Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-28T05:17:04.291Z Has data issue: false hasContentIssue false
  • English
  • Français

Activation of skeletal muscle protein breakdown following consumption of soyabean protein in pigs

Published online by Cambridge University Press:  09 March 2007

B. Löhrke ,
E. Saggau ,
R. Schadereit ,
M. Beyer ,
O. Bellmann ,
S. Kuhla  and
H. Hagemeister
B. Löhrke*
Affiliation:
Research Institute for Biology of Farm Animals, Dummerstorf-Rostock, Departments of Animal Nutrition “Oscar Kellner“ and Genetics and Biometry, 18059 Rostock, Justus-von-Liebig-Weg 2, Germany
E. Saggau
Affiliation:
Research Institute for Biology of Farm Animals, Dummerstorf-Rostock, Departments of Animal Nutrition “Oscar Kellner“ and Genetics and Biometry, 18059 Rostock, Justus-von-Liebig-Weg 2, Germany
R. Schadereit
Affiliation:
Research Institute for Biology of Farm Animals, Dummerstorf-Rostock, Departments of Animal Nutrition “Oscar Kellner“ and Genetics and Biometry, 18059 Rostock, Justus-von-Liebig-Weg 2, Germany
M. Beyer
Affiliation:
Research Institute for Biology of Farm Animals, Dummerstorf-Rostock, Departments of Animal Nutrition “Oscar Kellner“ and Genetics and Biometry, 18059 Rostock, Justus-von-Liebig-Weg 2, Germany
O. Bellmann
Affiliation:
Research Institute for Biology of Farm Animals, Dummerstorf-Rostock, Departments of Animal Nutrition “Oscar Kellner“ and Genetics and Biometry, 18059 Rostock, Justus-von-Liebig-Weg 2, Germany
S. Kuhla
Affiliation:
Research Institute for Biology of Farm Animals, Dummerstorf-Rostock, Departments of Animal Nutrition “Oscar Kellner“ and Genetics and Biometry, 18059 Rostock, Justus-von-Liebig-Weg 2, Germany
H. Hagemeister
Affiliation:
Research Institute for Biology of Farm Animals, Dummerstorf-Rostock, Departments of Animal Nutrition “Oscar Kellner“ and Genetics and Biometry, 18059 Rostock, Justus-von-Liebig-Weg 2, Germany
*
*Corresponding author: Dr Berthold Löhrke, fax +49 382 08 686 02, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Diets with protein of inferior quality may increase protein breakdown in skeletal muscle but the experimental results are inconsistent. To elucidate the relationship, pigs were fed isoenergetic and isonitrogenous diets based on soyabean-protein isolate or casein for 15 weeks, with four to six animals per group. A higher plasma level of urea (2.5-fold the casein group value, P=0.01), higher urinary N excretion (2.1-fold the casein group value, P=0.01), a postabsorptive rise in the plasma levels of urea, 3-methylhistidine and isoleucine in soyabean protein-fed pigs suggested recruitment of circulatory amino acids by protein breakdown in peripheral tissues. Significant differences between dietary groups were detected in lysosomal and ATP-dependent proteolytic activities in the semimembranosus muscle of food-deprived pigs. A higher concentration of cathepsin B protein was found, corresponding to a rise in the cathepsin B activity, in response to dietary soyabean protein. Muscle ATP-stimulated proteolytical activity was 1.6-fold the casein group value (P=0.03). A transient rise in the level of cortisol (2.9-times the casein group value, P=0.02) occurred in the postprandial phase only in the soyabean group. These data suggest that the inferior quality of dietary soyabean protein induces hormonally-mediated upregulation of muscle protein breakdown for recruitment of circulatory amino acids in a postabsorptive state.

