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High-protein diet during gestation and lactation affects mammary gland mRNA abundance, milk composition and pre-weaning litter growth in mice

Published online by Cambridge University Press:  08 September 2010

M. Kucia
Affiliation:
Research Unit Nutritional Physiology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
M. Langhammer
Affiliation:
Research Unit Genetics and Biometry, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
S. Görs
Affiliation:
Research Unit Nutritional Physiology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
E. Albrecht
Affiliation:
Research Unit Muscle Biology and Growth, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
H. M. Hammon
Affiliation:
Research Unit Nutritional Physiology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
G. Nürnberg
Affiliation:
Research Unit Genetics and Biometry, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
C. C. Metges*
Affiliation:
Research Unit Nutritional Physiology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
*
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Abstract

We evaluated the effect of a high-protein diet (HP) on pregnancy, lactational and rearing success in mice. At the time of mating, females were randomly assigned to isoenergetic diets with HP (40% w/w) or control protein levels (C; 20%). After parturition, half of the dams were fed the other diet throughout lactation resulting in four dietary groups: CC (C diet during gestation and lactation), CHP (C diet during gestation and HP diet during lactation), HPC (HP diet during gestation and C diet during lactation) and HPHP (HP diet during gestation and lactation). Maternal and offspring body mass was monitored. Measurements of maternal mammary gland (MG), kidney and abdominal fat pad masses, MG histology and MG mRNA abundance, as well as milk composition were taken at selected time points. HP diet decreased abdominal fat and increased kidney mass of lactating dams. Litter mass at birth was lower in HP than in C dams (14.8 v. 16.8 g). Dams fed an HP diet during lactation showed 5% less food intake (10.4 v. 10.9 g/day) and lower body and MG mass. On day 14 of lactation, the proportion of MG parenchyma was lower in dams fed an HP diet during gestation as compared to dams fed a C diet (64.8% v. 75.8%). Abundance of MG α-lactalbumin, β-casein, whey acidic protein, xanthine oxidoreductase mRNA at mid-lactation was decreased in all groups receiving an HP diet either during gestation and/or lactation. Milk lactose content was lower in dams fed an HP diet during lactation compared to dams fed a C diet (1.6% v. 2.0%). On days 14, 18 and 21 of lactation total litter mass was lower in litters of dams fed an HP diet during lactation, and the pups’ relative kidney mass was greater than in litters suckled by dams receiving a C diet. These findings indicate that excess protein intake in reproducing mice has adverse effects on offspring early in their postnatal growth as a consequence of impaired lactational function.

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Full Paper
Copyright
Copyright © The Animal Consortium 2010

