1932

Abstract

Skeletal muscle growth during the early postnatal period is rapid in the pig and dependent on the capacity of muscle to respond to anabolic and catabolic stimuli. Muscle mass is driven by the balance between protein synthesis and degradation. Among these processes, muscle protein synthesis in the piglet is exceptionally sensitive to the feeding-induced postprandial changes in insulin and amino acids, whereas muscle protein degradation is affected only during specific catabolic states. The developmental decline in the response of muscle to feeding is associated with changes in the signaling pathways located upstream and downstream of the mechanistic target of rapamycin protein complex. Additionally, muscle growth is supported by an accretion of nuclei derived from satellite cells. Activated satellite cells undergo proliferation, differentiation, and fusion with adjacent growing muscle fibers. Enhancing early muscle growth through modifying protein synthesis, degradation, and satellite cell activity is key to maximizing performance, productivity, and lifelong pig health.

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2019-02-15
2024-04-20
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Literature Cited

  1. 1.  Mahan DC, Shields RG Jr 1998. Essential and nonessential amino acid composition of pigs from birth to 145 kilograms of body weight and comparison to other studies. J. Anim. Sci. 76:513–21
    [Google Scholar]
  2. 2.  Davis TA, Fiorotto ML 2009. Regulation of muscle growth in neonates. Curr. Opin. Clin. Nutr. Metab. Care 12:78–85
    [Google Scholar]
  3. 3.  Odle J, Lin X, Jacobi SK, Kim SW, Stahl CH 2014. The suckling piglet as an agrimedical model for the study of pediatric nutrition and metabolism. Annu. Rev. Anim. Biosci. 2:419–44
    [Google Scholar]
  4. 4.  Thivierge MC, Bush JA, Suryawan A, Nguyen HV, Orellana RA et al. 2005. Whole-body and hindlimb protein breakdown are differentially altered by feeding in neonatal piglets. J. Nutr. 135:1430–37
    [Google Scholar]
  5. 5.  Wilson FA, Suryawan A, Orellana RA, Kimball SR, Gazzaneo MC et al. 2009. Feeding rapidly stimulates protein synthesis in skeletal muscle of neonatal pigs by enhancing translation initiation. J. Nutr. 139:1873–80
    [Google Scholar]
  6. 6.  El-Kadi SW, Suryawan A, Gazzaneo MC, Srivastava N, Orellana RA et al. 2012. Anabolic signaling and protein deposition are enhanced by intermittent compared with continuous feeding in skeletal muscle of neonates. Am. J. Physiol. Endocrinol. Metab. 302:E674–86
    [Google Scholar]
  7. 7.  O'Connor PMJ, Bush JA, Suryawan A, Nguyen HV, Davis TA 2003. Insulin and amino acids independently stimulate skeletal muscle protein synthesis in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 284:E110–19
    [Google Scholar]
  8. 8.  Gazzaneo MC, Suryawan A, Orellana RA, Torrazza RM, El-Kadi SW et al. 2011. Intermittent bolus feeding has a greater stimulatory effect on protein synthesis skeletal muscle than continuous feeding in neonatal pigs. J. Nutr. 141:2152–58
    [Google Scholar]
  9. 9.  El-Kadi SW, Boutry C, Gazzaneo MC, Suryawan A, Orellana RA et al. 2012. Lean growth is enhanced by intermittent bolus feeding compared with continuous feeding in neonates. FASEB J 26:Suppl.42.3
    [Google Scholar]
  10. 10.  Davis TA, Fiorotto ML, Burrin DG, Reeds PJ, Nguyen HV et al. 2002. Stimulation of protein synthesis by both insulin and amino acids is unique to skeletal muscle in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 282:E880–90
    [Google Scholar]
  11. 11.  Barazzoni R, Short KR, Asmann Y, Coenen-Schimke JM, Robinson MM, Nair KS 2012. Insulin fails to enhance mTOR phosphorylation, mitochondrial protein synthesis, and ATP production in human skeletal muscle without amino acid replacement. Am. J. Physiol. Endocrinol. Metab. 309:E1117–25
    [Google Scholar]
  12. 12.  Everman S, Meyer C, Tran L, Hoffman N, Carroll CC et al. 2016. Insulin does not stimulate muscle protein synthesis during increased plasma branched-chain amino acids alone but still decreases whole body proteolysis in humans. Am. J. Physiol. Endocrinol. Metab. 311:E671–77
    [Google Scholar]
  13. 13.  Saxton RA, Sabatini DM 2017. mTOR signaling in growth, metabolism, and disease. Cell 168:960–76
    [Google Scholar]
  14. 14.  Nojima H, Tokunaga C, Eguchi S, Oshiro N, Hidayat S et al. 2003. The mammalian target of rapamycin (mTOR) partner, raptor, binds the mTOR substrates p70 S6 kinase and 4E-BP1 through their TOR signaling (TOS) motifs. J. Biol. Chem. 278:15461–64
    [Google Scholar]
  15. 15.  Ma XM, Blenis J 2009. Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10:307–18
    [Google Scholar]
  16. 16.  Suryawan A, Orellana RA, Nguyen HV, Jeyapalan AS, Fleming JR, Davis TA 2007. Activation by insulin and amino acids of signaling components leading to translation initiation in skeletal muscle of neonatal pigs is developmentally regulated. Am. J. Physiol. Endocrinol. Metab. 293:E1597–605
