Skip to main content
SpringerLink
Log in

Maternal Nutrient Restriction and Skeletal Muscle Development: Consequences for Postnatal Health

  • Chapter
  • First Online:
Amino Acids in Nutrition and Health

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1265))

Abstract

Severe undernutrition and famine continue to be a worldwide concern, as cases have been increasing in the past 5 years, particularly in developing countries. The occurrence of nutrient restriction (NR) during pregnancy affects fetal growth, leading to small for gestational age (SGA) or intrauterine growth restricted (IUGR) offspring. During adulthood, SGA and IUGR offspring are at a higher risk for the development of metabolic syndrome. Skeletal muscle is particularly sensitive to prenatal NR. This tissue plays an essential role in oxidation and glucose metabolism because roughly 80% of insulin-mediated glucose uptake occurs in muscle, and it represents around 40% of body weight. Alterations in myofiber number, hypertrophy and myofiber type composition, decreased protein synthesis, lower mitochondrial content and activity of oxidative enzymes, and increased accumulation of intramuscular triglycerides are among the described programming effects of maternal NR on skeletal muscle. Together, these features would add to a phenotype that is prone to insulin resistance, type 2 diabetes, obesity, and metabolic syndrome. Insights from diverse animal models (i.e. ovine, swine, and rodent) have provided valuable information regarding the molecular mechanisms behind those altered developmental pathways. Understanding those molecular signatures supports the development of efficient treatments to counteract the effects of maternal NR on skeletal muscle, and its negative implications for postnatal health.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Argilés JM, Campos N, Lopez-Pedrosa JM, Rueda R, Rodriguez-Mañas L (2016) Skeletal muscle regulates metabolism via interorgan crosstalk: roles in health and disease. J Am Med Dir Assoc 17:789–796

    Article  PubMed  Google Scholar 

  • Baker J, Liu JP, Robertson EJ, Efstratiadis A (1993) Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73–82

    Article  CAS  PubMed  Google Scholar 

  • Barker DJP, Osmond C, Winter PD, Margetts B (1989) Weight in infancy and death from ischaemic heart disease. Lancet 2(8663):577–580

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp B, Ghosh S, Dysart MW et al (2015) Low birth weight is associated with adiposity, impaired skeletal muscle energetics and weight loss resistance in mice. Int J Obes 39:702–711

    Article  CAS  Google Scholar 

  • Belfiore A, Frasca F, Pandini G, Sciacca L, Vigneri R (2009) Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease. Endocr Rev 30:586–623

    Article  CAS  PubMed  Google Scholar 

  • Brown LD (2014) Endocrine regulation of fetal skeletal muscle growth: impact on future metabolic health. J Endocrinol 221:R13–R29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corcoran MP, Lamon-Fava S, Fielding RA (2007) Skeletal muscle lipid deposition and insulin resistance: effect of dietary fatty acids and exercise. Am J Clin Nutr 85:662–677

    CAS  PubMed  Google Scholar 

  • Costello PM, Rowlerson A, Astaman NA, Anthony FE, Sayer AA, Cooper C, Hanson M, Green L (2008) Peri-implantation and late gestation maternal undernutrition differentially affect fetal sheep skeletal muscle development. J Physiol 586:2371–2379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai ZL, Wu ZL, Yang Y, Wang JJ, Satterfield MC, Meininger CJ, Bazer FW, Wu G (2013) Nitric oxide and energy metabolism in mammals. Biofactors 39:383–391

    Article  CAS  PubMed  Google Scholar 

  • Davis TA, Suryawan A, Orellana RA, Fiorotto ML, Burrin DG (2010) Amino acids and insulin are regulators of muscle protein synthesis in neonatal pigs. Animal 4:1790–1796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Blasio MJ, Gatford KL, Robinson JS, Owens JA (2007) Placental restriction of fetal growth reduces size at birth and alters postnatal growth, feeding activity, and adiposity in the young lamb. Am J Physiol Integr Comp Physiol 292:R875–R886

