[en] BACKGROUND: Muscle growth depends on the fusion of proliferate satellite cells to existing myofibers. We reported previously that 0-14 day intermittent feeding led to persistent retardation in myofiber hypertrophy. However, how satellite cells respond to such nutritional insult has not been adequately elucidated. RESULTS: One-day-old broiler chicks were allocated to control (Con, ad libitum feeding), intermittent feeding (IF, feed provided on alternate days) and re-feeding (RF, 2 days ad libitum feeding after 12 days of intermittent feeding) groups. Chickens were killed on Day 15 and satellite cells were isolated. When cultured, satellite cells from the IF group demonstrated significant retardation in proliferation and differentiation potential, while RF partly restored the proliferation rate and differentiation potential of the satellite cells. Significant up-regulation of insulin like growth factor I receptor (IGF-IR) (P<0.05) and thyroid hormone receptor alpha (TRalpha) (P<0.05), and down-regulation of growth hormone receptor (GHR) (P<0.01) and IGF-I (P<0.01) mRNA expression was observed in freshly isolated IF satellite cells when compared with Con cells. In RF cells, the mRNA expression of IGF-I was higher (P<0.05) and of TRalpha was lower (P<0.01) than in IF cells, suggesting that RF restored the mRNA expression of TRalpha and IGF-I, but not of GHR and IGF-IR. The Bax/Bcl-2 ratio tended to increase in the IF group, which was reversed in the RF group (P<0.05), indicating that RF reduced the pro-apoptotic influence of IF. Moreover, no significant effect of T3 was detected on cell survival in IF cells compared with Con (P<0.001) or RF (P<0.05) cells. CONCLUSIONS: These data suggest that early-age feed restriction inhibits the proliferation and differentiation of satellite cells, induces changes in mRNA expression of the GH/IGF-I and thyroid hormone receptors in satellite cells, as well as blunted sensitivity of satellite cells to T3, and that RF partially reverses these effects. Thus, a moderate nutritional strategy for feed restriction should be chosen in early chick rearing systems.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Li, Yue
Yang, Xiaojing
Ni, Yingdong
Decuypere, Eddy
Buyse, Johan
Everaert, Nadia ; KU Leuven > Department of Biosystems > Division Livestock-Nutrition-Quality
Grossmann, Roland
Zhao, Ruqian
Language :
English
Title :
Early-age feed restriction affects viability and gene expression of satellite cells isolated from the gastrocnemius muscle of broiler chicks.
Demmelmair H, von Rosen J, Koletzko B. Long-term consequences of early nutrition. Early Hum Dev 2006, 82:567-574. 10.1016/j.earlhumdev.2006.07.004, 16887299.
Langley-Evans SC, Bellinger L, McMullen S. Animal models of programming: early life influences on appetite and feeding behaviour. Matern Child Nutr 2005, 1:142-148. 10.1111/j.1740-8709.2005.00015.x, 16881893.
de Moura EG, Passos MC. Neonatal programming of body weight regulation and energetic metabolism. Biosci Rep 2005, 25:251-269. 10.1007/s10540-005-2888-3, 16283556.
Li Y, Yuan L, Yang X, Ni Y, Xia D, Barth S, Grossmann R, Zhao RQ. Effect of early feed restriction on myofibre types and expression of growth-related genes in the gastrocnemius muscle of crossbred broiler chickens. Br J Nutr 2007, 98:310-319. 10.1017/S0007114507699383, 17445349.
Campion DR. The muscle satellite cell: a review. Int Rev Cytol 1984, 87:225-251.
Vierck J, O'Reilly B, Hossner K, et al. Satellite cell regulation following myotrauma caused by resistance exercise. Cell Biol Int 2000, 24:263-272. 10.1006/cbir.2000.0499, 10805959.
Halevy O, Geyra A, Barak M, Uni Z, Sklan D. Early posthatch starvation decreases satellite cell proliferation and skeletal muscle growth in chicks. J Nutr 2000, 130:858-864.
Halevy O, Krispin A, Leshem Y, McMurtry JP, Yahav S. Early-age heat exposure affects skeletal muscle satellite cell proliferation and differentiation in chicks. Am J Physiol Regul Integr Comp Physiol 2001, 281:R302-R309.
Halevy O, Nadel Y, Barak M, Rozenboim I, Sklan D. Early posthatch feeding stimulates satellite cell proliferation and skeletal muscle growth in turkey poults. J Nutr 2003, 133:1376-1382.
Mozdziak PE, Walsh TJ, McCoy DW. The effect of early posthatch nutrition on satellite cell mitotic activity. Poult Sci 2002, 81:1703-1708.
Moore DT, Ferket PR, Mozdziak PE. The effect of early nutrition on satellite cell dynamics in the young turkey. Poult Sci 2005, 84:748-756.
