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Published in: European Journal of Nutrition 2/2012

01-03-2012 | Original Contribution

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

Authors: Charlotte Rehfeldt, Louis Lefaucheur, Jana Block, Bernd Stabenow, Ralf Pfuhl, Winfried Otten, Cornelia C. Metges, Claudia Kalbe

Published in: European Journal of Nutrition | Issue 2/2012

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Abstract

Aim

This study investigated whether dietary protein intake less (50%) or greater (250%) than requirements throughout gestation differently affects offspring body composition and cellular properties of skeletal muscle and subcutaneous adipose tissue (SCAT).

Methods

Primiparous gilts were fed iso-energetic diets containing adequate (22 AP), high (21 HP), or low (19 LP) protein contents. Newborn (n = 166) and weanling piglets cross-fostered to sows fed a standard diet (day 28; n = 83) were examined by morphological, biochemical, histological, and molecular analyses of the body, SCAT, and semitendinosus, longissimus, biceps femoris muscles.

Results

Lowered birth weight (BW) in response to the HP and LP diets (p < 0.01) resulted from decreases in all body constituents in LP, and mainly from reduced body fat in HP piglets (p < 0.05). In the light BW class within litters, HP piglets exhibited a greater percentage of muscle tissue (p < 0.05) than LP piglets. Less SCAT mass in HP and LP piglets resulted from reduced (p < 0.05) number, but not the size of adipocytes. The LP diet adversely affected myogenesis and muscular differentiation derived from less (p < 0.01) primary and secondary myofibers, lower creatine kinase activity (p < 0.05), less IGF2 mRNA (p < 0.10), and greater expression of the embryonic myosin heavy chain isoform (p < 0.01). Catch-up growth of LP but not HP pigs until day 28 increased body fat (p = 0.01). Despite compensated muscle growth in LP piglets, the deficit in myofiber number remained.

Conclusion

Poor intrauterine environment by limited and excess protein supply retards fetal growth, but only limited protein supply impairs myogenesis, persistently restricts muscle growth potential, and favors obesity at infancy.
Appendix
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Literature
1.
go back to reference Gluckman PD, Hanson MA, Mitchell MD (2010) Developmental origins of health and disease: reducing the burden of chronic disease in the next generation. Genome Med 2:14CrossRef Gluckman PD, Hanson MA, Mitchell MD (2010) Developmental origins of health and disease: reducing the burden of chronic disease in the next generation. Genome Med 2:14CrossRef
2.
go back to reference Hales CN, Barker DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595–601CrossRef Hales CN, Barker DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595–601CrossRef
3.
go back to reference Gluckman PD, Hanson MA, Spencer HG (2005) Predictive adaptive responses and human evolution. Trends Ecol Evol 20:527–533CrossRef Gluckman PD, Hanson MA, Spencer HG (2005) Predictive adaptive responses and human evolution. Trends Ecol Evol 20:527–533CrossRef
4.
go back to reference Gluckman PD, Hanson MA, Cooper C, Thornburg KL (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359:61–73CrossRef Gluckman PD, Hanson MA, Cooper C, Thornburg KL (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359:61–73CrossRef
5.
go back to reference Wu G, Bazer FW, Wallace JM, Spencer TE (2006) Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci 84:2316–2337CrossRef Wu G, Bazer FW, Wallace JM, Spencer TE (2006) Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci 84:2316–2337CrossRef
6.
go back to reference Litten JC, Drury PC, Corson AM, Lean IJ, Clarke L (2003) The influence of piglet birth weight on physical and behavioural development in early life. Biol Neonate 84:311–318CrossRef Litten JC, Drury PC, Corson AM, Lean IJ, Clarke L (2003) The influence of piglet birth weight on physical and behavioural development in early life. Biol Neonate 84:311–318CrossRef
7.
go back to reference Gondret F, Lefaucheur L, Juin H, Louveau I, Lebret B (2006) Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs. J Anim Sci 84:93–103 Gondret F, Lefaucheur L, Juin H, Louveau I, Lebret B (2006) Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs. J Anim Sci 84:93–103
8.
go back to reference Rehfeldt C, Kuhn G (2006) Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci 84(Suppl):E113–E123 Rehfeldt C, Kuhn G (2006) Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci 84(Suppl):E113–E123
9.
go back to reference Rehfeldt C, Tuchscherer A, Hartung M, Kuhn G (2008) A second look at the influence of birth weight on carcass and meat quality in pigs. Meat Sci 78:170–175CrossRef Rehfeldt C, Tuchscherer A, Hartung M, Kuhn G (2008) A second look at the influence of birth weight on carcass and meat quality in pigs. Meat Sci 78:170–175CrossRef
10.
