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Growth and metabolism of fetal and maternal muscles of adolescent sheep on adequate or high feed intakes: possible role of protein kinase C-α in fetal muscle growth

Published online by Cambridge University Press:  09 March 2007

Robert M. Palmer*
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Michael G. Thompson
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Chrystel Meallet
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Amanda Thom
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Raymond P. Aitken
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Jacqueline M. Wallace
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
*
*Corresponding author:Dr Robert Palmer, fax +44 (0) 1224 716629, email [email protected]
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Abstract

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From days 4–104 of pregnancy, adolescent sheep, weighing 43·7 (SE 0·87)kg were offered a complete diet at two different intakes (approximately 5 or 15 kg/week) designed to meet slightly, or well above, maternal maintenance requirements. The fetal and maternal muscles were taken on day 104 of pregnancy and analysed for total DNA, RNA and protein. Ewes offered a high intake to promote rapid maternal weight gain, weighed more (76·5 (SE 4·5) v. 50·0 (SE 1·7) kg) and had muscles with a greater fresh weight, whilst their fetuses had smaller muscles, than those fed at a lower intake. Plantaris muscle of the ewes fed at the high intake contained more RNA and protein; again the opposite situation was found in the fetal muscle. On the higher maternal intakes, the DNA, RNA and protein contents of the fetal plantaris muscle were less than in fetuses of ewes fed at the lower intake. To investigate the possible mechanisms involved in this decrease in fetal muscle mass, cytosolic and membrane-associated muscle proteins were subjected to Western immunoblotting with antibodies to nine isoforms of protein kinase C (PKC), a family of enzymes known to play an important role in cell growth. Five PKC isoforms (α, ε, θ, μ and ζ) were identified in fetal muscle. One of these, PKC-α, was located predominantly in the cytosolic compartment in the smaller fetuses of the ewes fed at a high plane of nutrition, but was present to a greater extent in the membranes of the more rapidly growing fetuses of the ewes fed at the lower intake. This was the only isoform to demonstrate nutritionally related changes in its subcellular compartmentation suggesting that it may mediate some aspects of the change in fetal growth rate.

