Intermittent bolus feeding has a greater stimulatory effect on protein synthesis in skeletal muscle than continuous feeding in neonatal pigs

María C. Gazzaneo, Agus Suryawan Orellana, Roberto Murgas Torrazza, Samer W. El-Kadi, Fiona A. Wilson, Scot R. Kimball, Neeraj Srivastava, Hanh V. Nguyen, Marta L. Fiorotto, Teresa A. Davis

Research output: Contribution to journalArticle

33 Citations (Scopus)

Abstract

Orogastric tube feeding, using either continuous or intermittent bolus delivery, is common in infants forwhomnormal feeding is contraindicated. To compare the impact of different feeding strategies onmuscle protein synthesis, after withholding food overnight, neonatal pigs received a complete formula orally as a bolus feed every 4 h or were continuously fed. Protein synthesis rate and translational mechanisms in skeletalmusclewere examined after 0, 24, and 25.5 h. Plasma amino acid and insulin concentrations increased minimally and remained constant in continuously fed compared to feed-deprived pigs; however, the pulsatile meal feeding pattern was mimicked in bolus-fed pigs. Muscle protein synthesis was stimulated by feeding and the greatest response occurred after a bolus meal. Bolus but not continuous feeds increased polysome aggregation, the phosphorylation of protein kinase B, tuberous sclerosis complex 2, proline-rich Akt substrate of 40 kDa, eukaryotic initiation factor (eIF) 4E binding protein (4EBP1), and rp S6 kinase and enhanced dissociation of the 4EBP1 × eIF4E complex and formation of the eIF4E × eIF4G complex compared to feed deprivation (P < 0.05). Activation of insulin receptor substrate-1, regulatory associated protein of mammalian target of rapamycin, AMP-activated protein kinase, eukaryotic elongation factor 2, and eIF2α phosphorylation were unaffected by either feeding modality. These results suggest that in neonates, intermittent bolus feeding enhances muscle protein synthesis to a greater extent than continuous feeding by eliciting a pulsatile pattern of amino acid- and insulin-induced translation initiation.

Original languageEnglish (US)
Pages (from-to)2152-2158
Number of pages7
JournalJournal of Nutrition
Volume141
Issue number12
DOIs
StatePublished - Dec 1 2011

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Skeletal Muscle
Swine
Muscle Proteins
Meals
TOR Serine-Threonine Kinases
Phosphorylation
Eukaryotic Initiation Factor-4E
Peptide Elongation Factor 2
Insulin
Ribosomal Protein S6 Kinases
Insulin Receptor Substrate Proteins
Amino Acids
Proto-Oncogene Proteins c-akt
Proteins
AMP-Activated Protein Kinases
Tuberous Sclerosis
Polyribosomes
Enteral Nutrition
Feeding Behavior
Proline

