Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-19T20:00:21.564Z Has data issue: false hasContentIssue false
  • English
  • Français

Foetal life protein restriction in male mink (Neovison vison) kits lowers post-weaning protein oxidation and the relative abundance of hepatic fructose-1,6-bisphosphatase mRNA

Published online by Cambridge University Press:  19 August 2011

C. F. Matthiesen ,
D. Blache ,
P. D. Thomsen  and
A.-H. Tauson
C. F. Matthiesen
Affiliation:
Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
D. Blache
Affiliation:
Faculty of Natural and Agricultural Sciences, School of Animal Biology, University of Western Australia, 35 Stirling Highway, Crawley WA 6009, Perth, Australia
P. D. Thomsen
Affiliation:
Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
A.-H. Tauson*
Affiliation:
Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
*
†E-mail: aht@life.ku.dk
Get access

Abstract

Foetal life malnutrition has been studied intensively in a number of animal models. Results show that especially foetal life protein malnutrition can lead to metabolic changes later in life. This might be of particular importance for strict carnivores, for example, cat and mink (Neovison vison) because of their higher protein requirement than in other domestic mammals. This study aimed to investigate the effects of low protein provision during foetal life to male mink kits on their protein metabolism during the early post-weaning period of rapid growth and to investigate whether foetal life protein deficiency affects the response to adequate or deficient protein provision post weaning. Further, we intended to study whether the changes in the gene expression of key enzymes in foetal hepatic tissue caused by maternal protein deficiency were manifested post-weaning. A total of 32 male mink kits born to mothers fed either a low-protein diet (LP), that is, 14% of metabolizable energy (ME) from protein (foetal low – FL), n = 16, or an adequate-protein (AP) diet, that is, 29% of ME from protein (foetal adequate – FA), n = 16) in the last 16.3 ± 1.8 days of pregnancy were used. The FL offspring had lower birth weight and lower relative abundance of fructose-1,6-bisphosphatase (Fru-1,6-P2ase) and pyruvate kinase mRNA in foetal hepatic tissue than FA kits. The mothers were fed a diet containing adequate protein until weaning. At weaning (7 weeks of age), half of the kits from each foetal treatment group were fed an AP diet (32% of ME from protein; n = 8 FA and 8 FL) and the other half were fed a LP diet (18% of ME from protein; n = 8 FA and 8 FL) until 9.5 weeks of age, yielding four treatment groups (i.e. FA-AP, FA-LP, FL-AP and FL-LP). Low protein provision in foetal life lowered the protein oxidation post-weaning compared with the controls (P = 0.006), indicating metabolic flexibility and a better ability to conserve protein. This could not, however, be supported by changes in liver mass because of foetal life experience. A lower relative abundance of Fru-1,6-P2ase mRNA was observed (P < 0.05), being lower in 9.5-week-old FL than in FA kits. It can be concluded that foetal life protein restriction leads to changes in post-weaning protein metabolism through lower protein oxidation of male mink kits.