    Article  CAS  Google Scholar 

  • DeFronzo RA, Tripathy D (2009) Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32(Suppl 2):S157–SS63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desai M, Crowther NJ, Lucas A, Nicholas HC (1996) Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 76:591–603

    Article  CAS  PubMed  Google Scholar 

  • 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 83:2564–2571

    Article  CAS  PubMed  Google Scholar 

  • FAO (2017) The state of food security and nutrition in the world 2017. Building resilience for peace and food security. Rome, FAO

    Google Scholar 

  • Fernandez-Twinn DS, Ozanne SE (2006) Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome. Physiol Behav 88:234–243

    Article  CAS  PubMed  Google Scholar 

  • Ferrannini E, Bjorkman O, Reichard GA, Pilo A, Olsson M, Wahren J, DeFronzo R (1985) The disposal of an oral glucose load in healthy subjects. A quantitative study. Diabetes 34:580–588

    Article  CAS  PubMed  Google Scholar 

  • Fisher G, Windham ST, Griffin P, Warren J, Gower B, Hunter G (2017) Associations of human skeletal muscle fiber type and insulin sensitivity, blood lipids, and vascular hemodynamics in a cohort of premenopausal women. Eur J Appl Physiol 117:1413–1422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flynn NE, Wu G (1996) An important role for endogenous synthesis of arginine in maintaining arginine homeostasis in neonatal pigs. Am J Physiol 271:R1149–R1155

    Google Scholar 

  • Ford SP, Hess BW, Schwope MM, Nijland MJ, Gilbert JS, Vonnahme K, Means W, Han H, Nathanielsz PW (2007) Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. J Anim Sci 85:1285–1294

    Article  CAS  PubMed  Google Scholar 

  • Fowden AL, Hughes P, Comline RS (1989) The effects of insulin on the growth rate of the sheep fetus during late gestation. Q J Exp Physiol 74:703–714

    Article  CAS  PubMed  Google Scholar 

  • Gao J, Ren J, Gulve EA, Holloszy JO (1994) Additive effect of contractions and insulin on GLUT-4 translocation into the sarcolemma. J Appl Physiol 77:1597–1601

    Article  CAS  PubMed  Google Scholar 

  • Gao F, Hou XZ, Liu YC, Wu SQ, Ao CJ (2008) Effect of maternal under-nutrition during late pregnancy on lamb birth weight. Asian-Australasian J Anim Sci 21:371–375

    Article  Google Scholar 

  • Garber J, Missouri L (1976) Alanine and glutamine synthesis and release from skeletal muscle. J Biol Chem 251:836–843

    Article  CAS  PubMed  Google Scholar 

  • Gardner DS, Tingey K, Van Bon BWM, Ozanne SE, Wilson V, Dandrea J, Keisler DH, Stephenson T, Symonds ME (2005) Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition. Am J Physiol Regul Integr Comp Physiol 289:947–954

    Article  CAS  Google Scholar 

  • Gennser G, Rymark P, Isberg PE (1988) Low birth weight and risk of high blood pressure in adulthood. Br Med J (Clin Res Ed) 296:1498–1500

    Article  CAS  Google Scholar 

  • George LA, Zhang L, Tuersunjiang N, Ma Y, Long NM, Uthlaut AB, Smith DT, Nathanielsz PW, Ford SP (2012) Early maternal undernutrition programs increased feed intake, altered glucose metabolism and insulin secretion, and liver function in aged female offspring. Am J Physiol Regul Integr Comp Physiol 302:R795–R804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gluckman PD, Hanson MA, Spencer HG (2005) Predictive adaptive responses and human evolution. Trends Ecol Evol 20:527–533

    Article  PubMed  Google Scholar 

  • Goldenberg RL, Cliver SP (1997) Small for gestational age and intrauterine growth restriction: definitions and standards. Clin Obstet Gynecol 40:704–714

    Article  CAS  PubMed  Google Scholar 

  • Hales CN, Barker DJP (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595–601

    Article  CAS  PubMed  Google Scholar 

  • He J, Watkins S, Kelley DE (2001) Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 50:817–823