go back to reference Dwyer CM, Stickland NC (1991) Sources of variation in myofiber number within and between litters of pigs. Anim Prod 52:527–533CrossRef Dwyer CM, Stickland NC (1991) Sources of variation in myofiber number within and between litters of pigs. Anim Prod 52:527–533CrossRef
11.
go back to reference Langley-Evans SC (2009) Nutritional programming of disease: unravelling the mechanism. J Anat 215:36–51CrossRef Langley-Evans SC (2009) Nutritional programming of disease: unravelling the mechanism. J Anat 215:36–51CrossRef
12.
go back to reference Mahan DC (1977) Effect of feeding various gestation and lactation dietary protein sequences on long-term reproductive performance in swine. J Anim Sci 45:1061–1072 Mahan DC (1977) Effect of feeding various gestation and lactation dietary protein sequences on long-term reproductive performance in swine. J Anim Sci 45:1061–1072
13.
go back to reference Pond WG, Maurer RR, Mersmann HJ, Cummins S (1992) Response of fetal and newborn piglets to maternal protein restriction during early or late pregnancy. Growth Dev Aging 56:115–127 Pond WG, Maurer RR, Mersmann HJ, Cummins S (1992) Response of fetal and newborn piglets to maternal protein restriction during early or late pregnancy. Growth Dev Aging 56:115–127
14.
go back to reference Schoknecht PA, Newton GR, Weise DE, Pond WG (1994) Protein restriction in early pregnancy alters fetal and placental growth and allantoic fluid proteins in swine. Theriogenology 42:217–226CrossRef Schoknecht PA, Newton GR, Weise DE, Pond WG (1994) Protein restriction in early pregnancy alters fetal and placental growth and allantoic fluid proteins in swine. Theriogenology 42:217–226CrossRef
15.
go back to reference Pond WG, Yen JT, Mersmann HJ (1987) Effect of severe dietary protein, nonprotein calories or feed restriction during gestation on postnatal growth of progeny in swine. Growth 51:355–371 Pond WG, Yen JT, Mersmann HJ (1987) Effect of severe dietary protein, nonprotein calories or feed restriction during gestation on postnatal growth of progeny in swine. Growth 51:355–371
16.
go back to reference Pond WG, Yen JT, Mersmann HJ, Maurer RR (1990) Reduced mature size in progeny of swine severely restricted in protein intake during pregnancy. Growth Dev Aging 54:77–84 Pond WG, Yen JT, Mersmann HJ, Maurer RR (1990) Reduced mature size in progeny of swine severely restricted in protein intake during pregnancy. Growth Dev Aging 54:77–84
17.
go back to reference Pond WG, Maurer RR, Klindt J (1991) Fetal organ response to maternal protein deprivation during pregnancy in swine. J Nutr 121:504–509 Pond WG, Maurer RR, Klindt J (1991) Fetal organ response to maternal protein deprivation during pregnancy in swine. J Nutr 121:504–509
18.
go back to reference Schoknecht PA, Pond WG, Mersmann HJ, Maurer RR (1993) Protein restriction during pregnancy affects postnatal growth in swine progeny. J Nutr 123:1818–1825 Schoknecht PA, Pond WG, Mersmann HJ, Maurer RR (1993) Protein restriction during pregnancy affects postnatal growth in swine progeny. J Nutr 123:1818–1825
19.
go back to reference Sayer AA, Stewart C, Patel H, Cooper C (2010) The developmental origins of sarcopenia: from epidemiological evidence to underlying mechanisms. JDOHaD 1:150–157 Sayer AA, Stewart C, Patel H, Cooper C (2010) The developmental origins of sarcopenia: from epidemiological evidence to underlying mechanisms. JDOHaD 1:150–157
20.
go back to reference Daenzer M, Ortmann S, Klaus S, Metges CC (2002) Prenatal high protein exposure decreases energy expenditure and increases adiposity in young rats. J Nutr 132:142–144 Daenzer M, Ortmann S, Klaus S, Metges CC (2002) Prenatal high protein exposure decreases energy expenditure and increases adiposity in young rats. J Nutr 132:142–144
21.
go back to reference Thone-Reineke C, Kalk P, Dorn M, Klaus S, Simon K, Pfab T, Godes M, Persson P, Unger T, Hocher B (2006) High-protein nutrition during pregnancy and lactation programs blood pressure, food efficiency, and body weight of the offspring in a sex-dependent manner. Am J Physiol Regul Integr Comp Physiol 291:R1025–R1030CrossRef Thone-Reineke C, Kalk P, Dorn M, Klaus S, Simon K, Pfab T, Godes M, Persson P, Unger T, Hocher B (2006) High-protein nutrition during pregnancy and lactation programs blood pressure, food efficiency, and body weight of the offspring in a sex-dependent manner. Am J Physiol Regul Integr Comp Physiol 291:R1025–R1030CrossRef
22.