Keywords

Amino acid limitationProtein degradationEnergy retention
Type
Research Article
Information
British Journal of Nutrition , Volume 85 , Issue 4 , April 2001 , pp. 447 - 457
Copyright
Copyright © The Nutrition Society 2001

References

Assfalg-Machleidt, I, Rothe, G, Klingel, S, Banati, R, Mangel, WF, Valet, G & Machleidt, W (1992) Membrane permeable fluorogenic rhodamine substrates for selective determination of cathepsin L. Biological Chemistry Hoppe-Seyler 373, 433–440.CrossRefGoogle ScholarPubMed
Attaix, D, Aurousseau, E, Combaret, L, Kee, A, Larbaud, D, Ralliere, C, Souweine, B, Taillandier, D & Tilignac, T (1998) Ubiquitin-proteasome-dependent proteolysis in skeletal muscle. Reproduction Nutrition Development 38, 153–165.CrossRefGoogle ScholarPubMed
Baricos, WH, Zhou, Y, Mason, RW & Barrett, AJ (1988) Human kidney cathepsins B and L. Characterization and potential role in degradation of glomerular basement membrane. Biochemical Journal 252, 301–304.CrossRefGoogle ScholarPubMed
Barrett, AJ, Rawlings, ND, Davies, ME, Machleidt, W, Salvesen, G & Turk, V (1986) Cysteine proteinase inhibitors of cystatin superfamily. Proteinase Inhibitors pp.515–569[AJ, Barrett & G, Salvesen, editors]. Amsterdam: Elsevier.Google Scholar
Belkhou, R, Bechet, D, Cherel, Y, Galluser, M, Ferrara, M & le Maho, Y (1994) Effect of fasting and thyroidectomy on cysteine proteinase activities in liver and muscle. Biochimica et Biophysica Acta 1199, 195–201.CrossRefGoogle ScholarPubMed
Bonadonna, RC, Saccomani, MP, Cobelli, C & DeFronzo, RA (1993) Effect of insulin on system A amino acid transport in human skeletal muscle. Journal of Clinical Investigation 91, 514–521.CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Bruhat, A, Jousse, C, Wang, XZ, Ron, D, Ferrara, M & Fafournoux, P (1997) Amino acid limitation induces expression of CHOP, a CCAAT/enhancer binding protein-related gene, at both transcriptional and post-transcriptional levels. Journal of Biological Chemistry 272, 17588–17593.CrossRefGoogle Scholar
Chua, SC, Brown, AW, Kim, Y, Hennessey, KL, Leibel, RL & Hirsch, J (1991) Food deprivation and hypothalamic neuropeptide gene expression effects of strain background and the diabetes mutation. Molecular Brain Research 11, 291–299.CrossRefGoogle ScholarPubMed
Cannon, JG, Maydani, SN, Fielding, RA, Fiatarone, MA, Maydani, M, Farhangmer, M, Orencole, SF, Blumberg, J & Evans, WJ (1991) Acute phase response in exercise: Associations between vitamin E, cytokines, and muscle proteolysis. American Journal of Physiology 60, R1235–R1240.Google Scholar
Deutz, NE, Bruins, MJ & Soeters, PB (1998) Infusion of soy and casein protein meals affects interorgan amino acid metabolism and urea kinetics differently in pigs. Journal of Nutrition 128, 2435–2445.CrossRefGoogle ScholarPubMed
Dick, LR, Cruidshank, AA, Grenier, L, Melandri, FD, Nunes, SL & Stein, RL (1996) Mechanistic studies on the inactivation of the proteasome by lactacystin. Journal of Biological Chemistry 271, 7273–7276.CrossRefGoogle ScholarPubMed
Driscoll, J & Goldberg, AL (1990) The proteasome (multicatalytic protease) is a component of the 1500 kDa proteolytic complex which degrade ubiquitin-conjugated proteins. Journal of Biological Chemistry 268, 23593–23600.Google Scholar
Fenteany, G, Standaert, RF, Lane, WS, Choi, S, Corey, EJ & Schreiber, SL (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268, 726–731.CrossRefGoogle ScholarPubMed
Fereday, A, Gibson, NR, Cox, M, Pacy, DJ & Millward, DJ (1998) Variation in the apparent sensitivity of the insulin-mediated inhibition of proteolysis to amino acid supply determines the efficiency of protein utilization. Clinical Science 95, 725–733.CrossRefGoogle ScholarPubMed