    Article  CAS  PubMed  Google Scholar 

  • Hou YQ, Wu G (2018) L-Glutamate nutrition and metabolism in swine. Amino Acids 50:1497–1510

    Article  CAS  PubMed  Google Scholar 

  • Hou YQ, He WL, Hu SD, Wu G (2019) Composition of polyamines and amino acids in plant-source foods for human consumption. Amino Acids 51:1153–1165

    Article  CAS  PubMed  Google Scholar 

  • Hyatt MA, Gardner DS, Sebert S, Wilson V, Davidson N, Nigmatullina Y, Chan LLY, Budge H, Symonds ME (2011) Suboptimal maternal nutrition, during early fetal liver development, promotes lipid accumulation in the liver of obese offspring. Reproduction 141:119–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janssen I, Heymsfield SB, Wang Z, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol 89:81–88

    Article  CAS  PubMed  Google Scholar 

  • Ji Y, Wu ZL, Dai ZL, Sun KJ, Wang JJ, Wu G (2016) Nutritional epigenetics with a focus on amino acids: Implications for the development and treatment of metabolic syndrome. J Nutr Biochem 27:1–8

    Google Scholar 

  • Ji Y, Wu ZL, Dai ZL, Wang XL, Li J, Wang BG, Wu G (2017) Fetal and neonatal programming of postnatal growth and feed efficiency in swine. J Anim Sci Biotechnol 8:42

    Google Scholar 

  • Kalbe C, Bérard J, Porm M, Rehfeldt C, Bee G (2013) Maternal l-arginine supplementation during early gestation affects foetal skeletal myogenesis in pigs. Livest Sci 157:322–329

    Article  Google Scholar 

  • Kensara OA, Wootton SA, Phillips DI, Patel M, Jackson AA, Elia M (2005) Fetal programming of body composition: relation between birth weight and body composition measured with dual-energy X-ray absorptiometry and anthropometric methods in older Englishmen. Am J Clin Nutr 82:980–987

    Article  CAS  PubMed  Google Scholar 

  • Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM (2002) mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110:163–175

    Article  CAS  PubMed  Google Scholar 

  • Kohn AD, Summers SA, Birnbaum MJ, Roth RA (1996) Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J Biol Chem 271:31372–31378

    Article  CAS  PubMed  Google Scholar 

  • Kwon H, Ford SP, Bazer FW, Spencer TE, Nathanielsz PW, Nijland MJ, Hess BW, Wu G (2004) Maternal nutrient restriction reduces concentrations of amino acids and polyamines in ovine maternal and Fetal plasma and Fetal Fluids1. Biol Reprod 71:901–908

    Article  CAS  PubMed  Google Scholar 

  • Lassala A, Bazer FW, Cudd TA, Datta S, Keisler DH, Satterfield MC, Spencer TE, Wu G (2010) Parenteral administration of L-arginine prevents Fetal growth restriction in undernourished ewes. J Nutr 140:1242–1248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li P, Wu G (2018) Roles of dietary glycine, proline and hydroxyproline in collagen synthesis and animal growth. Amino Acids 50:29–38

    Article  CAS  PubMed  Google Scholar 

  • Li P, Wu G (2020) Composition of amino acids and related nitrogenous nutrients in feedstuffs for animal diets. Amino Acids 52:523–542 

    Google Scholar 

  • Li H, Xu M, Lee J, He C, Xie Z (2012) Leucine supplementation increases SIRT1 expression and prevents mitochondrial dysfunction and metabolic disorders in high-fat diet-induced obese mice. Am J Physiol Endocrinol Metab 303:1234–1244

    Article  CAS  Google Scholar 

  • Lillioja S, Young AA, Culter CL et al (1987) Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 80:415–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Pan S, Li X, Sun Q, Yang X, Zhao R (2015) Maternal low-protein diet affects myostatin signaling and protein synthesis in skeletal muscle of offspring piglets at weaning stage. Eur J Nutr 54:971–979