go back to reference Kucia M, Langhammer M, Görs S, Albrecht E, Hammon HM, Nürnberg G, Metges CC (2011) High protein diet during gestation and lactation affects mammary gland mRNA abundance, milk composition and pre-weaning litter growth in mice. Animal 5:268–277CrossRef Kucia M, Langhammer M, Görs S, Albrecht E, Hammon HM, Nürnberg G, Metges CC (2011) High protein diet during gestation and lactation affects mammary gland mRNA abundance, milk composition and pre-weaning litter growth in mice. Animal 5:268–277CrossRef
23.
go back to reference Campbell-Brown M, Johnstone FD, Kerr-Grieve JF (1986) The effect on birthweight of a high-protein, low carbohydrate diet during pregnancy. Proc Nutr Soc 45:90A (Abstr.) Campbell-Brown M, Johnstone FD, Kerr-Grieve JF (1986) The effect on birthweight of a high-protein, low carbohydrate diet during pregnancy. Proc Nutr Soc 45:90A (Abstr.)
24.
go back to reference Andreasyan K, Ponsonby AL, Dwyer T, Morley R, Riley M, Dear K, Cochrane J (2007) Higher maternal dietary protein intake in late pregnancy is associated with a lower infant ponderal index at birth. Eur J Clin Nutr 61:498–508 Andreasyan K, Ponsonby AL, Dwyer T, Morley R, Riley M, Dear K, Cochrane J (2007) Higher maternal dietary protein intake in late pregnancy is associated with a lower infant ponderal index at birth. Eur J Clin Nutr 61:498–508
25.
go back to reference Moran LJ, Noakes M, Clifton PM, Tomlinson L, Galletly C, Norman RJ (2003) Dietary composition in restoring reproductive and metabolic physiology in overweight women with polycystic ovary syndrome. J Clin Endocrinol Metab 88:812–819CrossRef Moran LJ, Noakes M, Clifton PM, Tomlinson L, Galletly C, Norman RJ (2003) Dietary composition in restoring reproductive and metabolic physiology in overweight women with polycystic ovary syndrome. J Clin Endocrinol Metab 88:812–819CrossRef
26.
go back to reference Rehfeldt C, Lang IS, Görs S, Hennig U, Kalbe C, Stabenow B, Brüssow KP, Pfuhl R, Bellmann O, Nürnberg G, Otten W, Metges CC (2011) Low and excess dietary protein levels during gestation affect growth and compositional traits in gilts and impair offspring fetal growth. J Anim Sci 89:329–341 Rehfeldt C, Lang IS, Görs S, Hennig U, Kalbe C, Stabenow B, Brüssow KP, Pfuhl R, Bellmann O, Nürnberg G, Otten W, Metges CC (2011) Low and excess dietary protein levels during gestation affect growth and compositional traits in gilts and impair offspring fetal growth. J Anim Sci 89:329–341
27.
go back to reference GfE (Gesellschaft für Ernährungsphysiologie) (2006) Empfehlungen zur Energie- und Nährstoffversorgung von Schweinen (Recommendations of energy and nutrient intake in pigs). DLG-Verlags-GmbH, Frankfurt am Main GfE (Gesellschaft für Ernährungsphysiologie) (2006) Empfehlungen zur Energie- und Nährstoffversorgung von Schweinen (Recommendations of energy and nutrient intake in pigs). DLG-Verlags-GmbH, Frankfurt am Main
28.
go back to reference AOAC (1990) Official methods of analysis, 15th edn. Assoc. Off. Anal. Chem, Washington, DC AOAC (1990) Official methods of analysis, 15th edn. Assoc. Off. Anal. Chem, Washington, DC
29.
go back to reference Kuhn G, Ender K, Nürnberg K (1994) Effects of recombinant porcine somatotropin on the chemical composition of the whole edible body at pigs. Arch Anim Breed 37:621–623 Kuhn G, Ender K, Nürnberg K (1994) Effects of recombinant porcine somatotropin on the chemical composition of the whole edible body at pigs. Arch Anim Breed 37:621–623
30.