    [Google Scholar]
  17. 17.  Inoki K, Li Y, Zhu T, Wu J, Guan KL 2003. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev 17:1829–34
    [Google Scholar]
  18. 18.  Garami A, Zwartkruis FJ, Nobukuni T, Joaquin M, Roccio M et al. 2003. Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol. Cell 11:1457–66
    [Google Scholar]
  19. 19.  Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y et al. 2006. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126:955–68
    [Google Scholar]
  20. 20.  Liu L, Cash TP, Jones RG, Keith B, Thompson CB, Simon MC 2006. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol. Cell 21:521–31
    [Google Scholar]
  21. 21.  Nicklin P, Bergman P, Zhang B, Triantafellow E, Wang B et al. 2009. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 136:521–34
    [Google Scholar]
  22. 22.  Boutry C, El-Kadi SW, Suryawan A, Steinhoff-Wagner J, Stoll B et al. 2016. Pulsatile delivery of a leucine supplement during long-term continuous enteral feeding enhances lean growth in term neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 310:E699–713
    [Google Scholar]
  23. 23.  Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC et al. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496–501
    [Google Scholar]
  24. 24.  Bar-Peled L, Schweitzer LD, Zoncu R, Sabatini DM 2012. Ragulator is a GEF for the rag GTPases that signal amino acid levels to mTORC1. Cell 150:1196–208
    [Google Scholar]
  25. 25.  Bar-Peled L, Chantranupong L, Cherniack AD, Chen WW, Ottina KA et al. 2013. A tumor suppressor complex with GAP activity for the Rag GTPases that signal amino acid sufficiency to mTORC1. Science 340:1100–6
    [Google Scholar]
  26. 26.  Wolfson RL, Chantranupong L, Wyant GA, Gu X, Orozco JM et al. 2017. KICSTOR recruits GATOR1 to the lysosome and is necessary for nutrients to regulate mTORC1. Nature 543:438–42
    [Google Scholar]
  27. 27.  Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM 2011. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires vacuolar H+-ATPase. Science 334:678–83
    [Google Scholar]
  28. 28.  Jewell JL, Kim YC, Russell RC, Yu F, Park HW et al. 2015. Differential regulation of mTORC1 by leucine and glutamine. Science 347:194–98
    [Google Scholar]
  29. 29.  Wolfson RL, Chantranupong L, Saxton RA, Shen K, Scaria SM et al. 2016. Sestrin2 is a leucine sensor for the mTORC1 pathway. Science 351:43–48
    [Google Scholar]
  30. 30.  Suryawan A, Davis TA 2018. Amino acid- and insulin-induced activation of mTORC1 in neonatal piglet skeletal muscle involves Sestrin2-GATOR2, Rag A/C-mTOR, and RHEB-mTOR complex formation. J. Nutr. 148:825–33
    [Google Scholar]
  31. 31.  Han JM, Jeong SJ, Park MC, Kim G, Kwon NH et al. 2012. Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell 149:410–24
    [Google Scholar]
  32. 32.  Chantranupong L, Scaria SM, Saxton RA, Gygi MP, Shen K et al. 2016. The CASTOR proteins are arginine sensors for the mTORC1 pathway. Cell 165:153–64
    [Google Scholar]
  33. 33.  Wyant GA, Abu-Remaileh M, Wolfson RL, Chen WW, Freinkman E et al. 2017. mTORC1 activator SLC38A9 is required to efflux essential amino acids from lysosomes and use protein as a nutrient. Cell 171:642–54
    [Google Scholar]
  34. 34.  Anthony JC, Yoshizawa F, Anthony TG, Vary TC, Jefferson LS, Kimball SR 2000. Orally administered leucine stimulates protein synthesis in skeletal muscle of postabsorptive rats in association with increased eIF4F formation. J. Nutr. 130:139–45
    [Google Scholar]
  35. 35.  Escobar J, Frank JW, Suryawan A, Nguyen HV, Kimball SR et al. 2005. Physiological rise in plasma leucine stimulates muscle protein synthesis in neonatal pigs by enhancing translation initiation factor activation. Am. J. Physiol. Endocrinol. Metab. 288:E914–21
    [Google Scholar]
  36. 36.  Suryawan A, Jeyapalan AS, Orellana RA, Wilson FA, Nguyen HV, Davis TA 2008. Leucine stimulates protein synthesis in skeletal muscle of neonatal pigs by enhancing mTORC1 activation. Am. J. Physiol. Endocrinol. Metab. 295:E868–75
    [Google Scholar]
  37. 37.  Naberhuis J, Suryawan A, Nguyen HV, Hernandez-Garcia A, Fiorotto ML et al. 2017. Prematurity blunts feeding-induced stimulation of translation initiation signaling and protein synthesis in muscle of neonatal piglets. FASEB J 31:Suppl.141.8
    [Google Scholar]
  38. 38.  Escobar J, Frank JW, Suryawan A, Nguyen HV, Davis TA 2007. Amino acid availability and age affect the leucine stimulation of protein synthesis and eIF4F formation in muscle. Am. J. Physiol. Endocrinol. Metab. 293:E1615–21
    [Google Scholar]
  39. 39.  Wilson FA, Suryawan A, Gazzaneo MC, Orellana RA, Nguyen HV, Davis TA 2010. Stimulation of muscle protein synthesis by prolonged parenteral infusion of leucine is dependent on amino acid availability in neonatal pigs. J. Nutr. 140:264–70
