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Pre- and early-postnatal nutrition modify gene and protein expressions of muscle energy metabolism markers and phospholipid Fatty Acid composition in a muscle type specific manner in sheep.

Hou L, Kongsted AH, Ghoreishi SM, Takhtsabzy TK, Friedrichsen M, Hellgren LI, Kadarmideen HN, Vaag A, Nielsen MO - PLoS ONE (2013)

Bottom Line: Except for fatty acid oxidation genes, these changes persisted into adulthood.No persistent expression changes were observed in BF and VSC.Tissues other than muscle may account for reduced whole body insulin sensitivity in adult LOW sheep.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Clinical and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg, Denmark.

ABSTRACT
We previously reported that undernutrition in late fetal life reduced whole-body insulin sensitivity in adult sheep, irrespective of dietary exposure in early postnatal life. Skeletal muscle may play an important role in control of insulin action. We therefore studied a range of putative key muscle determinants of insulin signalling in two types of skeletal muscles (longissimus dorsi (LD) and biceps femoris (BF)) and in the cardiac muscle (ventriculus sinister cordis (VSC)) of sheep from the same experiment. Twin-bearing ewes were fed either 100% (NORM) or 50% (LOW) of their energy and protein requirements during the last trimester of gestation. From day-3 postpartum to 6-months of age (around puberty), twin offspring received a high-carbohydrate-high-fat (HCHF) or a moderate-conventional (CONV) diet, whereafter all males were slaughtered. Females were subsequently raised on a moderate diet and slaughtered at 2-years of age (young adults). The only long-term consequences of fetal undernutrition observed in adult offspring were lower expressions of the insulin responsive glucose transporter 4 (GLUT4) protein and peroxisome proliferator-activated receptor gamma, coactivator 1α (PGC1α) mRNA in BF, but increased PGC1α expression in VSC. Interestingly, the HCHF diet in early postnatal life was associated with somewhat paradoxically increased expressions in LD of a range of genes (but not proteins) related to glucose uptake, insulin signalling and fatty acid oxidation. Except for fatty acid oxidation genes, these changes persisted into adulthood. No persistent expression changes were observed in BF and VSC. The HCHF diet increased phospholipid ratios of n-6/n-3 polyunsaturated fatty acids in all muscles, even in adults fed identical diets for 1½ years. In conclusion, early postnatal, but not late gestation, nutrition had long-term consequences for a number of determinants of insulin action and metabolism in LD. Tissues other than muscle may account for reduced whole body insulin sensitivity in adult LOW sheep.

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Related in: MedlinePlus

Principal component analysis score and loading plots for muscle phospholipid components of 2-years old sheep.Panel A and B, biceps femoris; panel C and D, longissimus dorsi; panel E and F, ventriculus sinister cordis. Panels A, C, and E are score plots; panels B, D, and F are loading plots. The first two principle components (PC) are plotted. NC, NH, LC, LH refer to experimental treatment groups. N and L refer to the prenatal nutrition offered to the twin-pregnant dams and fulfilling 100% and 50%, respectively, of daily requirements for energy and protein. C and H refer to a moderate or high-carbohydrate-high-fat diet, respectively, fed during the first 6 months of postnatal life. Legends for all panels are shown at the bottom of panel E.
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pone-0065452-g005: Principal component analysis score and loading plots for muscle phospholipid components of 2-years old sheep.Panel A and B, biceps femoris; panel C and D, longissimus dorsi; panel E and F, ventriculus sinister cordis. Panels A, C, and E are score plots; panels B, D, and F are loading plots. The first two principle components (PC) are plotted. NC, NH, LC, LH refer to experimental treatment groups. N and L refer to the prenatal nutrition offered to the twin-pregnant dams and fulfilling 100% and 50%, respectively, of daily requirements for energy and protein. C and H refer to a moderate or high-carbohydrate-high-fat diet, respectively, fed during the first 6 months of postnatal life. Legends for all panels are shown at the bottom of panel E.

Mentions: Visualized by PCA, the HCHF diet as expected had substantial impact on the FA-composition in the PL fraction of each muscle type in 6-months old lambs (data not shown). Interestingly, after dietary correction and feeding with the same diet for 1.5 years, these remarkable differences in PL FA-composition were still evident in 2-years old sheep (Figure 5).