go back to reference Lösel D, Nürnberg G, Rehfeldt C (2011) Regional differences in micro-structural and biochemical characteristics of growth and metabolism in semitendinosus muscle of 28-day old piglets. Meat Sci 87:19–25CrossRef Lösel D, Nürnberg G, Rehfeldt C (2011) Regional differences in micro-structural and biochemical characteristics of growth and metabolism in semitendinosus muscle of 28-day old piglets. Meat Sci 87:19–25CrossRef
31.
go back to reference Romeis B (1989) Mikroskopische Technik. Urban & Schwarzenberg, Munich Romeis B (1989) Mikroskopische Technik. Urban & Schwarzenberg, Munich
32.
go back to reference Guth L, Samaha FJ (1970) Procedure for the histochemical demonstration of actomyosin ATPase. Exp Neurol 28:365–367CrossRef Guth L, Samaha FJ (1970) Procedure for the histochemical demonstration of actomyosin ATPase. Exp Neurol 28:365–367CrossRef
33.
go back to reference Rehfeldt C, Kuhn G, Vanselow J, Fürbass R, Fiedler I, Nürnberg G, Clelland AK, Stickland NC, Ender K (2001) Maternal treatment with somatotropin during early gestation affects basic events of myogenesis in pigs. Cell Tissue Res 306:429–440CrossRef Rehfeldt C, Kuhn G, Vanselow J, Fürbass R, Fiedler I, Nürnberg G, Clelland AK, Stickland NC, Ender K (2001) Maternal treatment with somatotropin during early gestation affects basic events of myogenesis in pigs. Cell Tissue Res 306:429–440CrossRef
34.
go back to reference Spannhof L (1967) Einführung in die Praxis der Histochemie. VEB Gustav-Fischer-Verlag, Jena Spannhof L (1967) Einführung in die Praxis der Histochemie. VEB Gustav-Fischer-Verlag, Jena
35.
go back to reference Novikoff AB, Shin WY, Drucker J (1961) Mitochondrial localization of oxidative enzymes: staining results with two tetrazolium salts. J Biophys Biochem Cytol 9:47–61CrossRef Novikoff AB, Shin WY, Drucker J (1961) Mitochondrial localization of oxidative enzymes: staining results with two tetrazolium salts. J Biophys Biochem Cytol 9:47–61CrossRef
36.
go back to reference Rehfeldt C, Walther K (1997) A combined assay for DNA, protein, and incorporated [3H] label in cultured muscle cells. Anal Biochem 251:294–297CrossRef Rehfeldt C, Walther K (1997) A combined assay for DNA, protein, and incorporated [3H] label in cultured muscle cells. Anal Biochem 251:294–297CrossRef
37.
go back to reference Oksbjerg N, Petersen JS, Sorensen IL, Henckel P, Vestergaard M, Ertbjerg P, Moller AJ, Bejerholm C, Stoier S (2000) Long-term changes in performance and meat quality of Danish Landrace pigs: a study on a current compared with an unimproved genotype. Anim Sci 71:81–92 Oksbjerg N, Petersen JS, Sorensen IL, Henckel P, Vestergaard M, Ertbjerg P, Moller AJ, Bejerholm C, Stoier S (2000) Long-term changes in performance and meat quality of Danish Landrace pigs: a study on a current compared with an unimproved genotype. Anim Sci 71:81–92
38.
go back to reference Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346–356CrossRef Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346–356CrossRef
39.
go back to reference Talmadge RJ, Roy RR (1993) Electrophoretic separation of rat skeletal muscle myosin heavy chain isoforms. J Appl Physiol 75:2337–2340 Talmadge RJ, Roy RR (1993) Electrophoretic separation of rat skeletal muscle myosin heavy chain isoforms. J Appl Physiol 75:2337–2340
40.
go back to reference Lefaucheur L, Ecolan P, Lossec G, Gabillard JC, Butler-Browne GS, Herpin P (2001) Influence of early postnatal cold exposure on myofiber maturation in pig skeletal muscle. J Muscle Res Cell Motil 22:439–452CrossRef Lefaucheur L, Ecolan P, Lossec G, Gabillard JC, Butler-Browne GS, Herpin P (2001) Influence of early postnatal cold exposure on myofiber maturation in pig skeletal muscle. J Muscle Res Cell Motil 22:439–452CrossRef
41.
go back to reference Kalbe C, Puppe B (2010) Long-term cognitive enrichment affects opioid receptor expression in the amygdala of domestic pigs. Genes Brain Behav 9:75–83CrossRef Kalbe C, Puppe B (2010) Long-term cognitive enrichment affects opioid receptor expression in the amygdala of domestic pigs. Genes Brain Behav 9:75–83CrossRef
42.