    [Google Scholar]
  40. 40.  Columbus DA, Steinhoff-Wagner J, Suryawan A, Nguyen HV, Hernandez-Garcia A et al. 2015. Impact of prolonged leucine supplementation on protein synthesis and lean growth in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 309:E601–10
    [Google Scholar]
  41. 41.  Manjarín R, Columbus DA, Suryawan A, Nguyen HV, Hernandez-Garcia A et al. 2016. Leucine supplementation of a chronically restricted protein and energy diet enhances mTOR pathway activation but not muscle protein synthesis in neonatal pigs. Amino Acids 48:257–67
    [Google Scholar]
  42. 42.  Manjarín R, Columbus DA, Solis J, Hernandez-García AD, Suryawan A et al. 2018. Short and long-term effects of leucine and branched-chain amino acid supplementation of a protein- and energy-reduced diet on muscle protein metabolism in neonatal pigs. Amino Acids 50:943–59
    [Google Scholar]
  43. 43.  Suryawan A, Hawes JW, Harris RA, Shimomura Y, Jenkins AE, Hutson SM 1998. A molecular model of human branched-chain amino acid metabolism. Am. J. Clin. Nutr. 68:72–81
    [Google Scholar]
  44. 44.  Van Koevering M, Nissen S 1992. Oxidation of leucine and alpha-ketoisocaproate to beta-hydroxy-beta-methylbutyrate in vivo. Am. J. Physiol. Endocrinol. Metab. 262:E27–31
    [Google Scholar]
  45. 45.  Escobar J, Frank JW, Suryawan A, Nguyen HV, Van Horn CG et al. 2010. Leucine and α-ketoisocaproic acid, but not norleucine, stimulate skeletal muscle protein synthesis in neonatal pigs. J. Nutr. 140:1418–24
    [Google Scholar]
  46. 46.  Zanchi NE, Gerlinger-Romero F, Guimarães-Ferreira L, de Siqueira Filho MA, Felitti V et al. 2011. HMB supplementation: clinical and athletic performance-related effects and mechanisms of action. Amino Acids 40:1015–25
    [Google Scholar]
  47. 47.  Wheatley SM, El-Kadi SW, Suryawan A, Boutry C, Orellana RA et al. 2014. Protein synthesis in skeletal muscle of neonatal pigs is enhanced by administration of β-hydroxy-β-methylbutyrate. Am. J. Physiol. Endocrinol. Metab. 306:E91–99
    [Google Scholar]
  48. 48.  Kao M, Columbus DA, Suryawan A, Steinhoff-Wagner J, Hernandez-Garcia A et al. 2016. Enteral β-hydroxy-β-methylbutyrate supplementation increases protein synthesis in skeletal muscle of neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 310:E1072–84
    [Google Scholar]
  49. 49.  Eley HL, Russell ST, Baxter JH, Mukerji P, Tisdale MJ 2007. Signaling pathways initiated by β-hydroxy-β-methylbutyrate to attenuate the depression of protein synthesis in skeletal muscle in response to cachectic stimuli. Am. J. Physiol. Endocrinol. Metab. 293:E923–31
    [Google Scholar]
  50. 50.  Marini JC, Agarwal U, Robinson JL, Yuan Y, Didelija IC et al. 2017. The intestinal-renal axis for arginine synthesis is present and functional in the neonatal pig. Am. J. Physiol. Endocrinol. Metab. 313:E233–42
    [Google Scholar]
  51. 51.  Kim SW, McPherson RL, Wu G 2004. Dietary arginine supplementation enhances the growth of milk-fed young pigs. J. Nutr. 134:625–30
    [Google Scholar]
  52. 52.  Frank JW, Escobar J, Nguyen HV, Jobgen SC, Jobgen WS et al. 2007. Oral N-carbamylglutamate supplementation increases protein synthesis in skeletal muscle of piglets. J. Nutr. 137:315–19
    [Google Scholar]
  53. 53.  Yao K, Yin Y, Chu W, Liu Z, Deng D et al. 2008. Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. J. Nutr. 138:867–72
    [Google Scholar]
  54. 54.  Mateo RD, Wu G, Moon HK, Carroll JA, Kim SW 2008. Effects of dietary arginine supplementation during gestation and lactation on the performance of lactating primiparous sows and nursing piglets. J. Anim. Sci. 86:827–35
    [Google Scholar]
  55. 55.  Hurley WL 2015. Composition of sow colostrum and milk. The Gestating and Lactating Sow C Farmer 193–229 Wageningen, Neth: Wageningen Acad
    [Google Scholar]
  56. 56.  Burrin DG, Davis TA, Ebner S, Schoknecht PA, Fiorotto ML et al. 1995. Nutrient-independent and nutrient-dependent factors stimulate protein synthesis in colostrum-fed newborn pigs. Pediatr. Res. 37:593–99
    [Google Scholar]
  57. 57.  Fiorotto ML, Davis TA, Reeds PJ 2000. Regulation of myofibrillar protein turnover during maturation in normal and undernourished rat pups. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278:R845–54
    [Google Scholar]
  58. 58.  Sandri M 2013. Protein breakdown in muscle wasting: role of autophagy-lysosome and ubiquitin-proteasome. Int. J. Biochem. Cell Biol. 45:2121–29
    [Google Scholar]
  59. 59.  Smith IJ, Dodd SL 2008. Calpain activation causes a proteasome-dependent increase in protein degradation and inhibits the Akt signaling pathway in rat diaphragm muscle. Exp. Physiol. 92:561–73
    [Google Scholar]
  60. 60.  Bodine SC, Latres E, Baumhueter S, Lai VKM, Nunez L et al. 2001. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:1704–8