Fuller, MF, Reeds, PJ, Cadenheay, A & Seve, B (1987) Effects of the amount and quality of dietary protein on nitrogen metabolism and protein turnover of pigs. British Journal of Nutrition 58, 287–300.CrossRefGoogle ScholarPubMed
Garlick, PJ & Grant, I (1988) Amino acid infusion increases the sensitivity of muscle protein synthesis in vivo to insulin. Effect of branched-chain amino acids. Biochemical Journal 254, 579–584.CrossRefGoogle ScholarPubMed
Garlick, PJ, Clugston, GA & Waterlow, JC (1980) Influence of low energy diets on whole body protein turnover in obese subjects. American Journal of Physiology 238, E235–E244.Google ScholarPubMed
Glickman, MH, Rubin, DM, Coux, O, Wefes, I, Pfeifer, G, Cjeka, Z, Baumeister, W, Fried, VA & Finley, D (1998) A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94, 615–623.CrossRefGoogle Scholar
Grizard, JD, Dardevet, O, Papet, I, Masoni, L, Patureau, P, Attaix, D, Tauveron, I, Bonin, D & Arnal, M (1995) Nutrient regulation of skeletal muscle protein metabolism in animals. Nutrition Research Reviews 8, 67–91.CrossRefGoogle ScholarPubMed
Grofte, T, Jensen, DS, Gronbaek, H, Wolthers, T, Jensen, SA, Tygstrup, N & Vilstrup, H (1998) Effects of growth hormone on steroid-induced increase in ability of urea synthesis and urea enzyme mRNA levels. American Journal of Physiology 275, E79–E86.Google ScholarPubMed
Hajduch, E, Alessi, DR, Hemmings, BA & Hundal, HS (1998) Constitutive activation of protein kinase Bα by membrane targeting promotes glucose and system A amino acid transport, protein synthesis, and inactivation of glycogen synthase kinase 3 in L6 muscle cells. Diabetes 47, 1006–1013.CrossRefGoogle Scholar
Hall-Angeras, M, Hasselgren, PO, Dimlich, RV & Fischer, JE (1991) Myofibrillar proteinase, cathepsin B, and protein breakdown rates in skeletal muscle from septic rats. Metabolism 40, 302–306.CrossRefGoogle ScholarPubMed
Hansen, K, Sickelmann, F, Pietrowsky, R, Fehm, HL & Born, J (1997) Systemic immune changes following meal intake in humans. American Journal of Physiology 273, R548–R553.Google ScholarPubMed
Harris, CJ & Milne, G (1987) The identification of the N tau-methyl histidine-containing dipeptide, balanine, in muscle extracts from various mammals and the chicken. Comparative Biochemistry and Physiology B 86, 273–279.CrossRefGoogle Scholar
Hawrylewicz, EJ, Zapata, JJ & Blair, WH (1995) Soy and experimental cancer: animal studies. Journal of Nutrition 125, 6985–7085.Google ScholarPubMed
He, Y, Chen, H, Quon, MJ & Reitman, M (1995) The mouse obese gen. Genomic organization, promoter activity, and activation by CCAAT/enhancer-binding protein. Journal of Biological Chemistry 270, 28887–28891.CrossRefGoogle Scholar
Hirao, T, Hara, K & Takahashi, K (1984) Purification and characterization of cathepsin B from monkey skeletal muscle. Journal of Biochemistry 95, 871–879.CrossRefGoogle ScholarPubMed
Hoffmann, L, Beyer, M & Jentsch, W (1993) Abhängigkeit von Brutto-, verdaulicher und umsetzbarer Ernergie des Futters sowie des Energieansatzes vom Gehalt von verdaulichen Nährstoffen unter Berücksichtigung von Stärke und Zucker (Dependence of dietary total, digestible and metabolizable energy and of energy deposition on the content of digestible nutrients in consideration of starch and sugar). Archives of Animal Nutrition 44, 123–137.Google Scholar
Hong, BH & Forsberg, NE (1995) Effects of dexamethasone on protein degradation and protease gene expression in rat L8 myotube cultures. Molecular and Cellular Endocrinology 108, 199–209.CrossRefGoogle ScholarPubMed
Inubushi, T, Shikiji, M, Endo, K, Kakegawa, H, Kishino, Y & Katunuma, N (1996) Hormonal and dietary regulation of lysosomal cysteine proteinases in liver under gluconeogenesis conditions. Biological Chemistry Hoppe-Seyler 377, 539–542.Google ScholarPubMed