go back to reference Erkens T, van Poucke M, Vandesompele J, Goossens K, van Zeveren A, Peelman LJ (2006) Development of a new set of reference genes for normalization of real-time RT-PCR data of porcine backfat and longissimus dorsi muscle, and evaluation with PPARGCIA. BMC Biotechnol 6:41CrossRef Erkens T, van Poucke M, Vandesompele J, Goossens K, van Zeveren A, Peelman LJ (2006) Development of a new set of reference genes for normalization of real-time RT-PCR data of porcine backfat and longissimus dorsi muscle, and evaluation with PPARGCIA. BMC Biotechnol 6:41CrossRef
43.
go back to reference Langley-Evans SC, Gardner DS, Jackson AA (1996) Association of disproportionate growth of fetal rats in late gestation with raised systolic blood pressure in later life. J Reprod Fertil 106:307–312CrossRef Langley-Evans SC, Gardner DS, Jackson AA (1996) Association of disproportionate growth of fetal rats in late gestation with raised systolic blood pressure in later life. J Reprod Fertil 106:307–312CrossRef
44.
go back to reference Morise A, Seve B, Mace K, Magliola C, Le Huerou-luron I, Louveau I (2009) Impact of intrauterine growth retardation and early protein intake on growth, adipose tissue, and the insulin-like growth factor system in piglets. Pediatr Res 65:45–50CrossRef Morise A, Seve B, Mace K, Magliola C, Le Huerou-luron I, Louveau I (2009) Impact of intrauterine growth retardation and early protein intake on growth, adipose tissue, and the insulin-like growth factor system in piglets. Pediatr Res 65:45–50CrossRef
45.
go back to reference Halton TL, Hu FB (2004) The effects of high protein diets on thermogenesis, satiety and weight loss: a critical review. J Am Coll Nutr 23:373–385 Halton TL, Hu FB (2004) The effects of high protein diets on thermogenesis, satiety and weight loss: a critical review. J Am Coll Nutr 23:373–385
46.
go back to reference Kuhla B, Kucia M, Gors S, Albrecht D, Langhammer M, Kuhla S, Metges CC (2010) Effect of a high-protein diet on food intake and liver metabolism during pregnancy, lactation and after weaning in mice. Proteomics 10:2573–2588CrossRef Kuhla B, Kucia M, Gors S, Albrecht D, Langhammer M, Kuhla S, Metges CC (2010) Effect of a high-protein diet on food intake and liver metabolism during pregnancy, lactation and after weaning in mice. Proteomics 10:2573–2588CrossRef
47.
go back to reference Görs S, Lang IS, Stabenow B, Hennig U, Brüssow K, Otten W, Rehfeldt C, Metges CC (2010) Foetal umbilical venous and arterial plasma amino acid concentrations are depending on the protein level of gestation diets fed to gilts. In: Matteo Corvetto G (ed) Energy and protein metabolism and nutrition. EAAP publication No. 127, 3rd EAAP ISEP, Parma, Italy, 6–10 Sept 2010, The Netherlands, pp 221–223 Görs S, Lang IS, Stabenow B, Hennig U, Brüssow K, Otten W, Rehfeldt C, Metges CC (2010) Foetal umbilical venous and arterial plasma amino acid concentrations are depending on the protein level of gestation diets fed to gilts. In: Matteo Corvetto G (ed) Energy and protein metabolism and nutrition. EAAP publication No. 127, 3rd EAAP ISEP, Parma, Italy, 6–10 Sept 2010, The Netherlands, pp 221–223
48.
go back to reference Görs S, Lang IS, Junghans P, Hennig U, Stabenow B, Schneider F, Otten W, Rehfeldt C, Metges CC (2009) Influence of maternal low and high protein diets during pregnancy in young sows on glucose metabolism of their offspring. Proc Soc Nutr Physiol 18 (Abstr.) Görs S, Lang IS, Junghans P, Hennig U, Stabenow B, Schneider F, Otten W, Rehfeldt C, Metges CC (2009) Influence of maternal low and high protein diets during pregnancy in young sows on glucose metabolism of their offspring. Proc Soc Nutr Physiol 18 (Abstr.)