    Article  CAS  PubMed  Google Scholar 

  • Lloyd LJ, Foster T, Rhodes P, Rhind SM, Gardner DS (2012) Protein-energy malnutrition during early gestation in sheep blunts fetal renal vascular and nephron development and compromises adult renal function. J Physiol 590:377–393

    Article  CAS  PubMed  Google Scholar 

  • Long JHD, Lira VA, Soltow QA, Betters JL, Sellman JE, Criswell DS (2006) Arginine supplementation induces myoblast fusion via augmentation of nitric oxide production. J Muscle Res Cell Motil 27:577–584

    Article  CAS  PubMed  Google Scholar 

  • Maltin CA (2008) Muscle development and obesity. Organogenesis 4:158–169

    Article  PubMed  PubMed Central  Google Scholar 

  • Marliss EB, Aoki TT, Pozefsky T, Most AS, Cahill GF (1971) Muscle and splanchnic glutmine and glutamate metabolism in postabsorptive and starved man. J Clin Invest 50:814–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McMillen IC, Robinson JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85:571–633

    Article  CAS  PubMed  Google Scholar 

  • Mora S, Kaliman P, Chillarón J, Testar X, Palacín M, Zorzano A (1995) Insulin and insulin-like growth factor I (IGF-I) stimulate GLUT4 glucose transporter translocation in Xenopus oocytes. Biochem J 311:59–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mortensen OH, Olsen HL, Frandsen L, Nielsen PE, Grunnet N, Quistorff B (2010) Gestational protein restriction in mice has pronounced effects on gene expression in newborn offspring’s liver and skeletal muscle; protective effect of taurine. Pediatr Res 67:47–53

    Article  CAS  PubMed  Google Scholar 

  • Muhlhausler BS, Duffield JA, Ozanne SE, Pilgrim C, Turner N, Morrison JL, McMillen IC (2009) The transition from fetal growth restriction to accelerated postnatal growth: a potential role for insulin signalling in skeletal muscle. J Physiol 587:4199–4211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osgerby J, Wathes D, Howard D, Gadd T (2002) The effect of maternal undernutrition on ovine fetal growth. J Endocrinol 173:131–141

    Article  CAS  PubMed  Google Scholar 

  • Quigley SP, Kleemann DO, Kakar MA, Owens JA, Nattrass GS, Maddocks S, Walker SK (2005) Myogenesis in sheep is altered by maternal feed intake during the peri-conception period. Anim Reprod Sci 87:241–251

    Article  CAS  PubMed  Google Scholar 

  • Rich-Edwards JW, Colditz GA, Stampfer MJ, Willet CW, Gillman MW, Hennekens CH, Speizer FE, Manson JE (1999) Birthweight and the risk for type 2 diabetes mellitus in adult women. Ann Intern Med 130:278–284

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez J, Vernus B, Chelh I, Cassar-Malek I, Gabillard JC, Sassi AH, Seiliez I, Picard B, Bonnieu A (2014) Myostatin and the skeletal muscle atrophy and hypertrophy signaling pathways. Cell Mol Life Sci 71:4361–4371

    Article  CAS  PubMed  Google Scholar 

  • Satterfield MC, Bazer FW, Spencer TE, Wu G (2010) Sildenafil citrate treatment enhances amino acid availability in the Conceptus and Fetal growth in an ovine model of intrauterine growth restriction. J Nutr 140:251–258

    Article  CAS  PubMed  Google Scholar 

  • Satterfield MC, Dunlap KA, Keisler DH, Bazer FW, Wu G (2013) Arginine nutrition and fetal brown adipose tissue development in nutrient-restricted sheep. Amino Acids 45:489–499

    Article  CAS  PubMed  Google Scholar 

  • Scheepers A, Joost HG, Schürmann A (2004) The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function. J Parenter Enter Nutr 28:364–371

    Article  CAS  Google Scholar 

  • Shimizu N, Yoshikawa N, Ito N et al (2011) Crosstalk between glucocorticoid receptor and nutritional sensor mTOR in skeletal muscle. Cell Metab 13:170–182

