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The isotopic nitrogen turnover rate as a proxy to evaluate in the long-term the protein turnover in growing ruminants

Published online by Cambridge University Press:  20 March 2020

Gonzalo Cantalapiedra-Hijar Open the ORCID record for Gonzalo Cantalapiedra-Hijar [Opens in a new window] ,
Hélène Fouillet Open the ORCID record for Hélène Fouillet [Opens in a new window] ,
Céline Chantelauze ,
Nadezda Khodorova ,
Lahlou Bahloul  and
Isabelle Ortigues-Marty Open the ORCID record for Isabelle Ortigues-Marty [Opens in a new window]
Gonzalo Cantalapiedra-Hijar*
Affiliation:
INRAE, Université Clermont Auvergne, Vetagro Sup, UMRH, F-63122, Saint-Genès-Champanelle, France
Hélène Fouillet
Affiliation:
Université Paris-Saclay, AgroParisTech, INRAE, UMR PNCA, F-75005, Paris, France
Céline Chantelauze
Affiliation:
INRAE, Université Clermont Auvergne, Vetagro Sup, UMRH, F-63122, Saint-Genès-Champanelle, France
Nadezda Khodorova
Affiliation:
Université Paris-Saclay, AgroParisTech, INRAE, UMR PNCA, F-75005, Paris, France
Lahlou Bahloul
Affiliation:
Adisseo France S.A.S., Antony, France
Isabelle Ortigues-Marty
Affiliation:
INRAE, Université Clermont Auvergne, Vetagro Sup, UMRH, F-63122, Saint-Genès-Champanelle, France
*
Author for correspondence: Gonzalo Cantalapiedra-Hijar, E-mail: gonzalo.cantalapiedra@inrae.fr
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Abstract

Protein turnover is an energy-consuming process that is essential for ensuring the maintenance of living organisms. Gold standard methods for whole-body protein turnover (WBPT) measurement have inherent drawbacks precluding their generalization for large farm animals and use during long periods. Here, we proposed a non-invasive proxy for the WBPT over a long period of time and in a large number of beef cattle. The proxy is based on the rate at which urine-N and plasma proteins are progressively depleted in terms of 15N after a slight decrease in the isotopic N composition of the diet (i.e. diet switch). We aimed to test the ability of this proxy to adequately discriminate the WBPT of 36 growing-fattening young bulls assigned to different dietary treatments known to impact the WBPT rate, with different protein contents (normal v. high) and amino acid profiles (balanced v. unbalanced in methionine). The 15N depletion rate found in plasma proteins represented their fractional synthesis rate, whereas the slow depletion rate found in urine was interpreted as a proxy of the WBPT. The proxy tested in urine suggested different WBPT values between the normal- and high-protein diets but not between the balanced and unbalanced methionine diets. In contrast, the proxy tested in plasma indicated that both dietary conditions affected the fractional synthesis rate of plasma proteins. We considered that the rate at which urine is progressively 15N-depleted following an isotopic diet switch could be proposed as a non-invasive proxy of the WBPT rate in large farm animals.

Keywords

15Nbeef cattleisotopeprotein turnoverruminant
Type
Modelling Animal Systems Research Paper
Information
The Journal of Agricultural Science , Volume 157 , Issue 9-10 , December 2019 , pp. 701 - 710
Copyright
Copyright © Cambridge University Press 2020