49.
go back to reference Kanitz E, Gräbner M, Tuchscherer M, Brüssow KP, Stabenow B, Rehfeldt C, Metges CC, Otten W (2010) An inadequate maternal protein diet during pregnancy in pigs alters the expression of corticosteroid receptors and 11ß-hydroxysteroid dehydrogenase isoforms in the placenta and fetal brain. Endocr Abstr 22:P261 Kanitz E, Gräbner M, Tuchscherer M, Brüssow KP, Stabenow B, Rehfeldt C, Metges CC, Otten W (2010) An inadequate maternal protein diet during pregnancy in pigs alters the expression of corticosteroid receptors and 11ß-hydroxysteroid dehydrogenase isoforms in the placenta and fetal brain. Endocr Abstr 22:P261
50.
go back to reference Gregoire FM, Smas CM, Sul HS (1998) Understanding adipocyte differentiation. Physiol Rev 78:783–809 Gregoire FM, Smas CM, Sul HS (1998) Understanding adipocyte differentiation. Physiol Rev 78:783–809
51.
go back to reference Bieswal F, Hay SM, McKinnon C, Reusens B, Cuignet M, Rees WD, Remacle C (2004) Prenatal protein restriction does not affect the proliferation and differentiation of rat preadipocytes. J Nutr 134:1493–1499 Bieswal F, Hay SM, McKinnon C, Reusens B, Cuignet M, Rees WD, Remacle C (2004) Prenatal protein restriction does not affect the proliferation and differentiation of rat preadipocytes. J Nutr 134:1493–1499
52.
go back to reference Sarr O, Louveau I, Kalbe C, Metges CC, Rehfeldt C, Gondret F (2010) Prenatal exposure to maternal low or high protein diets induces modest changes in the adipose tissue proteome of newborn piglets. J Anim Sci 88:1626–1641CrossRef Sarr O, Louveau I, Kalbe C, Metges CC, Rehfeldt C, Gondret F (2010) Prenatal exposure to maternal low or high protein diets induces modest changes in the adipose tissue proteome of newborn piglets. J Anim Sci 88:1626–1641CrossRef
53.
go back to reference Louveau I, Gondret F (2004) Regulation of development and metabolism of adipose tissue by growth hormone and the insulin-like growth factor system. Domest Anim Endocrinol 27:241–255CrossRef Louveau I, Gondret F (2004) Regulation of development and metabolism of adipose tissue by growth hormone and the insulin-like growth factor system. Domest Anim Endocrinol 27:241–255CrossRef
54.
go back to reference Kalbe C, Rehfeldt C (2005) Aspects of prenatal development of muscle and adipose tissue: principles, regulation, and influence of maternal nutrition. Berl Munch Tierarztl Wochenschr 118:509–520 Kalbe C, Rehfeldt C (2005) Aspects of prenatal development of muscle and adipose tissue: principles, regulation, and influence of maternal nutrition. Berl Munch Tierarztl Wochenschr 118:509–520
55.
go back to reference Wigmore PM, Stickland NC (1983) Muscle development in large and small pig fetuses. J Anat 137:235–245 Wigmore PM, Stickland NC (1983) Muscle development in large and small pig fetuses. J Anat 137:235–245
56.
go back to reference Lefaucheur L, Edom F, Ecolan P, Butlerbrowne GS (1995) Pattern of muscle-fiber type formation in the pig. Dev Dyn 203:27–41CrossRef Lefaucheur L, Edom F, Ecolan P, Butlerbrowne GS (1995) Pattern of muscle-fiber type formation in the pig. Dev Dyn 203:27–41CrossRef
57.
go back to reference Rehfeldt C, Kalbe C, Block J, Nürnberg G, Stabenow B, Metges CC (2008) Long-term effects of low and high protein feeding to pregnant sows on offspring at market weight. In: Proceedings of international congress of meat science & technology. 10–15 Aug 2008, Cape Town, South Africa, 7B.15 Rehfeldt C, Kalbe C, Block J, Nürnberg G, Stabenow B, Metges CC (2008) Long-term effects of low and high protein feeding to pregnant sows on offspring at market weight. In: Proceedings of international congress of meat science & technology. 10–15 Aug 2008, Cape Town, South Africa, 7B.15
58.
go back to reference Bonen A (2010) Muscles as molecular and metabolic machines. Am J Physiol Endocrinol Metab 299:E143–E144 Bonen A (2010) Muscles as molecular and metabolic machines. Am J Physiol Endocrinol Metab 299:E143–E144
59.
go back to reference Lefaucheur L, Hoffman R, Okamura C, Gerrard D, Leger JJ, Rubinstein N, Kelly A (1997) Transitory expression of alpha cardiac myosin heavy chain in a subpopulation of secondary generation muscle fibers in the pig. Dev Dyn 210:106–116CrossRef Lefaucheur L, Hoffman R, Okamura C, Gerrard D, Leger JJ, Rubinstein N, Kelly A (1997) Transitory expression of alpha cardiac myosin heavy chain in a subpopulation of secondary generation muscle fibers in the pig. Dev Dyn 210:106–116CrossRef
60.