Keywords

protein oxidationprotein restrictionnitrogen metabolismmetabolic flexibilityenergy metabolism
Type
Full Paper
Information
animal , Volume 6 , Issue 1 , January 2012 , pp. 50 - 60
Copyright
Copyright © The Animal Consortium 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abraham, GE, Buster, JE, Teller, RC 1972. Radioimmunoassay of plasma cortisol. Analytical Letters 5, 757–765.CrossRefGoogle Scholar
Anonymous 1986. European Convention for Protection of Vertebrate Animals Used for Experimental and other Scientific Purposes. European Treaty Series no. 123. Council of Europe, Strasbourg, France.Google Scholar
Blache, D, Tellam, RL, Chagas, LM, Blackberry, MA, Vercoe, PE, Martin, GB 2000. Level of nutrition affects leptin concentrations in plasma and cerebrospinal fluid in sheep. Journal of Endocrinology 165, 625–637.CrossRefGoogle ScholarPubMed
Breier, BH, Gallaher, BW, Gluckman, PD 1991. Radioimmunoassay for insulin-like growth factor-I: solutions to some potential problems and pitfalls. Journal of Endocrinology 128, 347–357.CrossRefGoogle ScholarPubMed
Brouwer, E 1965. Report of sub-committee on constants and factors. In 3rd Symposium on Energy Metabolism, European Association of Animal Production (ed. KL Blaxter), Publication no. 11, pp. 441–443. Academic Press, London, UK.Google Scholar
Burdge, GC, Slater-Jefferies, J, Torrens, C, Phillips, ES, Hanson, MA, Lillycrop, KA 2007. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. British Journal of Nutrition 97, 435–439.CrossRefGoogle ScholarPubMed
Chwalibog, A, Tauson, AH, Thorbek, G 2004. Energy metabolism and substrate oxidation in pigs during feeding, starvation and re-feeding. Journal of Animal Physiology and Animal Nutrition 88, 101–112.CrossRefGoogle ScholarPubMed
Chwalibog, A, Jakobsen, K, Henckel, S, Thorbek, G 1992. Estimation of quantitative oxidation and fat retention from carbohydrate, protein and fat in growing pigs. Journal of Animal Physiology and Animal Nutrition 68, 123–135.CrossRefGoogle Scholar
Dahri, S, Reusens, B, Remacle, C, Hoet, JJ 1995. Nutritional influences on pancreatic development and potential links with non-insulin-dependent diabetes. Proceedings of the Nutrition Society 54, 345–356.CrossRefGoogle ScholarPubMed
Desai, M, Crowther, NJ, Lucas, A, Hales, CN 1996. Organ-selective growth in the offspring of protein-restricted mothers. British Journal of Nutrition 76, 591–603.CrossRefGoogle ScholarPubMed
Desai, M, Byrne, CD, Zhang, J, Petry, CJ, Lucas, A, Hales, CN 1997. Programming of hepatic insulin-sensitive enzymes in offspring of rat dams fed a protein-restricted diet. American Journal of Physiology – Gastrointestinal and Liver Physiology 272, G1083–G1090.CrossRefGoogle ScholarPubMed
Drowning, JA, Joss, J, Connell, P, Scaramuzzi, RJ 1995. Ovulation rate and the concentrations of gonadotrophic and metabolic hormones in ewes fed lupin grain. Journal of Reproduction and Fertility 103, 137–145.CrossRefGoogle Scholar
European Community 1998. Commission Directive 98/64/EEC. Official Journal of the European Communities L 257, 14–28.Google Scholar
Fink, R, Thomsen, PD, Tauson, A-H 2007. Metabolic flexibility of lactating mink (Mustela vison) is not reflected at transcriptional level but by changes in functional liver mass. In Energy and protein metabolism and nutrition (ed. I Ortigues-Marty, N Miraux and W Brand-Williams), pp. 477–478. Wageningen Academic Publishers, Wageningen, The Netherlands.CrossRefGoogle Scholar
Fink, R, Tauson, A, Chwalibog, A, Hansen, NE, Kristensen, NB, Wamberg, S 2004. Effects of substitution of dietary protein with carbohydrate on lactation performance in the mink (Mustela vison). Journal of Animal and Feed Sciences 13, 647–664.CrossRefGoogle Scholar
Fowden, AL, Forhead, AJ 2004. Endocrine mechanisms of intrauterine programming. Reproduction 127, 515–526.CrossRefGoogle ScholarPubMed
Gosby, AK, Stanton, LML, Maloney, CA, Thompson, M, Briody, J, Baxter, RC, Bryson, JM, Denyer, GS, Caterson, ID 2008. Postnatal nutrition alters body composition in adult offspring exposed to maternal protein restriction. British Journal of Nutrition 101, 1878–1884.CrossRefGoogle ScholarPubMed
Green, AS, Ramsey, JJ, Villaverde, C, Asami, DK, Wei, A, Fascetti, AJ 2008. Cats are able to adapt protein oxidation to protein intake provided their requirement for dietary protein is met. Journal of Nutrition 138, 1053–1060.CrossRefGoogle ScholarPubMed
Guan, H, Arany, E, van Beek, JP, Chamson-Reig, A, Thyssen, S, Hill, DJ, Yang, K 2005. Adipose tissue gene expression profiling reveals distinct molecular pathways that define visceral adiposity in offspring of maternal protein-restricted rats. American Journal of Physiology – Endocrinology and Metabolism 288, E663–E673.CrossRefGoogle ScholarPubMed
Hales, CN, Barker, DJP 1992. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595–601.CrossRefGoogle ScholarPubMed
Hendriks, WH, Moughan, PJ, Tarttelin, MF 1997. Urinary excretion of endogenous nitrogen metabolites in adult domestic cats using a protein-free diet and the regression technique. Journal of Nutrition 127, 623–629.CrossRefGoogle ScholarPubMed