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References

Abimorad, EG, Ducatti, C, Castellani, D, Jomori, RK, Portella, MC and Carneiro, DJ (2014) The use of stable isotopes to investigate the effects of supplemental lysine and methionine on protein turnover and amino acid utilization in pacu, Piaractus mesopotamicus, juveniles. Aquaculture 433, 119–124.CrossRefGoogle Scholar
Arneson, LS, MacAvoy, S and Basset, E (2006) Metabolic protein replacement drives tissue turnover in adult mice. Canadian Journal of Zoology 84, 992–1002.CrossRefGoogle Scholar
Bahar, B, Harrison, SM, Moloney, AP, Monahan, FJ and Schmidt, O (2014) Isotopic turnover of carbon and nitrogen in bovine blood fractions and inner organs. Rapid Communications in Mass Spectrometry 28, 1011–1018.CrossRefGoogle ScholarPubMed
Braun, A, Auerswald, K, Vikari, A and Schnyder, H (2013) Dietary protein content affects isotopic carbon and nitrogen turnover. Rapid Communications in Mass Spectrometry 27, 2676–2684.CrossRefGoogle ScholarPubMed
Cantalapiedra-Hijar, G, Ortigues-Marty, I, Sepchat, B, Agabriel, J, Huneau, JF and Fouillet, H (2015) Diet–animal fractionation of nitrogen stable isotopes reflects the efficiency of nitrogen assimilation in ruminants. British Journal of Nutrition 113, 1158–1169.CrossRefGoogle ScholarPubMed
Cantalapiedra-Hijar, G, Bahloul, L, Chantelauze, C, Largeau, V, Khodorova, N, Fouillet, H and Ortigues-Marty, I (2018) Improved cattle performance by methionine-balanced diets does not results from decreased protein degradation. Proceedings of the European Association for Animal Production. 476 (Abstract).Google Scholar
Carleton, SA and Martinez del Rio, C (2005) The effect of cold-induced increased metabolic rate on the rate of 13C and 15N incorporation in house sparrows (Passer domesticus). Oecologia 144, 226–232.CrossRefGoogle Scholar
Carleton, SA, Kelly, L, Anderson-Sprecher, R and Martinez del Rio, C (2008) Should we use one-, or multi-compartment models to describe 13C incorporation into animal tissues? Rapid Communications in Mass Spectrometry 22, 3008–3014.CrossRefGoogle ScholarPubMed
Carter, WA, Bauchinger, U and McWilliams, SR (2019) The Importance of Isotopic turnover for understanding key aspects of animal ecology and nutrition. Diversity 11, 84.CrossRefGoogle Scholar
Castro Bulle, FCP, Paulino, PV, Sanches, AC and Sainz, RD (2007) Growth, carcass quality, and protein and energy metabolism in beef cattle with different growth potentials and residual feed intakes. Journal of Animal Science 85, 928–936.CrossRefGoogle ScholarPubMed
Caton, JS, Bauer, ML and Hidari, H (2000) Metabolic components of energy expenditure in growing beef cattle-review. Asian-Australasian Journal of Animal Sciences 13, 702–710.CrossRefGoogle Scholar
Cerling, TE, Ayliffe, LK, Dearing, MD, Ehleringer, JR, Passey, BH, Podlesak, DW, Torregrossa, AM and West, AG (2007) Determining biological tissue turnover using stable isotopes: the reaction progress variable. Oecologia 151, 175–189.CrossRefGoogle ScholarPubMed
Connell, A, Calder, AG, Anderson, SE and Lobley, GE (1997) Hepatic protein synthesis in the sheep: effect of intake as by use of stable-isotope-labelled glycine, leucine and phenylalanine. British Journal of Nutrition 77, 255–271.CrossRefGoogle ScholarPubMed
Davis, SR, Barry, TN and Hughson, GA (1981) Protein synthesis in tissues of growing lambs. British Journal of Nutrition 46, 409–419.CrossRefGoogle ScholarPubMed
Fry, B and Arnold, C (1982) Rapid 13 C/12 C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54, 200–204.CrossRefGoogle Scholar
Geay, Y and Robelin, J (1979) Variation of meat production capacity in cattle due to genotype and level of feeding: genotype-nutrition interaction. Livestock Production Science 6, 263–276.CrossRefGoogle Scholar
Harris, CI and Milne, G (1981) The urinary excretion of N-methyl histidine by cattle: validation as an index of muscle protein breakdown. British Journal of Nutrition 45, 411–422.CrossRefGoogle Scholar
Harrison, SM, Schmidt, O, Moloney, AP, Kelly, SD, Rossmann, A, Schellenberg, A, Camin, F, Perini, M, Hoogewerff, J and Monahan, FJ (2011) Tissue turnover in ovine muscles and lipids as recorded by multiple (H, C, O, S) stable isotope ratios. Food Chemistry 124, 291–297.CrossRefGoogle Scholar