go back to reference Langley-Evans SC, Gardner DS, Jackson AA (1996) Maternal protein restriction influences the programming of the rat hypothalamic-pituitary-adrenal axis. J Nutr 126:1578–1585 Langley-Evans SC, Gardner DS, Jackson AA (1996) Maternal protein restriction influences the programming of the rat hypothalamic-pituitary-adrenal axis. J Nutr 126:1578–1585
61.
go back to reference Edwards CR, Benediktsson R, Lindsay RS, Seckl JR (1996) 11 beta-Hydroxysteroid dehydrogenases: key enzymes in determining tissue-specific glucocorticoid effects. Steroids 61:263–269CrossRef Edwards CR, Benediktsson R, Lindsay RS, Seckl JR (1996) 11 beta-Hydroxysteroid dehydrogenases: key enzymes in determining tissue-specific glucocorticoid effects. Steroids 61:263–269CrossRef
62.
go back to reference Kayali AG, Young VR, Goodman MN (1987) Sensitivity of myofibrillar proteins to glucocorticoid-induced muscle proteolysis. Am J Physiol 252:E621–E626 Kayali AG, Young VR, Goodman MN (1987) Sensitivity of myofibrillar proteins to glucocorticoid-induced muscle proteolysis. Am J Physiol 252:E621–E626
63.
go back to reference Millward DJ, Garlick PJ, Nnanyelugo DO, Waterlow JC (1976) The relative importance of muscle protein synthesis and breakdown in the regulation of muscle mass. Biochem J 156:185–188 Millward DJ, Garlick PJ, Nnanyelugo DO, Waterlow JC (1976) The relative importance of muscle protein synthesis and breakdown in the regulation of muscle mass. Biochem J 156:185–188
64.
go back to reference Colenbrander B, de Jong FH, Wensing CJ (1978) Changes in serum testosterone concentrations in the male pig during development. J Reprod Fertil 53:377–380CrossRef Colenbrander B, de Jong FH, Wensing CJ (1978) Changes in serum testosterone concentrations in the male pig during development. J Reprod Fertil 53:377–380CrossRef
65.
go back to reference Mayer M, Rosen F (1977) Interaction of glucocorticoids and androgens with skeletal muscle. Metabolism 26:937–962CrossRef Mayer M, Rosen F (1977) Interaction of glucocorticoids and androgens with skeletal muscle. Metabolism 26:937–962CrossRef
66.
go back to reference Zhao W, Pan J, Zhao Z, Wu Y, Bauman WA, Cardozo CP (2008) Testosterone protects against dexamethasone-induced muscle atrophy, protein degradation and MAFbx upregulation. J Steroid Biochem Mol Biol 110:125–129CrossRef Zhao W, Pan J, Zhao Z, Wu Y, Bauman WA, Cardozo CP (2008) Testosterone protects against dexamethasone-induced muscle atrophy, protein degradation and MAFbx upregulation. J Steroid Biochem Mol Biol 110:125–129CrossRef
67.
go back to reference Graebner M, Kanitz E, Tuchscherer M, Stabenow B, Metges CC, Rehfeldt C, Otten W (2009) Maternal low and high protein diets during pregnancy affect body weight and stress reactivity in the offspring of pigs. J Anim Sci 87 E-Suppl 2/J Dairy Sci 92 E-Suppl. 1:234 (Abstr.) Graebner M, Kanitz E, Tuchscherer M, Stabenow B, Metges CC, Rehfeldt C, Otten W (2009) Maternal low and high protein diets during pregnancy affect body weight and stress reactivity in the offspring of pigs. J Anim Sci 87 E-Suppl 2/J Dairy Sci 92 E-Suppl. 1:234 (Abstr.)
68.
go back to reference Florini JR, Magri KA, Ewton DZ, James PL, Grindstaff K, Rotwein PS (1991) “Spontaneous” differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. J Biol Chem 266:15917–15923 Florini JR, Magri KA, Ewton DZ, James PL, Grindstaff K, Rotwein PS (1991) “Spontaneous” differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. J Biol Chem 266:15917–15923
69.
go back to reference Florini JR, Ewton DZ, Coolican SA (1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 17:481–517 Florini JR, Ewton DZ, Coolican SA (1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 17:481–517
70.
go back to reference Kalbe C, Mau M, Rehfeldt C (2008) Developmental changes and the impact of isoflavones on mRNA expression of IGF-I receptor, EGF receptor and related growth factors in porcine skeletal muscle cell cultures. Growth Horm IGF Res 18:424–433CrossRef Kalbe C, Mau M, Rehfeldt C (2008) Developmental changes and the impact of isoflavones on mRNA expression of IGF-I receptor, EGF receptor and related growth factors in porcine skeletal muscle cell cultures. Growth Horm IGF Res 18:424–433CrossRef
71.