Type
Animal Nutrition
Copyright
Copyright © The Nutrition Society 1998

References

Ashford, AJ & Pain, VM (1986) Effect of diabetes on the rates of synthesis and degradation of ribosomes in rat muscle and liver in vivo. Journal of Biological Chemistry 261, 40594065.CrossRefGoogle ScholarPubMed
Avignon, A, Yamada, K, Zhou, X, Spencer, B, Cardona, O, Saba Siddique, S, Galloway, L, Standaert, ML & Farese, RV (1996) Chronic activation of protein kinase C in soleus muscle and other tissues of insulin resistant, obese Zucker rats. Diabetes 45, 13941404.CrossRefGoogle Scholar
Bell, RM (1986) Protein kinase C activation by diacylglycerol second messengers. Cell 45, 631632.CrossRefGoogle ScholarPubMed
Berry, N, Ase, K, Kishimoto, A & Nishizuka, Y (1990) Activation of resting human T cells requires prolonged stimulation of protein kinase C. Proceedings of the National Academy of Sciences USA 87, 22942298.CrossRefGoogle Scholar
Burton, K (1956) A study of the conditions and mechanisms of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochemical Journal 62, 315318.CrossRefGoogle ScholarPubMed
Chin, JE, Dickens, M, Tavare, JM & Roth, RA (1993) Over-expression of protein kinase C isoenzymes α, β-I, gamma and ε in cells overexpressing the insulin receptor. Journal of Biological Chemistry 268, 63386347.CrossRefGoogle Scholar
de Haro, C, Mendez, R & Santoyo, J (1996) The eIF-2α kinases and the control of protein synthesis. FASEB Journal 10, 13781387.CrossRefGoogle ScholarPubMed
Garlick, PJ, McNurlan, MA & Preedy, VR (1980) A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of [3H]-phenylalanine. Biochemical Journal 192, 719723.CrossRefGoogle ScholarPubMed
Godson, C, Bell, KS & Insel, PA (1993) Inhibition of expression of protein kinase C α by antisense cDNA inhibits phorbol ester-mediated arachidonate release. Journal of Biological Chemistry 268, 1194611950.CrossRefGoogle ScholarPubMed
Godson, C, Masliah, E, Balboa, MA, Ellisman, MH & Insel, PA (1996) Isoform-specific redistribution of protein kinase C in living cells. Biochimica et Biophysica Acta 1313, 6371.CrossRefGoogle ScholarPubMed
Hei, Y-J, McNeill, JH, Sanghera, JS, Diamond, J, Bryer-Ash, M & Pelech, SL (1993) Characterisation of insulin-stimulated seryl/ threonyl kinases in rat skeletal muscle. Journal of Biological Chemistry 268, 1320313213.CrossRefGoogle ScholarPubMed
Hei, Y-J, Pelech, SL, Chen, X, Diamond, J & McNeill, JH (1994) Purification and characterisation of a novel ribosomal S6-kinase from skeletal muscle of insulin treated rats. Journal of Biological Chemistry 269, 78167823.CrossRefGoogle ScholarPubMed
Hong, D-H, Huan, J, Ou, BR, YehJ-Y, J-Y,, Saido, TC, Cheeke, PR & Forsberg, NE (1995) Protein kinase C isoforms in muscle cells and their regulation by phorbol ester and calpain. Biochimica et Biophysica Acta 1267, 4554.CrossRefGoogle ScholarPubMed
Jaken, S (1996) Protein kinase C isozymes and substrates. Current Opinion in Cell Biology 8, 168173.CrossRefGoogle ScholarPubMed
Kraft, AS & Anderson, WB (1983) Phorbol esters increase the amount of Ca2+, phospholipid dependent protein kinase associated with plasma membrane. Nature 301, 621623.CrossRefGoogle ScholarPubMed
Lisanti, MP, Scherer, PE, Vidugiriene, J, Tang, Z, Hermanowski-Vosatka, A, Tu, Y-H, Cook, RF & Sargiacomo, M (1994) Characterisation of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. Journal of Cellular Biology 126, 111126.CrossRefGoogle ScholarPubMed
Liu, J-P (1996) Protein kinase C and its substrates. Molecular and Cellular Endocrinology 116, 129.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL & Randall, RJ (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265272.CrossRefGoogle ScholarPubMed
Morrison, KS, Mackie, SC, Palmer, RM & Thompson, MG (1995) Stimulation of protein and DNA synthesis in mouse C2C12 satellite cells: evidence for phospholipase D-dependent and -independent pathways. Journal of Cellular Physiology 165, 273283.CrossRefGoogle ScholarPubMed
Naismith, DJ (1969) The foetus as a parasite. Proceedings of the Nutrition Society 28, 2531.CrossRefGoogle ScholarPubMed
Nishizuka, Y (1995) Protein kinase C and lipid signalling for sustained cellular responses. FASEB Journal 9, 484496.CrossRefGoogle ScholarPubMed
Palmer, RM, Thom, A & Flint, DJ (1996) Repartitioning of maternal muscle towards the foetus induced by a polyclonal antibody to rat growth hormone. Journal of Endocrinology 151, 395400.CrossRefGoogle Scholar
Pause, A, Belsham, GJ, Lin, TA, Lawrence, JC Jr & Sonenberg, N (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5'-cap function. Nature 371, 762767.CrossRefGoogle Scholar
Reeds, PJ & Palmer, RM (1983) The possible involvement of prostaglandin F2 α in the stimulation of muscle protein synthesis by insulin. Biochemical and Biophysical Research Communications 116, 10841090.CrossRefGoogle ScholarPubMed
Russel, AJF, Doney, JM & Gunn, RG (1969) Subjective assessment of body fat in live sheep. Journal of Agricultural Science, Cambridge 72, 451454.CrossRefGoogle Scholar
Scholl, TO & Hediger, ML (1993) A review of the epidemiology of nutrition and adolescent pregnancy: maternal growth during pregnancy and its effect on the fetus. Journal of the American College of Nutrition 12, 101107.CrossRefGoogle ScholarPubMed
Smart, EJ, Ying, Y-S, Mineo, C & Anderson, RGW (1995) A detergent-free method for purifying caveolae membrane from tissue culture cells. Proceedings of the National Academy of Sciences USA 92, 1010410108.CrossRefGoogle ScholarPubMed
Thompson, MG, Mackie, SC, Thom, A & Palmer, RM (1997) Regulation of phospholipase D in L6 skeletal muscle myoblasts: role of protein kinase C and relationship to protein synthesis. Journal of Biological Chemistry 272, 1091010916.CrossRefGoogle ScholarPubMed
Wallace, JM, Aitken, RP & Cheyne, MA (1996) Nutrient partitioning and fetal growth in rapidly growing adolescent ewes. Journal of Reproduction and Fertility 107, 183190.CrossRefGoogle ScholarPubMed
Yamada, K, Avignon, A, Standaert, ML, Cooper, DR, Spencer, B & Farese, RV (1995) Effects of insulin on the translocation of protein kinase C-θ and other protein kinase C isoforms in rat skeletal muscles. Biochemical Journal 308, 177180.CrossRefGoogle Scholar
Zappelli, F, Willems, D, Osada, S, Ohno, S, Wetsel, WC, Molinaro, M, Cossu, G & Bouche, M (1996) The inhibition of differentiation caused by TGF β in fetal myoblasts is dependent upon selective expression of PKC θ: a possible molecular basis for myoblast diversification during limb histogenesis. Developmental Biology 180, 156164.CrossRefGoogle Scholar