Halevy O, Hodik V, Mett A. The effects of growth hormone on avian skeletal muscle satellite cell proliferation and differentiation. Gen Comp Endocrinol 1996, 101:43-52. 10.1006/gcen.1996.0006, 8713643.
Hodik V, Mett A, Halevy O. Mutual effects of growth hormone and growth factors on avian skeletal muscle satellite cells. Gen Comp Endocrinol 1997, 108:161-170. 10.1006/gcen.1997.6964, 9378270.
Cassar-Malek I, Langlois N, Picard B, Geay Y. Regulation of bovine satellite cell proliferation and differentiation by insulin and triiodothyronine. Domest Anim Endocrinol 1999, 17:373-388. 10.1016/S0739-7240(99)00055-7, 10628428.
Jeanplong F, Bass JJ, Smith HK, Kirk SP, Kambadur R, Sharma M, Oldham JM. Prolonged underfeeding of sheep increases myostatin and myogenic regulatory factor Myf-5 in skeletal muscle while IGF-I and myogenin are repressed. J Endocrinol 2003, 176:425-437. 10.1677/joe.0.1760425, 12630927.
Jacobs SC, Bar PR, Bootsma AL. Effect of hypothyroidism on satellite cells and postnatal fiber development in the soleus muscle of rat. Cell Tissue Res 1996, 286:137-144. 10.1007/s004410050682, 8781220.
Doumit ME, Merkel RA. Conditions for isolation and culture of porcine myogenic satellite cells. Tissue Cell 1992, 24:253-262. 10.1016/0040-8166(92)90098-R, 1589873.
Mau M, Oksbjerg N, Rehfeldt C. Establishment and conditions for growth and differentiation of a myoblast cell line derived from the semimembranosus muscle of newborn piglets. In Vitro Cell Dev Biol Anim 2008, 44:1-5.
Grant AL, Helferich WG, Merkel RA, Bergen WG. Effects of phenethanolamines and propranolol on the proliferation of cultured chick breast muscle satellite cells. J Anim Sci 1990, 68:652-658.
Chen Y, Wang K, Zhu DH. Isolation, culture, identification and biological characteristics of chicken skeletal muscle satellite cells. Yi Chuan 2006, 28:257-260.
Xu P, Gu X. The effects of EGF, TGF-beta and insulin on the growth of rabbit's skeletal muscle satellite cell. Zhonghua Kou Qiang Yi Xue Za Zhi 2000, 35:289-291.
Barandier C, Montani JP, Yang Z. Mature adipocytes and perivascular adipose tissue stimulate vascular smooth muscle cell proliferation: effects of aging and obesity. Am J Physiol Heart Circ Physiol 2005, 289:H1807-H1813. 10.1152/ajpheart.01259.2004, 16024563.
Wang BH, Ouyang JP, Liu YM, Zheng HQ, Wei L, Yang JW, Li K, YANG HL. Effects of thyroid hormone on the myosin heavy chain mRNA expression in cardiac myocytes induced by angiotensin II. Chin J Pathophysiol 2003, 19:1463-1467.
Nakashima K, Ohtsuka A, Hayashi K. Effects of thyroid hormones on myofibrillar proteolysis and activities of calpain, proteasome, and cathepsin in primary cultured chick muscle cells. J Nutr Sci Vitaminol (Tokyo) 1998, 44:799-807.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
Moore DT, Ferket PR, Mozdziak PE. Early post-hatch fasting induces satellite cell self-renewal. Comp Biochem Physiol A Mol Integr Physiol 2005, 142:331-339. 10.1016/j.cbpa.2005.08.007, 16185905.
Mozdziak PE, Evans JJ, McCoy DW. Early posthatch starvation induces myonuclear apoptosis in chickens. J Nutr 2002, 132:901-903.
Nunes VA, Gozzo AJ, Juliano MA, Cesar MC, Sampaio MU, Sampaio CA. Antioxidant dietary deficiency induces caspase activation in chick skeletal muscle cells. Braz J Med Biol Res 2003, 36:1047-1053.
Pophal S, Evans JJ, Mozdziak PE. Myonuclear apoptosis occurs during early posthatch starvation. Comp Biochem Physiol B Biochem Mol Biol 2003, 135:677-681. 10.1016/S1096-4959(03)00148-9, 12892759.
Salakou S, Kardamakis D, Tsamandas AC, Zolota V, Apostolakis E, Tzelepi V, Papathanasopoulos P, Bonikos DS, Papapetropoulos T, Petsas T, Dougenis D. Increased Bax/Bcl-2 ratio up-regulates caspase-3 and increasesapoptosis in the thymus of patients with myasthenia gravis. In Vivo 2007, 21:123-132.