go back to reference Lee CY, Chung CS, Simmen FA (1993) Ontogeny of the porcine insulin-like growth factor system. Mol Cell Endocrinol 93:71–80CrossRef Lee CY, Chung CS, Simmen FA (1993) Ontogeny of the porcine insulin-like growth factor system. Mol Cell Endocrinol 93:71–80CrossRef
72.
go back to reference Peng M, Pelletier G, Palin MF, Veronneau S, LeBel D, Abribat T (1998) Ontogeny of IGFs and IGFBPs mRNA levels and tissue concentrations in liver, kidney and skeletal muscle of pig. Growth Dev Aging 60:171–187 Peng M, Pelletier G, Palin MF, Veronneau S, LeBel D, Abribat T (1998) Ontogeny of IGFs and IGFBPs mRNA levels and tissue concentrations in liver, kidney and skeletal muscle of pig. Growth Dev Aging 60:171–187
73.
go back to reference 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 76:1004–1011 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 76:1004–1011
74.
go back to reference Fix JS, Cassady JP, Herring WO, Holl JW, Culbertson MS, See MT (2010) Effect of piglet birth weight on body weight, growth, backfat, and longissimus muscle area of commercial market swine. Livest Sci 127:51–59CrossRef Fix JS, Cassady JP, Herring WO, Holl JW, Culbertson MS, See MT (2010) Effect of piglet birth weight on body weight, growth, backfat, and longissimus muscle area of commercial market swine. Livest Sci 127:51–59CrossRef
75.
go back to reference Beaulieu AD, Aalhus JL, Williams NH, Patience JF (2010) Impact of piglet birth weight, birth order, and litter size on subsequent growth performance, carcass quality, muscle composition, and eating quality of pork. J Anim Sci 88:2767–2778CrossRef Beaulieu AD, Aalhus JL, Williams NH, Patience JF (2010) Impact of piglet birth weight, birth order, and litter size on subsequent growth performance, carcass quality, muscle composition, and eating quality of pork. J Anim Sci 88:2767–2778CrossRef
76.
go back to reference Bieswal F, Ahn MT, Reusens B, Holvoet P, Raes M, Rees WD, Remacle C (2006) The importance of catch-up growth after early malnutrition for the programming of obesity in male rat. Obesity (Silver Spring) 14:1330–1343CrossRef Bieswal F, Ahn MT, Reusens B, Holvoet P, Raes M, Rees WD, Remacle C (2006) The importance of catch-up growth after early malnutrition for the programming of obesity in male rat. Obesity (Silver Spring) 14:1330–1343CrossRef
77.
go back to reference Bol VV, Delattre AI, Reusens B, Raes M, Remacle C (2009) Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice. Am J Physiol Regul Integr Comp Physiol 297:R291–R299CrossRef Bol VV, Delattre AI, Reusens B, Raes M, Remacle C (2009) Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice. Am J Physiol Regul Integr Comp Physiol 297:R291–R299CrossRef
78.
go back to reference Liang J, Zhang X, Zhao R, Maak S, Yang X (2010) Effect of maternal protein restriction on lipid metabolism in Meishan piglets at weaning. Livest Sci 136:157–163CrossRef Liang J, Zhang X, Zhao R, Maak S, Yang X (2010) Effect of maternal protein restriction on lipid metabolism in Meishan piglets at weaning. Livest Sci 136:157–163CrossRef
79.
go back to reference Snoeck A, Remacle C, Reusens B, Hoet JJ (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57:107–118CrossRef Snoeck A, Remacle C, Reusens B, Hoet JJ (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57:107–118CrossRef
80.
go back to reference Bennis-Taleb N, Remacle C, Hoet JJ, Reusens B (1999) A low-protein isocaloric diet during gestation affects brain development and alters permanently cerebral cortex blood vessels in rat offspring. J Nutr 129:1613–1619 Bennis-Taleb N, Remacle C, Hoet JJ, Reusens B (1999) A low-protein isocaloric diet during gestation affects brain development and alters permanently cerebral cortex blood vessels in rat offspring. J Nutr 129:1613–1619
Metadata
Title
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
Authors
Charlotte Rehfeldt
Louis Lefaucheur
Jana Block
Bernd Stabenow
Ralf Pfuhl
Winfried Otten
Cornelia C. Metges
Claudia Kalbe
Publication date
01-03-2012
Publisher
Springer-Verlag
Published in
European Journal of Nutrition / Issue 2/2012
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-011-0201-8

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