    Article  CAS  PubMed  Google Scholar 

  • Shukla P, Ghatta S, Dubey N et al (2014) Maternal nutrient restriction during pregnancy impairs an endothelium-derived hyperpolarizing factor-like pathway in sheep fetal coronary arteries. Am J Physiol Heart Circ Physiol 307:134–142

    Article  CAS  Google Scholar 

  • Stuart CA, Wen G, Gustafson WC, Thompson EA (2000) Comparison of GLUT1, GLUT3, and GLUT4 mRNA and the subcellular distribution of their proteins in normal human muscle. Metabolism 49:1604–1609

    Article  CAS  PubMed  Google Scholar 

  • Sun K, Wu Z, Ji Y, Wu G (2016) Glycine regulates protein turnover by activating protein kinase B/mammalian target of rapamycin and by inhibiting MuRF1 and atrogin-1 gene expression in C2C12 myoblasts. J Nutr 146:2461–2467

    Article  CAS  PubMed  Google Scholar 

  • Symonds ME, Sebert SP, Hyatt MA, Budge H (2009) Nutritional programming of the metabolic syndrome. Nat Rev Endocrinol 5:604–610

    Article  CAS  PubMed  Google Scholar 

  • Tan B, Yin Y, Liu Z et al (2011) Dietary L-arginine supplementation differentially regulates expression of lipid-metabolic genes in porcine adipose tissue and skeletal muscle. J Nutr Biochem 22:441–445

    Article  CAS  PubMed  Google Scholar 

  • Taniguchi CM, Emanuelli B, Kahn CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7:85–96

    Article  CAS  PubMed  Google Scholar 

  • UNICEF (2004) Low birtweight: country, regional and global estimates. UNICEF, New York

    Google Scholar 

  • Vonnahme KA, Hess BW, Hansen TR et al (2003) Maternal undernutrition from early- to mid-gestation leads to growth retardation, cardiac ventricular hypertrophy, and increased liver weight in the fetal sheep. Biol Reprod 69:133–140

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Chen L, Li D, Yin Y, Wang X, Li P, Dangott LJ, Hu W, Wu G (2008) Intrauterine growth restriction affects the proteomes of the small intestine, liver, and skeletal muscle in newborn pigs. J Nutr 138:60–66

    Article  CAS  PubMed  Google Scholar 

  • Wang XQ, Ying W, Dunlap KA, Lin G, Satterfield MC, Burghardt RC, Wu G, Bazer FW (2014) Arginine decarboxylase and agmatinase: an alternative pathway for de novo biosynthesis of polyamines for development of mammalian conceptuses. Biol Reprod 90:84

    PubMed  Google Scholar 

  • Wang J, Cao M, Zhuo Y, Che L, Fang Z, Xu S, Lin Y, Feng B, Wu D (2016) Catch-up growth following food restriction exacerbates adulthood glucose intolerance in pigs exposed to intrauterine undernutrition. Nutrition 32:1275–1284

    Article  CAS  PubMed  Google Scholar 

  • Wei C, Li L, Su H, Xu L, Lu J, Zhang L, Liu W, Ren H, Du L (2014) Identification of the crucial molecular events during the large-scale myoblast fusion in sheep. Physiol Genomics 46:429–440

    Article  PubMed  CAS  Google Scholar 

  • Wu G (2013) Amino acids: biochemistry and nutrition. CRC Press, Boca Raton

    Book  Google Scholar 

  • Wu G (2018) Principles of animal nutrition. CRC Press, Boca Raton

    Google Scholar 

  • Wu G, Thompson JR (1990) The effect of glutamine on protein turnover in chick skeletal muscle in vitro. Biochem J 265:593–598

    Google Scholar 

  • Wu G, Thompson JR, Baracos VE (1991) Glutamine metabolism in skeletal muscle from the broiler chick (Gallus domesticus) and the laboratory rat (Rattus norvegicus). Biochem J 274:769–774

    Google Scholar 

  • Wu G, Morris SM Jr (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336:1–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu G, Bazer FW, Wallace JM, Spencer TE (2006) Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci 84:2316–2337