Ishidoh, K, Kominami, E, Suzuki, K & Katunuma, N (1989) Gene structure and 5′-upstream sequence of rat cathepsin L. FEBS Letters 259, 71–74.CrossRefGoogle Scholar
Jousse, C, Bruhat, A, Harding, HP, Ferrara, M, Ron, D & Fafournoux, P (1999) Amino acid limitation regulates CHOP expression through a specific pathway independent of the unfolded protein response. FEBS Letters 448, 211–216.CrossRefGoogle ScholarPubMed
Kaestner, KH, Christy, RJ & Lane, MD (1990) Mouse insulin-responsive glucose transporter gene. Characterization of the gene and trans-activation by the CCAAT/enhancer binding protein. Proceedings of the National Academy of Sciences USA 87, 251–255.CrossRefGoogle ScholarPubMed
Kennedy, AR (1995) The evidence for soybean products as cancer-preventive agents. Journal of Nutrition 125, 7335–7439.Google ScholarPubMed
Kerr, BJ & Easter, RA (1995) Effect of feeding reduced protein, amino acid-supplemented diets on nitrogen and energy balance in growing pigs. Journal of Animal Science 73, 3000–3008.CrossRefGoogle Scholar
Larbaud, D, Debras, E, Taillandier, D, Samuels, SE, Temparis, S, Champredon, C, Grizard, J & Attaix, D (1996) Euglycemic hyperinsulinemia and hyperaminoacidemia decrease skeletal muscle ubiquitin mRNA in goats. American Journal of Physiology 271, E505–E512.Google ScholarPubMed
Leonardi, A, Turk, B & Turk, V (1996) Inhibition of bovine cathepsins L and S by stefins and cystatins. Biological Chemistry Hoppe-Seyler 377, 319–321.Google Scholar
Liener, IE (1994) Implications of antinutritional components in soybean foods. Critical Reviews in Food Science and Nutrition 34, 31–67.CrossRefGoogle ScholarPubMed
Liener, IE (1995) Possible adverse effects of soybean anticarcinogens. Journal of Nutrition 125, 7449–7509.Google ScholarPubMed
Löhrke, B, Shahi, SK, Krüger, B, Schmidt, P, Renne, U & Dietl, G (2000) Thiazolidinedione-induced activation of the transcription factor peroxisome proliferator-activated receptor γ in cells adjacent to the murine skeletal muscle: implications for fibroblast functions. Pflügers Archiv-European Journal of Physiology 439, 288–296.CrossRefGoogle Scholar
Löhrke, B, Krüger, B & Viergutz, T (1993) The glycosylation as source of the variability in prolactin patterns of individual human amniotic fluids. Biological Chemistry Hoppe-Seyler 374, 271–279.CrossRefGoogle ScholarPubMed
Löhrke, B, Wegner, J, Viergutz, T, Dietl, G & Ender, K (1995) Flow cytometric analysis of oxidative and proteolytical activities in tissue – associated phagocytes from normal and hypertrophic muscles. Analytical Cellular Pathology 9, 281–293.Google ScholarPubMed
Löhrke, B, Viergutz, T, Shahi, SK, Pöhland, R, Wollenhaupt, K, Goldammer, T, Walzel, H & Kanitz, W (1998) Detection and functional characterisation of the transcription factor peroxisome proliferator-activated receptor in lutein cells. Journal of Endocrinology 159, 429–439.CrossRefGoogle ScholarPubMed
Mackenzie, BM, Ahmed, A & Rennie, MJ (1993) Muscle amino acid metabolism and transport Mammalian Amino Acid Transport: Mechanisms and Control pp.195–232 [MS, KilbergandD, Haussinger, editors]. New York, NY: Plenum.Google Scholar
Mansoor, O, Beaufrere, B, Boirie, Y, Ralliere, C, Taillandier, D, Aurousseau, E, Schoeffler, P, Arnal, M & Attaix, D (1996) Increased mRNA levels for components of the lysosomal, Ca2+-activated and ATP-ubiquitin-dependent proteolytic pathways in skeletal muscle from head trauma patients. Proceedings of the National Academy of Sciences USA 93, 2714–2718.CrossRefGoogle ScholarPubMed
Mortimore, GE & Pösö, AR (1987) Intracellular protein catabolism and its control during nutrient deprivation and supply. Annual Review of Nutrition 7, 539–564.CrossRefGoogle ScholarPubMed
Moundras, C, Remesy, C, Levrat, MA & Demigne, C (1995) Methionine deficiency in rats fed soy protein induces hypercholesterolemia and potentiates lipoprotein susceptibility to peroxidation. Metabolism 44, 1146–1152.CrossRefGoogle ScholarPubMed