    [Google Scholar]
  61. 61.  Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V et al. 2004. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18:39–51
    [Google Scholar]
  62. 62.  Zhao J, Brault JJ, Schild A, Cao P, Sandri M et al. 2007. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6:472–83
    [Google Scholar]
  63. 63.  Boutry C, El-Kadi SW, Suryawan A, Wheatley SM, Orellana RA et al. 2013. Leucine pulses enhance skeletal muscle protein synthesis during continuous feeding in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 305:E620–31
    [Google Scholar]
  64. 64.  Suryawan A, Davis TA 2014. Regulation of protein degradation pathways by amino acids and insulin in skeletal muscle of neonatal pigs. J. Anim. Sci. Biotechnol. 5:8–19
    [Google Scholar]
  65. 65.  Breuille DF, Arnal M, Rambourdin F, Bayle G, Levieux D, Obled C 1998. Sustained modifications of protein metabolism in various tissues in a rat model of long-lasting sepsis. Clin. Sci. 94:413–24
    [Google Scholar]
  66. 66.  Bruins MJ, Deutz NEP, Soeters PB 2003. Aspects of organ protein, amino acid, and glucose metabolism in a porcine model of hypermetabolic sepsis. Clin. Sci. 104:127–41
    [Google Scholar]
  67. 67.  Orellana RA, Suryawan A, Wilson FA, Gazzaneo MC, Fiorotto ML et al. 2012. Development aggravates the severity of skeletal muscle catabolism induced by endotoxemia in neonatal pigs. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302:R682–90
    [Google Scholar]
  68. 68.  McPherron AC, Lee SJ 1997. Double muscling in cattle due to mutations in the myostatin gene. PNAS 94:12457–61
    [Google Scholar]
  69. 69.  McPherron AC, Lawler AM, Lee SJ 1997. Regulation of skeletal muscle mass in mice by a new TGF-β superfamily member. Nature 387:83–90
    [Google Scholar]
  70. 70.  Amirouche A, Durieux A, Banzet S, Koulmann N, Bonnefoy R et al. 2009. Down-regulation of Akt/mammalian target of rapamycin signaling pathway in response to myostatin overexpression in skeletal muscle. Endocrinology 150:286–94
    [Google Scholar]
  71. 71.  Cai C, Qian L, Jiang S, Sun Y, Wang Q et al. 2017. Loss-of-function myostatin mutation increases insulin sensitivity and browning of white fat in Meishan pigs. Oncotarget 8:34911–22
    [Google Scholar]
  72. 72.  Hennebry A, Oldham J, Shavlakadze T, Grounds MD, Sheard P et al. 2017. IGF1 stimulates greater muscle hypertrophy in the absence of myostatin in male mice. J. Endocrinol. 234:187–200
    [Google Scholar]
  73. 73.  Lang CH, Frost RA 2004. Differential effect of sepsis on ability of leucine and IGF-1 to stimulate translation initiation. Am. J. Physiol. Endocrinol. Metab. 287:E721–30
    [Google Scholar]
  74. 74.  Lang CH, Frost RA 2005. Endotoxin disrupts the leucine-signaling pathway involving phosphorylation of mTOR, 4E-BP1, and S6K1 in skeletal muscle. J. Cell. Physiol. 203:144–55
    [Google Scholar]
  75. 75.  Breuille DF, Rose F, Arnal M, Melin C, Obled C 1994. Sepsis modifies the contribution of different organs to whole-body protein synthesis in rats. Clin. Sci. 86:663–69
    [Google Scholar]
  76. 76.  Orellana RA, O'Connor PMJ, Nguyen HV, Bush JA, Suryawan A et al. 2002. Endotoxemia reduces skeletal muscle protein synthesis in neonates. Am. J. Physiol. Endocrinol. Metab. 283:E909–16
    [Google Scholar]
  77. 77.  Hernandez-García AD, Columbus DA, Manjarin R, Nguyen HV, Suryawan A et al. 2016. Leucine supplementation stimulates protein synthesis and reduces degradation signal activation in muscle of newborn pigs during acute endotoxemia. Am. J. Physiol. Endocrinol. Metab. 311:E791–801
    [Google Scholar]
  78. 78.  Mackenzie ML, Warren MR, Wykes LJ 2003. Colitis increases albumin synthesis at the expense of muscle protein synthesis in macronutrient-restricted pigs. J. Nutr. 133:1875–81
    [Google Scholar]
  79. 79.  Lang CH, Frost RA 2006. Glucocorticoids and TNFα interact cooperatively to mediate sepsis-induced leucine resistance in skeletal muscle. Mol. Med. 12:291–99
    [Google Scholar]
  80. 80.  Lebrun P, van Obberghen E 2007. SOCS proteins causing trouble in insulin action. Acta Physiol 192:29–36
    [Google Scholar]
  81. 81.  Shimizu N, Yoshikawa N, Ito N, Maruyama T, Suzuki Y et al. 2011. Crosstalk between glucocorticoid receptor and nutritional sensor mTOR in skeletal muscle. Cell Metab 13:170–82
    [Google Scholar]
  82. 82.  Gilson H, Schakman O, Combaret L, Lause P, Grobet L et al. 2007. Myostatin gene deletion prevents glucocorticoid-induced muscle atrophy. Endocrinology 148:452–60
    [Google Scholar]
  83. 83.  Orellana RA, O'Connor PMJ, Bush JA, Suryawan A, Thivierge MC et al. 2006. Modulation of muscle protein synthesis by insulin is maintained during neonatal endotoxemia. Am. J. Physiol. Endocrinol. Metab. 291:E159–66
    [Google Scholar]