INRA (2018) INRA Feeding System for Ruminants. Wageningen, The Netherlands: Wageningen Academic Publishers.Google Scholar
Liu, SM, Lobley, GE, MacLeod, NA, Kyle, DJ, Chen, XB and Ørskov, ER (1995) Effects of long-term protein excess or deficiency on whole-body protein turnover in sheep nourished by intragastric infusion of nutrients. British Journal of Nutrition 73, 829–839.CrossRefGoogle ScholarPubMed
Lobley, GE (2003) Protein turnover – what does it mean for animal production? Canadian Journal of Animal Science 83, 327–340.CrossRefGoogle Scholar
Lobley, GE, Milne, V, Lovie, JM, Reeds, PJ and Pennie, K (1980) Whole body and tissue protein synthesis in cattle. British Journal of Nutrition 43, 491–502.CrossRefGoogle ScholarPubMed
MacAvoy, SE, Macko, SA and Arneson, LS (2005) Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Canadian Journal of Zoology 83, 631–641.CrossRefGoogle Scholar
Martinez del Rio, CMD and Anderson-Sprecher, R (2008) Beyond the reaction progress variable: the meaning and significance of isotopic incorporation data. Oecologia 156, 765–772.CrossRefGoogle ScholarPubMed
Martinez del Rio, CMD and Carleton, SA (2012) How fast and how faithful: the dynamics of isotopic incorporation into animal tissues. Journal of Mammalogy 93, 353–359.CrossRefGoogle Scholar
Mohan, JA, Smith, SD, Connelly, TL, Attwood, ET, McClelland, JW, Herzka, SZ and Walther, BD (2016) Tissue-specific isotope turnover and discrimination factors are affected by diet quality and lipid content in an omnivorous consumer. Journal of Experimental Marine Biology and Ecology 479, 35–45.CrossRefGoogle Scholar
Nishizawa, N, Toyoda, Y, Noguchi, T, Hareyama, S, Itabashi, H and Funabiki, R (1979) N τ-Methylhistidine content of organs and tissues of cattle and an attempt to estimate fractional catabolic and synthetic rates of myofibrillar proteins of skeletal muscle during growth by measuring urinary output of N τ-methylhistidine. British Journal of Nutrition 42, 247–252.CrossRefGoogle Scholar
Pinheiro, JC and Bates, DM (2000) Linear mixed-effects models. In Chambers, J, Eddy Hardle, W, Sheather, S and Tierney, L (eds), Mixed-effects Models in S and S-Plus. New York, USA: Springer, pp. 3–56.CrossRefGoogle Scholar
Poupin, N, Huneau, JF, Mariotti, F, Tomé, D, Bos, C and Fouillet, H (2012) Isotopic and modeling investigation of long-term protein turnover in rat tissues. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 304, R218–R231.CrossRefGoogle ScholarPubMed
Raggio, G, Lobley, GE, Berthiaume, R, Pellerin, D, Allard, G, Dubreuil, P and Lapierre, H et al. (2007) Effect of protein supply on hepatic synthesis of plasma and constitutive proteins in lactating dairy cows. Journal of Dairy Science 90, 352–359.CrossRefGoogle ScholarPubMed
Steinbock, HL and Tarver, H (1954) Plasma protein. 5. The effect of the protein content of the diet on turnover. Journal of Biological Chemistry 209, 127–132.Google Scholar
Tieszen, LL, Boutton, TW, Tesdahl, KG and Slade, NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57, 32–37.CrossRefGoogle Scholar
Tsahar, E, Wolf, N, Izhaki, I, Arad, Z and Martinez del Rio, C (2008) Dietary protein influences the rate of 15N incorporation in blood cells and plasma of yellow-vented bulbuls (Pycnonotus xanthopygos). The Journal of Experimental Biology 211, 459–465.CrossRefGoogle Scholar
Wallace, RJ and McPherson, CA (1987) Factors affecting the rate of breakdown of bacterial protein in rumen fluid. British Journal of Nutrition 58, 313–323.CrossRefGoogle ScholarPubMed
Waterlow, JC (1984) Protein turnover with special reference to man. Experimental Physiology 69, 409–438.CrossRefGoogle Scholar
Waterlow, JC (2006) Protein turnover. CAB International, Nosworthy Wag Wallingford, Oxfordshire OX10 8DE, UK.Google Scholar
Wessels, RH, Titgemeyer, EC and St Jean, G (1997) Effect of amino acid supplementation on whole-body protein turnover in Holstein steers. Journal of Animal Science 75, 3066–3073.CrossRefGoogle ScholarPubMed
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