Chang HK, Shin MS, Yang HY, Lee JW, Kim YS, Lee MH, Kim J, Kim KH, Kim CJ. Amygdalin induces apoptosis through regulation of Bax and Bcl-2expressions in human DU145 and LNCaP prostate cancer cells. Biol Pharm Bull 2006, 29:1597-1602. 10.1248/bpb.29.1597, 16880611.
Oksbjerg N, Gondret F, Vestergaard M. Basic principles of muscle development and growth in meat-producing mammals as affected by the insulin-like growth factor (IGF) system. Domest Anim Endocrinol 2004, 27:219-240. 10.1016/j.domaniend.2004.06.007, 15451071.
Leili S, Buonomo FC, Scanes CG. The effects of dietary restriction on insulin-like growth factor (IGF)-I and II, and IGF-binding proteins in chickens. Proc Soc Exp Biol Med 1997, 216:104-111.
Morishita D, Sasaki K, Wakita M, Hoshino S. Effect of fasting on serum insulin-like growth factor-I (IGF-I) levels and IGF-I-binding activity in cockerels. J Endocrinol 1993, 139:363-370. 10.1677/joe.0.1390363, 7510768.
Kuhn ER, Herremans M, Dewil E, Vanderpooten A, Rudas P, Bartha T, Verheyen G, Berghman L, Decuypere E. Thyrotropin-releasing hormone (TRH) is not thyrotropic but somatotropic in fed and starved adult chickens. Reprod Nutr Dev 1991, 31:431-439. 10.1051/rnd:19910409, 1747201.
Kita K, Tomas FM, Owens PC, Knowles SE, Forbes BE, Upton Z, Hughes R, Ballard FJ. Influence of nutrition on hepatic IGF-I mRNA levels and plasma concentrations of IGF-I and IGF-II in meat-type chickens. J Endocrinol 1996, 149:181-190. 10.1677/joe.0.1490181, 8676050.
Tanaka M, Hayashida Y, Sakaguchi K, Ohkubo T, Wakita M, Hoshino S, Nakashima K. Growth hormone-independent expression of insulin-like growth factor I messenger ribonucleic acid in extrahepatic tissues of the chicken. Endocrinology 1996, 137:30-34. 10.1210/en.137.1.30, 8536628.
Buyse J, Decuypere E. The role of the somatotrophic axis in the metabolism of the chicken. Domest Anim Endocrinol 1999, 17:245-255. 10.1016/S0739-7240(99)00041-7, 10527127.
Levesque HM, Shears MA, Fletcher GL, Moon TW. Myogenesis and muscle metabolism in juvenile Atlantic salmon (Salmo salar) made transgenic for growth hormone. J Exp Biol 2008, 211:128-137. 10.1242/jeb.006890, 18083741.
Ullman M, Oldfors A. Skeletal muscle regeneration in young rats is dependent on growth hormone. J Neurol Sci 1991, 106:67-74. 10.1016/0022-510X(91)90196-E, 1779241.
Florini JR, Ewton DZ, Coolican SA. Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 1996, 17:481-517.
Palmer RM, Thompson MG, Knott RM, Campbell GP, Thom A, Morrison KS. Insulin and insulin-like growth factor-I responsiveness and signalling mechanisms in C2C12 satellite cells: effect of differentiation and fusion. Biochim Biophys Acta 1997, 1355:167-176. 10.1016/S0167-4889(96)00127-9, 9042337.
Rousse S, Montarras D, Pinset C, Dubois C. Up-regulation of insulin-like growth factor binding protein-5 is independent of muscle cell differentiation, sensitive to rapamycin, but insensitive to wortmannin and LY294002. Endocrinology 1998, 139:1487-1493. 10.1210/en.139.4.1487, 9528925.
McFarland DC, Pesall JE, Gilkerson KK. The influence of growth factors on turkey embryonic myoblasts and satellite cells in vitro. Gen Comp Endocrinol 1993, 89:415-424. 10.1006/gcen.1993.1049, 7687577.
Vasilatos-Younken R. Absence of growth hormone-induced avian muscle growth in vivo. Poult Sci 1999, 78:759-768.
Kandalla PK, Goldspink G, Butler-Browne G, Mouly V. Mechano Growth Factor E peptide (MGF-E), derived from an isoform of IGF-1, activates human muscle progenitor cells and induces an increase in their fusion potential at different ages. Mech Ageing Dev 2011, 132:154-162. 10.1016/j.mad.2011.02.007, 21354439.
Marchal S, Cassar-Malek I, Pons F, Wrutniak C, Cabello G. Triiodothyronine influences quail myoblast proliferation and differentiation. Biol Cell 1993, 78:191-197. 10.1016/0248-4900(93)90129-3, 8241960.
Beermann DH, Liboff M, Wilson DB, Hood LF. Effects of exogenous thyroxine and growth hormone on satellite cell and myonuclei populations in rapidly growing rat skeletal muscle. Growth 1983, 47:426-436.