  84. 84.  Orellana RA, Jeyapalan A, Escobar J, Frank JW, Nguyen HV et al. 2007. Amino acids augment muscle protein synthesis in neonatal pigs during acute endotoxemia by stimulating mTOR-dependent translation initiation. Am. J. Physiol. Endocrinol. Metab. 293:E1416–25
    [Google Scholar]
  85. 85.  Kazi AA, Pruznak AM, Frost RA, Lang CH 2011. Sepsis-induced alterations in protein-protein interactions within mTOR complex 1 and the modulating effect of leucine on muscle protein synthesis. Shock 35:117–25
    [Google Scholar]
  86. 86.  Davis TA, Burrin DG, Fiorotto ML, Nguyen HV 1996. Protein synthesis in skeletal muscle and jejunum is more responsive to feeding in 7- than in 26-day-old pigs. Am. J. Physiol. Endocrinol. Metab. 270:E802–9
    [Google Scholar]
  87. 87.  Davis TA, Fiorotto ML, Beckett PR, Burrin DG, Reeds PJ et al. 2001. Differential effects of insulin on peripheral and visceral tissue protein synthesis in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 280:E770–79
    [Google Scholar]
  88. 88.  Suryawan A, Nguyen HV, Bush JA, Davis TA 2001. Developmental changes in the feeding-induced activation of the insulin-signaling pathway in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 281:E908–15
    [Google Scholar]
  89. 89.  Suryawan A, Escobar J, Frank JW, Nguyen HV, Davis TA 2006. Developmental regulation of the activation of signaling components leading to translation initiation in skeletal muscle of neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 291:E849–59
    [Google Scholar]
  90. 90.  Suryawan A, Nguyen HV, Almonaci RD, Davis TA 2013. Abundance of amino acid transporters involved in mTORC1 activation in skeletal muscle of neonatal pigs is developmentally regulated. Amino Acids 45:523–30
    [Google Scholar]
  91. 91.  Suryawan A, Frank JW, Nguyen HV, Davis TA 2006. Expression of the TGF-β family of ligands is developmentally regulated in skeletal muscle of neonatal rats. Pediatr. Res. 59:175–79
    [Google Scholar]
  92. 92.  White RB, Bierinx AS, Gnocchi VF, Zammit PS 2010. Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev. Biol. 10:21–31
    [Google Scholar]
  93. 93.  Campion DR, Richardson RL, Reagan JO, Kraeling RR 1981. Changes in the satellite cell population during postnatal growth of pig skeletal muscle. J. Anim. Sci. 54:1014–18
    [Google Scholar]
  94. 94.  Mesires NT, Doumit ME 2002. Satellite cell proliferation and differentiation during postnatal growth of porcine skeletal muscle. Am. J. Physiol. Cell Physiol. 282:C899–906
    [Google Scholar]
  95. 95.  Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA 2000. Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–86
    [Google Scholar]
  96. 96.  Relaix F, Rocancourt D, Mansouri A, Buckingham MA 2005. Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948–53
    [Google Scholar]
  97. 97.  Schultz E 1996. Satellite cell proliferative compartments in growing skeletal muscles. Dev. Biol. 175:84–94
    [Google Scholar]
  98. 98.  Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA et al. 2006. Pax7 and myogenic progression in skeletal muscle satellite cells. J. Cell Sci. 119:1824–32
    [Google Scholar]
  99. 99.  Miersch C, Stange K, Hering S, Kolisek M, Viergutz T, Rontgen M 2017. Molecular and functional heterogeneity of early postnatal porcine satellite cell populations is associated with bioenergetic profile. Sci. Rep. 7:45052–65
    [Google Scholar]
  100. 100.  Chen Y, Zhu H, McCauley SR, Zhao L, Johnson SE et al. 2017. Diminished satellite cell fusion and S6K1 expression in myotubes derived from skeletal muscle of low birth weight neonatal pigs. Physiol. Rep. 5:e13075–85
    [Google Scholar]
  101. 101.  Lepper C, Conway SJ, Fan CM 2009. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460:627–31
    [Google Scholar]
  102. 102.  Kawano F, Takeno Y, Nakai N, Higo Y, Terada M et al. 2008. Essential role of satellite cells in the growth of rat soleus muscle fibers. Am. J. Physiol. Cell Physiol. 295:C458–67
    [Google Scholar]
  103. 103.  Dellavalle A, Maroli G, Covarello D, Azzoni E, Innocenzi A et al. 2011. Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat. Commun. 2:499–509
    [Google Scholar]
  104. 104.  Sambasivan R, Yao R, Kissenpfennig A, van Wittenberghe L, Paldi A et al. 2011. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138:3647–56
    [Google Scholar]
  105. 105.  McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K et al. 2011. Effective fiber hypertrophy in satellite-cell depleted skeletal muscle. Development 138:3657–66
    [Google Scholar]
  106. 106.  Egner IM, Bruusgaard JC, Gunderson K 2016. Satellite cell depletion prevents fiber hypertrophy in skeletal muscle. Development 143:2898–906
    [Google Scholar]
  107. 107.  Blaauw B, Canato M, Agatea L, Toniolo L, Mammucari C et al. 2009. Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation. FASEB J 23:3896–905