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References

Anderson, SM, Rudolph, MC, McManaman, JL, Neville, MC 2007. Secretory activation in the mammary gland: it’s not just about milk protein synthesis! Breast Cancer Research 9. Retrieved from http://breast-cancer-research.com/content/9/1/204CrossRefGoogle Scholar
Aoki, N, Yamaguchi, Y, Ohira, S, Matsuda, T 1999. High fat feeding of lactating mice causing a drastic reduction in fat and energy content in milk without affecting the apparent growth of their pups and the production of a major milk fat globule membrane components MFG-E8 and butyrophilin. Bioscience Biotechnology and Biochemistry 63, 17491755.CrossRefGoogle Scholar
Boston, WS, Bleck, GT, Conroy, JC, Wheeler, MB, Miller, DJ 2001. Short communication: effects of increased expression of α-lactalbumin in transgenic mice on milk yield and pup growth. Journal of Dairy Science 84, 620622.CrossRefGoogle ScholarPubMed
Daenzer, M, Ortmann, S, Klaus, S, Metges, CC 2002. Prenatal high protein exposure decreases energy expenditure and increases adiposity in young rats. Journal of Nutrition 132, 142144.CrossRefGoogle ScholarPubMed
Del Prado, M, Delgado, G, Villalpando, S 1997. Maternal lipid intake during pregnancy and lactation alters milk composition and production and litter growth in rats. Journal of Nutrition 127, 458462.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, 591603.CrossRefGoogle ScholarPubMed
Desai, M, Byrne, CD, Meeran, K, Martinez, ND, Bloom, SR, Hales, CN 1997. Regulation of hepatic enzymes and insulin levels in offspring of rat dams fed a reduced-protein diet. American Journal of Physiology 273, G899G904.Google ScholarPubMed
Fagundes, AT, Moura, EG, Passos, MC, Oliviera, E, Toste, FP, Bonomo, IT, Trevenzoli, IH, Garcia, RM, Lisboa, PC 2007. Maternal low-protein diet during lactation programmes body composition and glucose homeostasis in the adult rat offspring. British Journal of Nutrition 98, 922928.CrossRefGoogle ScholarPubMed
Farnsworth, E, Luscombe, ND, Noakes, M, Wittert, G, Argyiou, E, Clifton, PM 2003. Effect of a high-protein, energy-restricted diet on body composition, glycemic control, and lipid concentrations in overweight and obese hyperinsulinemic men and women. The American Journal of Clinical Nutrition 78, 3139.CrossRefGoogle ScholarPubMed
Flint, DJ, Travers, MT, Barber, MC, Binart, N, Kelly, PA 2005. Diet-induced obesity impairs mammary development and lactogenesis in murine mammary gland. American Journal of Physiology. Endocrinology and Metabolism 288, E1179E1187.CrossRefGoogle ScholarPubMed
Gardner, DK, Stilley, KS, Lane, M 2004. High protein diet inhibits inner cell mass formation and increases apoptosis in mouse blastocysts developed in vivo by increasing the levels of ammonium in the reproductive tract. Reproduction, Fertility and Development 16, 190, Abstract no. 136.CrossRefGoogle Scholar
Godfrey, K, Robinson, S, Barker, DJP, Osmond, C, Cox, V 1996. Maternal nutrition in early and late pregnancy in relation to placental and fetal growth. British Medical Journal 312, 410414.CrossRefGoogle ScholarPubMed
Görs, S, Kucia, M, Langhammer, M, Junghans, P, Metges, CC 2009. Milk composition in mice – methodological aspects and effects of mouse strain and lactation day. Journal of Dairy Science 92, 632637.CrossRefGoogle ScholarPubMed
Halton, TL, Hu, FB 2004. The effects of high protein diets on thermogenesis, satiety and weight loss: a critical review. Journal of the American College of Nutrition 23, 373385.CrossRefGoogle ScholarPubMed
Hammon, HM, Sauter, SN, Reist, M, Zbinden, Y, Philipona, C, Morel, C, Blum, JW 2003. Dexamethasone and colostrum feeding affect hepatic gluconeogenic enzymes differently in neonatal calves. Journal of Animal Science 81, 30953106.CrossRefGoogle ScholarPubMed
Hammond, KA, Janes, DN 1998. The effects of increased protein intake on kidney size and function. Journal of Experimental Biology 201, 20812090.CrossRefGoogle ScholarPubMed
Jean, C, Rome, S, Mathé, V, Huneau, J-F, Aattouri, N, Fromentin, G, Achagiotis, CL, Tomé, D 2001. Metabolic evidence for adaptation to a high protein diet in rats. Journal of Nutrition 131, 9198.CrossRefGoogle ScholarPubMed