Pre- and early-postnatal nutrition modify gene and protein expressions of muscle energy metabolism markers and phospholipid Fatty Acid composition in a muscle type specific manner in sheep.

Hou L, Kongsted AH, Ghoreishi SM, Takhtsabzy TK, Friedrichsen M, Hellgren LI, Kadarmideen HN, Vaag A, Nielsen MO - PLoS ONE (2013)

Principal component analysis score and loading plots for muscle phospholipid components of 2-years old sheep.Panel A and B, biceps femoris; panel C and D, longissimus dorsi; panel E and F, ventriculus sinister cordis. Panels A, C, and E are score plots; panels B, D, and F are loading plots. The first two principle components (PC) are plotted. NC, NH, LC, LH refer to experimental treatment groups. N and L refer to the prenatal nutrition offered to the twin-pregnant dams and fulfilling 100% and 50%, respectively, of daily requirements for energy and protein. C and H refer to a moderate or high-carbohydrate-high-fat diet, respectively, fed during the first 6 months of postnatal life. Legends for all panels are shown at the bottom of panel E.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3675032&req=5

pone-0065452-g005: Principal component analysis score and loading plots for muscle phospholipid components of 2-years old sheep.Panel A and B, biceps femoris; panel C and D, longissimus dorsi; panel E and F, ventriculus sinister cordis. Panels A, C, and E are score plots; panels B, D, and F are loading plots. The first two principle components (PC) are plotted. NC, NH, LC, LH refer to experimental treatment groups. N and L refer to the prenatal nutrition offered to the twin-pregnant dams and fulfilling 100% and 50%, respectively, of daily requirements for energy and protein. C and H refer to a moderate or high-carbohydrate-high-fat diet, respectively, fed during the first 6 months of postnatal life. Legends for all panels are shown at the bottom of panel E.
Mentions: Visualized by PCA, the HCHF diet as expected had substantial impact on the FA-composition in the PL fraction of each muscle type in 6-months old lambs (data not shown). Interestingly, after dietary correction and feeding with the same diet for 1.5 years, these remarkable differences in PL FA-composition were still evident in 2-years old sheep (Figure 5).

Bottom Line: Except for fatty acid oxidation genes, these changes persisted into adulthood.No persistent expression changes were observed in BF and VSC.Tissues other than muscle may account for reduced whole body insulin sensitivity in adult LOW sheep.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Clinical and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg, Denmark.

ABSTRACT
We previously reported that undernutrition in late fetal life reduced whole-body insulin sensitivity in adult sheep, irrespective of dietary exposure in early postnatal life. Skeletal muscle may play an important role in control of insulin action. We therefore studied a range of putative key muscle determinants of insulin signalling in two types of skeletal muscles (longissimus dorsi (LD) and biceps femoris (BF)) and in the cardiac muscle (ventriculus sinister cordis (VSC)) of sheep from the same experiment. Twin-bearing ewes were fed either 100% (NORM) or 50% (LOW) of their energy and protein requirements during the last trimester of gestation. From day-3 postpartum to 6-months of age (around puberty), twin offspring received a high-carbohydrate-high-fat (HCHF) or a moderate-conventional (CONV) diet, whereafter all males were slaughtered. Females were subsequently raised on a moderate diet and slaughtered at 2-years of age (young adults). The only long-term consequences of fetal undernutrition observed in adult offspring were lower expressions of the insulin responsive glucose transporter 4 (GLUT4) protein and peroxisome proliferator-activated receptor gamma, coactivator 1α (PGC1α) mRNA in BF, but increased PGC1α expression in VSC. Interestingly, the HCHF diet in early postnatal life was associated with somewhat paradoxically increased expressions in LD of a range of genes (but not proteins) related to glucose uptake, insulin signalling and fatty acid oxidation. Except for fatty acid oxidation genes, these changes persisted into adulthood. No persistent expression changes were observed in BF and VSC. The HCHF diet increased phospholipid ratios of n-6/n-3 polyunsaturated fatty acids in all muscles, even in adults fed identical diets for 1½ years. In conclusion, early postnatal, but not late gestation, nutrition had long-term consequences for a number of determinants of insulin action and metabolism in LD. Tissues other than muscle may account for reduced whole body insulin sensitivity in adult LOW sheep.

Show MeSH
Related in: MedlinePlus