    [Google Scholar]
  108. 108.  Dhawan J, Rando TA 2005. Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation, and replenishment. Trends Cell Biol 15:666–73
    [Google Scholar]
  109. 109.  Fry CS, Kirby TJ, Kosmac K, McCarthy JJ, Peterson CA 2017. Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy. Cell Stem Cell 20:56–69
    [Google Scholar]
  110. 110.  Tatsumi R, Allen RE 2004. Active hepatocyte growth factor is present in skeletal muscle extracellular matrix. Muscle Nerve 30:654–58
    [Google Scholar]
  111. 111.  Yamada M, Sankoda Y, Tatsumi R, Minunoya W, Ikeuchi Y et al. 2008. Matrix metalloproteinase-2 mediates stretch-induced activation of skeletal muscle satellite cells in a nitric oxide-dependent manner. Int. J. Biochem. Cell Biol. 40:2183–91
    [Google Scholar]
  112. 112.  Doumit ME, Cook DR, Merkel RA 1993. Fibroblast growth factor, epidermal growth factor, insulin-like growth factors, and platelet-derived growth factor-BB stimulate proliferation of clonally derived porcine myogenic satellite cells. J. Cell. Physiol. 157:326–32
    [Google Scholar]
  113. 113.  Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE 1998. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev. Biol. 194:114–28
    [Google Scholar]
  114. 114.  Tatsumi R 2010. Mechano-biology of skeletal muscle hypertrophy and regeneration: possible mechanism of stretch-induced activation of resident myogenic stem cells. Anim. Sci. J. 81:11–20
    [Google Scholar]
  115. 115.  Leshem Y, Spider DB, Gai-Levi R, Halevy O 2000. Hepatocyte growth factor (HGF) inhibits skeletal muscle cell differentiation: a role for the bHLH protein twist and the cdk inhibitor p27. J. Cell. Physiol. 184:101–9
    [Google Scholar]
  116. 116.  Yamada S, Buffinger N, DiMario J, Strohman RC 1989. Fibroblast growth factor is stored in fiber extracellular matrix and plays a role in regulating muscle hypertrophy. Med. Sci. Sports Exerc. 21:S173–80
    [Google Scholar]
  117. 117.  Kastner S, Elias MC, Rivera AJ, Yablonka-Reuveni Z 2000. Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J. Histochem. Cytochem. 48:1079–96
    [Google Scholar]
  118. 118.  Scata KA, Bernard DW, Fox J, Swain JL 1999. FGF receptor availability regulates skeletal myogenesis. Exp. Cell Res. 250:10–21
    [Google Scholar]
  119. 119.  Yakar S, Liu JL, Stannard B, Butler A, Accili D et al. 1999. Normal growth and development in the absence of hepatic insulin-like growth factor 1. PNAS 96:7324–29
    [Google Scholar]
  120. 120.  Gerrard DE, Okamura CS, Ranalletta MA, Grant AL 1998. Developmental expression and location of IGF-I and IGF-II mRNA and protein in skeletal muscle. J. Anim. Sci. 76:1004–11
    [Google Scholar]
  121. 121.  Adi S, Cheng Z, Zhang P, Wu N, Mellon SH, Rosenthal SM 2000. Opposing early inhibitory and late stimulatory effects of insulin-like growth factor-1 on myogenin gene transcription. J. Cell. Biochem. 78:617–26
    [Google Scholar]
  122. 122.  Adi S, Bin-Abbas B, Wu N, Rosenthal SM 2002. Early stimulation and late inhibition of extracellular signal-related kinase 1/2 phosphorylation by IGF-1: a potential mechanism mediating the switch in IGF-1 action on skeletal muscle cell differentiation. Endocrinology 143:511–16
    [Google Scholar]
  123. 123.  Matheny RW Jr, Nindl BC, Adamo ML 2010. Mechano-growth factor: a putative product of IGF-1 gene expression involved in tissue regeneration and repair. Endocrinology 151:865–75
    [Google Scholar]
  124. 124.  Yang SY, Goldspink G 2002. Different roles of the IGF-1Ec peptide (MGF) and mature IGF-1 in myoblast proliferation and differentiation. FEBS Lett 522:156–60
    [Google Scholar]
  125. 125.  Qin L, Li X, Xu J, Mo D, Tong X et al. 2012. Mechano growth factor (MGF) promotes proliferation and inhibits differentiation of porcine satellite cells (PSCs) by down-regulation of key myogenic transcriptional factors. Mol. Cell. Biochem. 370:221–30
    [Google Scholar]
  126. 126.  Fornaro M, Hinken AC, Needle S, Hu E, Trendelenburg A et al. 2014. Mechano-growth factor peptide, the COOH terminus of unprocessed insulin-like growth factor 1, has no apparent effect on myoblasts or primary muscle stem cells. Am. J. Physiol. Endocrinol. Metab. 306:E150–56
    [Google Scholar]
  127. 127.  Conboy IM, Rando TA 2002. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 3:397–409
    [Google Scholar]
  128. 128.  Wen Y, Bi P, Liu W, Asakura A, Keller C, Kuang S 2012. Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol. Cell. Biol. 32:2300–11
    [Google Scholar]
  129. 129.  Qin L, Xu J, Wu Z, Zhang Z, Li J et al. 2013. Notch-1 mediated signaling regulates proliferation of porcine satellite cells (PSCs). Cell. Signal. 25:561–69
    [Google Scholar]
  130. 130.  Golpinath SD, Webb AE, Brunet A, Rando TA 2014. FOXO3 promotes quiescence in adult muscle stem cells during the process of self-renewal. Stem Cell Rep 2:414–26