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Collins JK, Perkins-Veazie P, Siddiq M, Dolan KD, Kelly KA, Heaps CL, Meininger CJ (2007) Dietary supplementation with watermelon pomace juice enhances arginine availability and ameliorates the metabolic syndrome in Zucker diabetic fatty rats. J Nutr 137:2680–2685

    Article  CAS  PubMed  Google Scholar 

  • Wu ZL, Hou YQ, Hu SD, Bazer FW, Meininger CJ, McNeal CJ, Wu G (2016) Catabolism and safety of supplemental L-arginine in animals. Amino Acids 48:1541–1552

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Bazer FB, Johnson GA, Hou YQ (2018) Arginine nutrition and metabolism in growing, gestating and lactating swine. J Anim Sci 96:5035–5051

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu ZL, Hou YQ, Dai ZL, Hu CA, Wu G (2019) Metabolism, nutrition and redox signaling of hydroxyproline. Antioxid Redox Signal 30:674–682

    Article  CAS  PubMed  Google Scholar 

  • Yao K, Yin Y, Chu W et al (2008) Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. J Nutr 138:867–872

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Yao K, Liu Z, Gong M, Ruan Z, Deng D, Tan B, Liu Z, Wu G (2010) Supplementing l-leucine to a low-protein diet increases tissue protein synthesis in weanling pigs. Amino Acids 39:1477–1486

    Article  CAS  PubMed  Google Scholar 

  • Yoon MS (2017) mTOR as a key regulator in maintaining skeletal muscle mass. Front Physiol 8:1–9

    Article  CAS  Google Scholar 

  • Zheng S, Rollet M, Pan YX (2011) Maternal protein restriction during pregnancy induces CCAAT/enhancer-binding protein (C/EBPβ) expression through the regulation of histone modification at its promoter region in female offspring rat skeletal muscle. Epigenetics 6:161–170

    Article  CAS  PubMed  Google Scholar 

  • Zheng S, Rollet M, Pan YX (2012) Protein restriction during gestation alters histone modifications at the glucose transporter 4 (GLUT4) promoter region and induces GLUT4 expression in skeletal muscle of female rat offspring. J Nutr Biochem 23:1064–1071

    Article  CAS  PubMed  Google Scholar 

  • Zhu M-J, Ford SP, Nathanielsz PW, Du M (2004) Effect of maternal nutrient restriction in sheep on the development of fetal skeletal muscle1. Biol Reprod 71:1968–1973

    Article  CAS  PubMed  Google Scholar 

  • Zhu MJ, Ford SP, Means WJ, Hess BW, Nathanielsz PW, Du M (2006) Maternal nutrient restriction affects properties of skeletal muscle in offspring. J Physiol 575:241–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou T, Yu B, Yu J, Mao X, Zheng P, He J, Huang Z, Liu Y, Chen D (2016) Moderately decreased maternal dietary energy intake during pregnancy reduces fetal skeletal muscle mitochondrial biogenesis in the pigs. Genes Nutr 11:1–10

    Article  CAS  Google Scholar 

Download references

Acknowledgements

C. Sandoval was supported by Becas Chile (CONICYT) during the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Department of Animal Science, Texas A&M University, College Station, TX, USA

    Camila Sandoval, Guoyao Wu, Stephen B. Smith, Kathrin A. Dunlap & M. Carey Satterfield

Authors
  1. Camila Sandoval
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guoyao Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen B. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kathrin A. Dunlap
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Carey Satterfield
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Carey Satterfield .

Editor information

Editors and Affiliations

  1. Department of Animal Science, Texas A&M University, College Station, TX, USA

    Guoyao Wu

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sandoval, C., Wu, G., Smith, S.B., Dunlap, K.A., Satterfield, M.C. (2020). Maternal Nutrient Restriction and Skeletal Muscle Development: Consequences for Postnatal Health. In: Wu, G. (eds) Amino Acids in Nutrition and Health. Advances in Experimental Medicine and Biology, vol 1265. Springer, Cham. https://doi.org/10.1007/978-3-030-45328-2_9

Download citation

Publish with us

Policies and ethics

Search

Navigation