Husted, SM, Nielsen, MO, Tygesen, MP, Kiani, A, Blache, D, Ingvartsen, KL 2007. Programming of intermediate metabolism in young lambs affected by late gestational maternal undernourishment. American Journal of Physiology – Endocrinology and Metabolism 293, E548–E557.CrossRefGoogle ScholarPubMed
Kettelhut, IC, Foss, MC, Mighorini, RH 1980. Glucose homeostasis in carnivorous animal (cat) and rats fed a high protein diet. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 239, R437–R444.CrossRefGoogle Scholar
Kwong, WY, Miller, DJ, Wilkins, AP, Dear, MS, Wreight, JN, Osmond, C, Zhang, J, Fleming, TP 2007. Maternal low protein diet restricted to the preimplantation period induces a genderspecific change on hepatic gene expression in rat fetuses. Molecular Reproduction and Development 74, 48–56.CrossRefGoogle Scholar
Lillycrop, KA, Slater-Jefferies, JL, Hanson, MA, Godfrey, KM, Jackson, AA, Burdge, GC 2007. Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. British Journal of Nutrition 97, 1064–1073.CrossRefGoogle ScholarPubMed
Lingas, RI, Matthews, SG 2001. A short period of maternal nutrient restriction in late gestation modifies pituitary-adrenal function in adult guinea pig offspring. Neuro-endocrinology 73, 302–311.CrossRefGoogle Scholar
Littell, RC, Milliken, GA, Stroup, WW, Wolfinger, RD, Schabenberger, O 2006. SAS for mixed models, 2nd edition. SAS Institute Inc., Cary, NC, USA.Google Scholar
Matthiesen, CF, Blache, D, Thomsen, PD, Hansen, NE, Tauson, A-H 2010a. Effect of late gestation low protein supply to mink (Mustela vison) dams on reproductive performance and metabolism of dam and offspring. Archives of Animal Nutrition 64, 56–76.CrossRefGoogle ScholarPubMed
Matthiesen, CF, Blache, D, Thomsen, PD, Tauson, A-H 2010b. Feeding mink (Neovison vison) a protein-restricted diet during pregnancy induces higher birth weight and altered hepatic gene expression in the F2 offspring. British Journal of Nutrition 104, 544–553.CrossRefGoogle Scholar
Nes, N, Einarsson, EJ, Lohi, O 1987. Beautiful fur animals and their colour genetics. Scientifur, Hillerød, Denmark.Google Scholar
NRC 1982. Nutrient requirements of mink and foxes, 2nd edition. National Research Council, Washington, USA.Google Scholar
Ozanne, SE, Hales, CN 2002. Early programming of glucose-insulin metabolism. Trends in Endocrinology and Metabolism 13, 368–373.CrossRefGoogle ScholarPubMed
Pinheiro, AR, Salvucci, IDM, Aguila, MB, Mandarim-de-Lacerda, CA 2008. Protein restriction during gestation and/or lactation causes adverse transgenerational effects on biometry and glucose metabolism in F1 and F2 progenies of rats. Clinical Science 114, 381–392.CrossRefGoogle ScholarPubMed
Reusens, B, Remacle, C 2006. Programming of the endocrine pancreas by the early nutritional environment. The International Journal of Biochemistry & Cell Biology 38, 913–922.CrossRefGoogle ScholarPubMed
Rogers, QR, Morris, JG, Freedland, RA 1977. Lack of hepatic enzymatic adaption to low and high levels of dietary protein in the adult cat. Enzyme 22, 348–356.CrossRefGoogle ScholarPubMed
Russell, K, Murgatroyd, PR, Batt, RM 2002. Net protein oxidation is adapted to dietary protein intake in domestic cats (Felis silvestris catus). Journal of Nutrition 132, 456–460.CrossRefGoogle ScholarPubMed
Russell, K, Lobley, GE, Rawlings, J, Millward, J, Harper, EJ 2000. Urea kinetics of a carnivore (Felis silvestris catus). British Journal of Nutrition 84, 597–604.CrossRefGoogle ScholarPubMed
Seckl, JR 2004. Prenatal glucocorticoids and long-term programming. European Journal of Endocrinology 151, U49–U62.CrossRefGoogle ScholarPubMed
Silva, SVPS, Mercer, JR 1985. Effect of protein intake on amino acid catabolism and gluconeogenesis by isolated hepatocytes from the cat (Felis domestica). Comparative Biochemistry and Physiology Part B, Comparative Biochemistry 80, 603–607.CrossRefGoogle ScholarPubMed
Snoeck, A, Remacle, C, Reusens, B, Hoet, JJ 1990. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biology of the Neonate 57, 107–118.CrossRefGoogle ScholarPubMed
Tauson, A-H, Forsberg, M 2002. Body-weight changes are clearly reflected in plasma concentrations of leptin in female mink (Mustela vison). British Journal of Nutrition 87, 101–105.CrossRefGoogle ScholarPubMed
Tauson, A-H, Fink, R, Chwalibog, A 2001. Protein as glucose precursor in lactating mink (Mustela vison) estimated by decarboxylation of 1-13C-labelled leucine. In Proceedings of the 15th Symposium on Energy Metabolism in Animals (ed. A Chwalibog and K Jakobsen), pp. 261–264. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Tindal, JS, Knaggs, GS, Hart, IC, Blake, LA 1978. Release of growth hormone in lactating and non-lactating goats in relation to behaviour, stages of sleep, electroencephalograms, environmental stimuli and levels of prolactin, insulin, glucose and free fatty acids in the circulation. Journal of Endocrinology 76, 333–346.CrossRefGoogle ScholarPubMed
Waterlow, JC 1999. The mysteries of nitrogen balance. Nutrition Research Reviews 12, 25–54.CrossRefGoogle ScholarPubMed
Zambrano, E, Martinez-Samayoa, PM, Bautista, CJ, Deas, M, Guillen, L, Rodriguez-Gonzalez, GL, Guzman, C, Larrea, F, Nathanielsz, PW 2005. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. Journal of Physiology 566, 225–236.CrossRefGoogle ScholarPubMed