All Science Journal Classification (ASJC) codes

  • Medicine (miscellaneous)
  • Nutrition and Dietetics

Cite this

Gazzaneo, María C. ; Orellana, Agus Suryawan ; Torrazza, Roberto Murgas ; El-Kadi, Samer W. ; Wilson, Fiona A. ; Kimball, Scot R. ; Srivastava, Neeraj ; Nguyen, Hanh V. ; Fiorotto, Marta L. ; Davis, Teresa A. / Intermittent bolus feeding has a greater stimulatory effect on protein synthesis in skeletal muscle than continuous feeding in neonatal pigs. In: Journal of Nutrition. 2011 ; Vol. 141, No. 12. pp. 2152-2158.
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abstract = "Orogastric tube feeding, using either continuous or intermittent bolus delivery, is common in infants forwhomnormal feeding is contraindicated. To compare the impact of different feeding strategies onmuscle protein synthesis, after withholding food overnight, neonatal pigs received a complete formula orally as a bolus feed every 4 h or were continuously fed. Protein synthesis rate and translational mechanisms in skeletalmusclewere examined after 0, 24, and 25.5 h. Plasma amino acid and insulin concentrations increased minimally and remained constant in continuously fed compared to feed-deprived pigs; however, the pulsatile meal feeding pattern was mimicked in bolus-fed pigs. Muscle protein synthesis was stimulated by feeding and the greatest response occurred after a bolus meal. Bolus but not continuous feeds increased polysome aggregation, the phosphorylation of protein kinase B, tuberous sclerosis complex 2, proline-rich Akt substrate of 40 kDa, eukaryotic initiation factor (eIF) 4E binding protein (4EBP1), and rp S6 kinase and enhanced dissociation of the 4EBP1 × eIF4E complex and formation of the eIF4E × eIF4G complex compared to feed deprivation (P < 0.05). Activation of insulin receptor substrate-1, regulatory associated protein of mammalian target of rapamycin, AMP-activated protein kinase, eukaryotic elongation factor 2, and eIF2α phosphorylation were unaffected by either feeding modality. These results suggest that in neonates, intermittent bolus feeding enhances muscle protein synthesis to a greater extent than continuous feeding by eliciting a pulsatile pattern of amino acid- and insulin-induced translation initiation.",
author = "Gazzaneo, {Mar{\'i}a C.} and Orellana, {Agus Suryawan} and Torrazza, {Roberto Murgas} and El-Kadi, {Samer W.} and Wilson, {Fiona A.} and Kimball, {Scot R.} and Neeraj Srivastava and Nguyen, {Hanh V.} and Fiorotto, {Marta L.} and Davis, {Teresa A.}",
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Gazzaneo, MC, Orellana, AS, Torrazza, RM, El-Kadi, SW, Wilson, FA, Kimball, SR, Srivastava, N, Nguyen, HV, Fiorotto, ML & Davis, TA 2011, 'Intermittent bolus feeding has a greater stimulatory effect on protein synthesis in skeletal muscle than continuous feeding in neonatal pigs', Journal of Nutrition, vol. 141, no. 12, pp. 2152-2158. https://doi.org/10.3945/jn.111.147520

Intermittent bolus feeding has a greater stimulatory effect on protein synthesis in skeletal muscle than continuous feeding in neonatal pigs. / Gazzaneo, María C.; Orellana, Agus Suryawan; Torrazza, Roberto Murgas; El-Kadi, Samer W.; Wilson, Fiona A.; Kimball, Scot R.; Srivastava, Neeraj; Nguyen, Hanh V.; Fiorotto, Marta L.; Davis, Teresa A.

In: Journal of Nutrition, Vol. 141, No. 12, 01.12.2011, p. 2152-2158.

Research output: Contribution to journalArticle

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T1 - Intermittent bolus feeding has a greater stimulatory effect on protein synthesis in skeletal muscle than continuous feeding in neonatal pigs

AU - Gazzaneo, María C.

AU - Orellana, Agus Suryawan

AU - Torrazza, Roberto Murgas

AU - El-Kadi, Samer W.

AU - Wilson, Fiona A.

AU - Kimball, Scot R.

AU - Srivastava, Neeraj

AU - Nguyen, Hanh V.

AU - Fiorotto, Marta L.

AU - Davis, Teresa A.

PY - 2011/12/1

Y1 - 2011/12/1

N2 - Orogastric tube feeding, using either continuous or intermittent bolus delivery, is common in infants forwhomnormal feeding is contraindicated. To compare the impact of different feeding strategies onmuscle protein synthesis, after withholding food overnight, neonatal pigs received a complete formula orally as a bolus feed every 4 h or were continuously fed. Protein synthesis rate and translational mechanisms in skeletalmusclewere examined after 0, 24, and 25.5 h. Plasma amino acid and insulin concentrations increased minimally and remained constant in continuously fed compared to feed-deprived pigs; however, the pulsatile meal feeding pattern was mimicked in bolus-fed pigs. Muscle protein synthesis was stimulated by feeding and the greatest response occurred after a bolus meal. Bolus but not continuous feeds increased polysome aggregation, the phosphorylation of protein kinase B, tuberous sclerosis complex 2, proline-rich Akt substrate of 40 kDa, eukaryotic initiation factor (eIF) 4E binding protein (4EBP1), and rp S6 kinase and enhanced dissociation of the 4EBP1 × eIF4E complex and formation of the eIF4E × eIF4G complex compared to feed deprivation (P < 0.05). Activation of insulin receptor substrate-1, regulatory associated protein of mammalian target of rapamycin, AMP-activated protein kinase, eukaryotic elongation factor 2, and eIF2α phosphorylation were unaffected by either feeding modality. These results suggest that in neonates, intermittent bolus feeding enhances muscle protein synthesis to a greater extent than continuous feeding by eliciting a pulsatile pattern of amino acid- and insulin-induced translation initiation.

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