    [Google Scholar]
  131. 131.  von Maltzahn J, Chang NC, Bentzinger CF, Rudnicki MA 2012. Wnt signaling in myogenesis. Trends Cell Biol 22:602–9
    [Google Scholar]
  132. 132.  Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA 2008. A temporal switch from Notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2:50–59
    [Google Scholar]
  133. 133.  van der Velden JLJ, Langen RCJ, Kelders MCJM, Wouters EFM, Janssen-Heininger YMW, Schols AMWJ 2006. Inhibition of glycogen synthase kinase-3β activity is sufficient to stimulate myogenic differentiation. Am. J. Physiol. Cell Physiol. 290:C453–62
    [Google Scholar]
  134. 134.  Le Grand F, Jones AE, Seale V, Scime A, Rudnicki MA 2009. Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4:535–47
    [Google Scholar]
  135. 135.  Bentzinger CF, Wang YX, von Maltzahn J, Soleimani VD, Yin H, Rudnicki MA 2013. Fibronectin regulates Wnt7a signaling and satellite cell expansion. Cell Stem Cell 12:75–87
    [Google Scholar]
  136. 136.  Horsley V, Jansen KM, Mills ST, Pavlath GK 2003. IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 113:483–94
    [Google Scholar]
  137. 137.  Serrano AL, Baeza-Raja B, Perdiguero E, Jardí M, Muñoz-Cánoves P 2008. Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 7:33–44
    [Google Scholar]
  138. 138.  Guerci A, Lahoute C, Hebrard S, Collard L, Graindorge D et al. 2012. Srf-dependent paracrine signals produced by myofibers control satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 15:25–37
    [Google Scholar]
  139. 139.  Amthor H, Otto A, Vulin A, Rochat A, Dumonceaux J et al. 2009. Muscle hypertrophy driven by myostatin blockade does not require stem/precursor-cell activity. PNAS 106:7479–84
    [Google Scholar]
  140. 140.  Lee S, Huynh TV, Lee Y, Sebald SM, Wilcox-Adelman SA et al. 2012. Role of satellite cells versus myofibers in muscle hypertrophy induced by inhibition of the myostatin/activin signaling pathway. PNAS 109:E2353–60
    [Google Scholar]
  141. 141.  Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ 2009. Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am. J. Physiol. Cell Physiol. 296:C1258–70
    [Google Scholar]
  142. 142.  Gilson H, Schakman O, Kalista S, Lause P, Tsuchida K, Thissen J 2009. Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin. Am. J. Physiol. Endocrinol. Metab. 297:E157–64
    [Google Scholar]
  143. 143.  Jones AE, Price FD, Le Grand F, Soleimani VD, Dick SA et al. 2015. Wnt/β-catenin controls follistatin signaling to regulate satellite cell myogenic potential. Skelet. Muscle 5:14–24
    [Google Scholar]
  144. 144.  Stantzou A, Schirwis E, Swist S, Alonso-Martin S, Polydorou I et al. 2017. BMP signaling regulates satellite cell-dependent postnatal muscle growth. Development 144:2737–47
    [Google Scholar]
  145. 145.  Gokulakrishnan G, Chang X, Fleischmann R, Fiorotto ML 2017. Precocious glucocorticoid exposure reduces skeletal muscle satellite cells in the fetal rat. J. Endocrinol. 232:561–72
    [Google Scholar]
  146. 146.  Dong Y, Pan JS, Zhang L 2013. Myostatin suppression of Akirin1 mediates glucocorticoid-induced satellite cell dysfunction. PLOS ONE 8:e58554–66
    [Google Scholar]
  147. 147.  Glore SR, Layman DK 1983. Cellular development of skeletal muscle during early periods of nutritional restriction and subsequent rehabilitation. Pediatr. Res. 17:602–5
    [Google Scholar]
  148. 148.  Fiorotto ML, Columbus DA, Steinhoff-Wagner J, Suryawan A, Nguyen HV, Davis TA 2016. Postnatal muscle growth is dependent on satellite cell proliferation which demonstrates a specific requirement for dietary protein. FASEB J 30:Suppl.1244.1
    [Google Scholar]
  149. 149.  Han B, Tong J, Zhu MJ, Ma C, Du M 2008. Insulin-like growth factor-1 (IGF-1) and leucine activate pig myogenic satellite cells through mammalian target of rapamycin (mTOR) pathway. Mol. Reprod. Dev. 75:810–17
    [Google Scholar]
  150. 150.  Kornasio R, Riederer I, Butler-Browne G, Mouly V, Uni Z, Halevy O 2009. β-hydroxy-β-methylbutyrate (HMB) stimulates myogenic cell proliferation, differentiation, and survival via the MAPK/ERK and PI3K/Akt pathways. Biochim. Biophys. Acta 1793:755–63
    [Google Scholar]
  151. 151.  Foxcroft GR, Dixon WT, Novak S, Putman CT, Town SC, Vinsky MDA 2006. The biological basis for prenatal programming of postnatal performance in pigs. J. Anim. Sci. 84:E. Suppl.E105–12
    [Google Scholar]
  152. 152.  Milligan BN, Fraser D, Kramer DL 2002. Within-litter birth weight variation in the domestic pig and its relation to pre-weaning survival, weight gain, and variation in weaning weights. Livest. Prod. Sci. 76:181–91
    [Google Scholar]
  153. 153.  Dwyer CM, Fletcher JM, Stickland NC 1994. Muscle cellularity and postnatal growth in the pig. J. Anim. Sci. 71:3339–43
    [Google Scholar]
