-2061
  30. Hunt, D. W., Henricks, D. M., Skelley, G. C. and Grimes, L. M. 1991. Use of trenbolone acetate and estradiol in intact and castrate male cattle: Effect of growth, serum hormones, and carcass characteristics. J. Ani. Sci. 69:2452-2462. https://doi.org/10.2527/1991.6962452x
  31. Johnson, B. J., Anderson, P. T., Meiske, J. C. and Dayton, W. R. 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. 74:363-71. https://doi.org/10.2527/1996.742363x
  32. Johnson, B. J., Halstead, N., White, M. E., Hathaway, M. R. and Dayton, W. R. 1998. Activation state of muscle satellite cells isolated from steers implanted with a combined trenbolone acetate and estradiol implant. J. Anim. Sci. 76: 2779-86. https://doi.org/10.2527/1998.76112779x
  33. Kamanga-Sollo, E., Pampusch, M. S., Xi, G., White, M. E., Hathaway, M. R. and Dayton, W. R. 2004 IGF-I mRNA levels in bovine satellite cell cultures: effects of fusion and anabolic steroid treatment. J. Cell. Physiol. 201:181-189. https://doi.org/10.1002/jcp.20000
  34. Kamanga-Sollo, E., White, M. E., Hathaway, M. R., Chung, K. Y., Johnson, B. J. and Dayton, W. R. 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
  35. Kampa, M., Bakogeorgou, E., Hatzolgou, A., Damianaki, A., Martin, P. M. and Castanas, E. 1997. Opioid alkaloids and casomorphin peptides decrease the proliferation of prostatic cancer cell lines (LNCaP, PC3 and DU145) through a partial interaction with opioid receptors. Eur. J. Pharmacol. 335:255-65. https://doi.org/10.1016/S0014-2999(97)01213-2
  36. Kubo, Y., Adelman, J. P., Clapham, D. E., Jan, L. Y., Karschin, A., Kurachi, Y., Lazdunski, M., Nichols, C. G., Seino, S. and Vandenberg, C. A. 2005. International Union of Pharmacology. LIV. Nomenclature and molecular relationships of inwardly rectifying potassium channels. Pharmacol. Rev. 57:509-526. https://doi.org/10.1124/pr.57.4.11
  37. Landry, F., Lombardo, C. R. and Smith, J. W. 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
  38. Lee, E. J., Choi, J., Hyun, J. H, Cho, K. H., Hwanf, I., Lee, H. J., Chang, J. and Chi, I. 2007. . Asian-Aust. J. Ani. Sci. 20: 501-510. https://doi.org/10.5713/ajas.2007.501
  39. Lindquist, D. L. and de Alarcon, P. A. 1987. Charcoal-dextran treatment of fetal bovine serum removes an inhibitor of human CFU-megakaryocytes. Exp. Hematol. 15:234-238.
  40. Mampuru, L. J., Chen, S., Kalenik, J. L., Bradley, M. E. and Lee, T. 1996. Analysis of events associated withsSerum deprivation-induced apoptosis in C3H/Sol8 muscle satellite cells. Exp. Cell. Res. 226:372-380. https://doi.org/10.1006/excr.1996.0238
  41. McCuscker, R. H. and Campion, D. R. 1986. Effect of growth-hormone secreting tumors on skeletal muscle cellularity in the rat. J. Endocrinol. 111:279-285. https://doi.org/10.1677/joe.0.1110279
  42. Mirua, S., Takeshita, T., Asao, H., Kimura, Y., Murata, K., Sasaki, Y., Hanai, J., Beppu, H., Tsukazaki, T., Wrana, J. L., Miyazono, K. and Sugamura, K. 2000. Hgs (Hrs), a FYVE Domain Protein, Is Involved in Smad Signaling through Cooperation with SARA. Mol. Cell. Biol. 20:9346-9355. https://doi.org/10.1128/MCB.20.24.9346-9355.2000
  43. Moss, F. P. and Leblond, C. P. 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
  44. Murphy, C., McGurk, M., Pettigrew, J., Santinelli, A., Mazzucchelli, R., Johnston, G. P., Montironi, R. and Waugh, D. J. 2005. Nonapical and cytoplasmic expression of interleukin-8, CXCR1, and CXCR2 correlateswith cell proliferation and microvessel density in prostate cancer. Clin. Cancer Res. 11:4117. https://doi.org/10.1158/1078-0432.CCR-04-1518
  45. Rabilloud, T. 1998. Use of thiourea to increase the solubility of membrane proteins in two-dimensional electrophoresis, Electrophoresis 19:758-760. https://doi.org/10.1002/elps.1150190526
  46. Sebestyen, A., Barnaa, G., Nagya, K., Janosi, J., Paku, S., Kohut, E., Berczi, L., Mihalik, R. and Kopper, L. 2005. Smad signal and TGFb induced apoptosis in human lymphoma cells. Cytokine. 30:228-235. https://doi.org/10.1016/j.cyto.2005.01.013
  47. Sinha-Hikim, I., Artaza, J., Woodhouse, L., Gonzalez-Cadavid, N., Singh, A. B. and Lee, M. I. 2002. Testosterone-induced increase in muscle size in healthy young men is associated with muscle fiber hypertrophy. Am. J. Physiol. Endocrinol. Metab. 283:E154-164. https://doi.org/10.1152/ajpendo.00502.2001
  48. Sinha-Hikim, I., Roth, S. M., Lee, M. I. and Bhasin, S. 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 https://doi.org/10.1152/ajpendo.00370.2002
  49. Spagnuolo, P. A., Bird, R. P. and Hoffman-Goetz, L. 2007. Effect of short-term dietary intake of bovine lactoferrin on intestinal lymphocyte apoptosis in healthy mice. Nutrition 23:812-817. https://doi.org/10.1016/j.nut.2007.07.006
  50. Thompson, S. H., Boxhorn, L. K., Kong, W. Y. and Allen, R. E. 1989. Trenbolone alters the responsiveness of skeletal muscle satellite cells to fibroblast growth factor and insulin-like growth factor I. Endocrinology. 124:2110-2121. https://doi.org/10.1210/endo-124-5-2110
  51. Thompson, S. H., Boxhorn, L. K., Kong, W. Y. and Allen, R. E. 1989. Trenbolone alters the responsiveness of skeletal muscle satellite cells to fibroblast growth factor and insulinlike growth factor I. Endocrinology 124:2110-2117. https://doi.org/10.1210/endo-124-5-2110
  52. Tonge, R., Shaw, J., Middleton, B., Rowlinson, R., Rayner, S., Young, J., Pognan, F., Hawkins, E., Currie, I. and Davison, M. 2001. Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics. 1:377-396. https://doi.org/10.1002/1615-9861(200103)1:3<377::AID-PROT377>3.0.CO;2-6
  53. Wang, S., Z, Ying., Y, Yun., Li, X., Guo-qiang, C., Yong-zong, Y. and Li-shun, W. 2008. Phosphorylation of b-actin by protein kinase C-delta in camptothecinanalog-induced leukemic cell apoptosis. Acta Pharmacol Sin. 29:135-142. https://doi.org/10.1111/j.1745-7254.2008.00753.x
  54. Yongfeng Wei, Tolib B. Sanni, Peter X. F., Atadja, J. and Pili, R. 2007. Antitumor effect of the histone deacetylase inhibitor LAQ824 in combination with 13-cis-retinoic acid in human malignant melanoma. Mol. Cancer. Ther. 6:70-81. https://doi.org/10.1158/1535-7163.MCT-06-0125