Murakami, Y, Matsufuji, S, Kameji, T, Hayashi, S, Igarashi, K, Tamura, T, Tanaka, K & Ichihara, A (1992) Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature 360, 597–599.CrossRefGoogle Scholar
Nakai, I, Deshmukh, AR, Liener, IE & Sutherland, DE (1992) Effect of soybean flour on exocrine function in rat pancreas transplant with bladder drainage. Pancreas 7, 334–338.CrossRefGoogle ScholarPubMed
Patti, ME, Brambilla, E, Luzi, L, Landaker, EJ & Kahn, CR (1998) Bidirectional modulation of insulin action by amino acids. Journal of Clinical Investigation 101, 1519–1529.CrossRefGoogle ScholarPubMed
Reynisdottir, S, Wahrenberg, H, Bylin, G & Arner, P (1993) Effect of glucocorticoid treatment on β-adrenoceptor subtype function in adipocytes from patients with asthma. Clinical Science 85, 237–244.CrossRefGoogle ScholarPubMed
Rosser, BG, Powers, SP & Gores, GJ (1993) Calpain activity increases in hepatocytes following addition of ATP. Demonstration by a novel fluorescent approach. Journal of Biological Chemistry 268, 23593–23600.CrossRefGoogle ScholarPubMed
Salter, DN, Montgomery, AI, Hudson, A, Quelch, DB & Elliott, RJ (1990) Lysine requirements and whole-body protein turnover in growing pigs. British Journal of Nutrition 63, 503–513.CrossRefGoogle ScholarPubMed
Smith, K, Reynolds, N, Downie, S, Patel, A & Rennie, MJ (1998) Effects of flooding amino acids on incorporation of labeled amino acids into human muscle protein. American Journal of Physiology 275, E73–E78.Google ScholarPubMed
Schmitz, M, Hagemeister, H & Erbersdobler, HF (1991) Homoarginine labelling is suitable for determination of protein absorption in minipigs. Journal of Nutrition 121, 1575–1580.CrossRefGoogle Scholar
Schneible, PA, Airhart, J & Low, RB (1981) Differential compartmentation of leucine for oxidation and for protein synthesis in cultured skeletal muscle. Journal of Biological Chemistry 156, 4888–4894.CrossRefGoogle Scholar
Seve, B & Ponter, AA (1997) Nutrient-hormone signals regulating muscle protein turnover in pigs. Proceedings of the Nutrition Society 56, 565–580.CrossRefGoogle ScholarPubMed
Suemaru, S, Hashimoto, K, Hattori, T, Inoue, H, Kageyama, J & Ota, Z (1986) Starvation-induced changes in rat brain corticotropin-releasing factor (CRF) and pituitary-adrenocortical response. Life Science 39, 1161–1166.CrossRefGoogle ScholarPubMed
Tsakiridis, T, McDowell, HE, Walker, T, Downes, CP, Hundal, HS, Vranic, M & Klip, A (1995) Multiple roles of phosphatidylinositol 3-kinase in regulation of glucose transport, amino acid transport, and glucose transporters in L6 skeletal muscle cells. Endocrinology 136, 4315–4322.CrossRefGoogle ScholarPubMed
Tsujinaka, T, Kishibuchi, M, Yano, M, Morimoto, T, Ebisui, C, Fujita, J, Ogawa, A, Shiozaki, H, Kominami, E & Monden, M (1997) Involvement of interleukin-6 in activation of lysosomal cathepsins and atrophy of muscle fibers induced by intramuscular injection of turpentine oil in mice. Journal of Biochemistry (Tokyo) 122, 595–600.CrossRefGoogle ScholarPubMed
Towatari, T, Nikawa, T, Murata, M, Yokoo, C, Temai, M, Hanada, K & Katunuma, N (1991) Novel epoxysuccinyl peptides. A selective inhibitor of cathepsin B in vivo. FEBS Letters 280, 311–315.CrossRefGoogle ScholarPubMed
Woodward, CJH, Hervey, GR, Oakey, RE & Whitaker, EM (1991) The effect of fasting on plasma corticosterone kinetics in rats British Journal of Nutrition 66, 117–127.CrossRefGoogle ScholarPubMed
Young, VR, El-Khoury, AE, Raguso, CA, Forslund, AH & Hambraeus, L (2000) Rates of urea production and hydrolysis and leucine oxidation change linearly over widely varying protein intakes in healthy adults. Journal of Nutrition 130, 761-766.CrossRefGoogle ScholarPubMed