  154. 154.  Wigmore PMC, Stickland NC 1983. Muscle development in large and small pig fetuses. J. Anat. 137:235–45
    [Google Scholar]
  155. 155.  Fiorotto ML 2012. The making of a muscle. Biochemist 34:4–11
    [Google Scholar]
  156. 156.  Rehfeldt C, Kuhn G, Vanselow J, Furbass R, Fielder I et al. 2001. Maternal treatment with somatotropin during early gestation affects basic events of myogenesis. Cell Tissue Res 306:429–40
    [Google Scholar]
  157. 157.  Berard J, Kalbe C, Losel D, Tuchscherer A, Rehfeldt C 2011. Potential sources of early-postnatal increase in myofiber number in pig skeletal muscle. Histochem. Cell Biol. 136:217–25
    [Google Scholar]
  158. 158.  Dwyer CM, Stickland NC, Fletcher JM 1994. The influence of maternal nutrition on muscle fiber development in the porcine foetus and on subsequent postnatal growth. J. Anim. Sci. 72:911–17
    [Google Scholar]
  159. 159.  Fahey AJ, Brameld JM, Parr T, Buttery PJ 2005. The effect of maternal undernutrition before muscle differentiation on the muscle fiber development of the newborn lamb. J. Anim. Sci. 83:2564–71
    [Google Scholar]
  160. 160.  Nissen PM, Danielsen VO, Jorgensen PF, Oksbjerg N 2003. Increased maternal nutrition of sows has no beneficial effects on muscle fiber number or postnatal growth and has no impact on the meat quality of the offspring. J. Anim. Sci. 81:3018–27
    [Google Scholar]
  161. 161.  Rehfeldt C, Lefaucheur L, Block J, Stabenow B, Pfuhl R et al. Limited and excess protein intake of pregnant gilts differently affects body composition and cellularity of skeletal muscle and subcutaneous adipose tissue of newborn and weanling piglets. Eur. J. Nutr. 51:151–65
    [Google Scholar]
  162. 162.  Brown LD, Hay WW 2016. Impact of placental insufficiency on fetal skeletal muscle growth. Mol. Cell. Endocrinol. 435:69–77
    [Google Scholar]
  163. 163.  Pardo CE, Berard J, Kreuzer M, Bee G 2013. Intrauterine crowding impairs formation and growth of secondary myofibers in pigs. Animal 7:430–38
    [Google Scholar]
  164. 164.  Rosario FJ, Jansson N, Kanai Y, Prasad PD, Powell TL, Jansson T 2011. Maternal protein restriction in the rat inhibits placental insulin, mTOR, and STAT3 signaling and down-regulates placental amino acid transporters. Endocrinology 152:1119–29
    [Google Scholar]
  165. 165.  Yates DT, Clarke DS, Macko AR, Anderson MJ, Shelton LA et al. Myoblasts from intrauterine growth-restricted sheep fetuses exhibit intrinsic deficiencies in proliferation that contribute to smaller semitendinosus myofibers. J. Physiol. 592:3113–25
    [Google Scholar]
  166. 166.  Soto SM, Black AC, Wesolowski SR, Rozance PJ, Barthel KB et al. 2017. Myoblast replication is reduced in the IUGR fetus despite maintained proliferative capacity in vitro. J. . Endocrinol 232:475–91
    [Google Scholar]
  167. 167.  Wu G, Bazer FW, Burghardt RC, Johnson GA, Kim SW et al. 2010. Impacts of amino acid nutrition on pregnancy outcome in pigs: mechanisms and implications for swine production. J. Anim. Sci. 88:E. Suppl.E195–204
    [Google Scholar]
  168. 168.  Mateo RD, Wu G, Bazer FW, Park JC, Shinzato I, Kim SW 2007. Dietary l-arginine supplementation enhances the reproductive performance of gilts. J. Anim. Sci. 137:652–56
    [Google Scholar]
  169. 169.  Madsen JG, Pardo C, Kreuzer M, Bee G 2017. Impact of dietary l-arginine supply during early gestation on myofiber development in newborn pigs exposed to intrauterine crowding. J. Anim. Sci. Biotechnol. 8:58–69
    [Google Scholar]
  170. 170.  Bourdon A, Parnet P, Nowak C, Tran NT, Winer N, Darmaun D 2016. l-citrulline supplementation enhances fetal growth and protein synthesis in rats with intrauterine growth restriction. J. Nutr. 146:532–41
    [Google Scholar]
  171. 171.  Tran NT, Amarger V, Bourdon A, Misbert E, Grit I et al. 2017. Maternal citrulline supplementation enhances placental function and fetal growth in a rat model of IUGR: involvement of insulin-like growth factor 2 and angiogenic factors. J. Matern. Fetal Neonatal Med. 30:1906–11
    [Google Scholar]
  172. 172.  Chen J, Tao Y, Li J, Deng Z, Yan Z et al. 2010. microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J. Cell Biol. 190:867–79
    [Google Scholar]
  173. 173.  Crist CG, Montarras D, Buckingham M 2012. Muscle satellite cells are primed for myogenesis but maintain quiescence with the sequestration of Myf5 mRNA targeted by microRNA-31 in mRNP granules. Cell Stem Cell 11:118–26
    [Google Scholar]
  174. 174.  McCarthy JJ, Esser KA 2007. MicroRNA-1 and microRNA-133α expression are decreased during skeletal muscle hypertrophy. J. Appl. Physiol. 102:306–13
    [Google Scholar]
  175. 175.  Sheets TP, Park K-E, Park C-H, Swift SM, Powell A et al. 2018. Targeted mutation of NGN3 gene disrupts pancreatic endocrine cell development in pigs. Sci. Rep. 8:3582–91
    [Google Scholar]
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