Johnston, CS, Day, CS, Swan, PD 2002. Postprandial thermogenesis is increased 100% on a high-protein, low-fat diet versus a high-carbohydrate, low-fat diet in healthy, young women. Journal of the American College of Nutrition 21, 5561.CrossRefGoogle ScholarPubMed
King, RH, Toner, MS, Dove, H, Atwood, CS, Brown, WG 1993. The response of first-litter sows to dietary protein level during lactation. Journal of Animal Science 71, 24572463.CrossRefGoogle ScholarPubMed
Kuhla, B, Kucia, M, Görs, S, Albrecht, D, Langhammer, M, Kuhla, S, Metges, CC 2010. Effect of a high-protein diet on food intake and liver metabolism during pregnancy, lactation and after weaning in mice. Proteomics 10, 25732588.CrossRefGoogle ScholarPubMed
Kumar, S, Clarke, AR, Hooper, ML, Horne, DS, Law, AJ, Leaver, J, Springbett, A, Stevenson, E, Simons, JP 1994. Milk composition and lactation of β-casein-deficient mice. Proceedings of the National Academy of Sciences of the United States of America 91, 61386142.CrossRefGoogle ScholarPubMed
Lacroix, M, Gaudichon, C, Martin, A, Morens, C, Mathé, V, Tomé, D, Huneau, J-F 2004. A long-term high-protein diet markedly reduces adipose tissue without major side effects in Wistar male rats. American Journal of Physiology. Regulatory, Integrative, and Comparative Physiology 287, R934R942.CrossRefGoogle ScholarPubMed
Langhammer, M, Derno, M, Dietrich, N, Renne, U, Nürnberg, G, Hennig, U, Metges, CC 2006. Fetal programming of offspring growth due to maternal high protein diet is genotype dependent in mice. Journal of Animal Science 84 (suppl. 1), 144 (abstract).Google Scholar
Layman, DK, Boileau, RA, Erickson, DJ, Painter, JE, Shiue, H, Sather, C, Christou, DD 2003. A reduced ratio of dietary carbohydrate to protein improves body composition and lipid blood profiles during weight loss in adult women. Journal of Nutrition 133, 411417.CrossRefGoogle ScholarPubMed
McManaman, JL, Palmer, CA, Wright, RM, Neville, MC 2002. Functional regulation of xanthine oxidoreductase expression and localization in the mouse mammary gland: evidence of a role in lipid secretion. Journal of Physiology 545, 567579.CrossRefGoogle ScholarPubMed
Metges, CC, Lang, IS, Goers, S, Junghans, P, Hennig, U, Stabenow, B, Schneider, F, Otten, W, Rehfeldt, C 2009. Inadequate protein levels during gestation in gilts affect gestation body mass and fatness as well as offspring birth weight and insulin sensitivity at 10 wk of age. Journal of Animal Science 87 (E-suppl. 2), 503504.Google Scholar
Mitchell, M, Schulz, SL, Armstrong, DT, Lane, M 2009. Metabolic and mitochondrial dysfunction in early mouse embryos following maternal dietary protein intervention. Biology of Reproduction 80, 622630.CrossRefGoogle ScholarPubMed
Murray, BM, Brown, GP, Schoenl, M 1998. Interaction of gender and dietary protein on renal growth and the renal growth hormone-insulin-like growth factor axis. Journal of Laboratory and Clinical Medicine 131, 360369.CrossRefGoogle ScholarPubMed
Ozanne, SE, Lewis, R, Jennings, BJ, Hales, CN 2004. Early programming of weight gain in mice prevents the induction of obesity by a highly palatable diet. Clinical Science (London) 106, 141145.CrossRefGoogle ScholarPubMed
Passos, MCF, Ramos, CF, Moura, EG 2000. Short and long-term effects of malnutrition in rats during lactation on the body weight of offspring. Nutrition Research 20, 16031612.CrossRefGoogle Scholar
Pfaffl, MW 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, 20022007.CrossRefGoogle ScholarPubMed
Pichon, L, Huneau, J-F, Fromentin, G, Tomé, D 2006. A high-protein, high-fat, carbohydrate free diet reduces energy intake, hepatic lipogenesis, and adiposity in rats. Journal of Nutrition 136, 12561260.CrossRefGoogle ScholarPubMed
Pine, P, Jessop, NS, Oldham, JD 1994. Maternal protein reserves and their influence on lactational performance in rats 3. The effects of dietary protein restriction and stage of lactation on milk composition. British Journal of Nutrition 72, 815830.CrossRefGoogle ScholarPubMed
Rasmussen, R 2001. Quantification on the LightCycler. In Rapid cycle real-time PCR, methods and applications (ed. S Meuer, C Wittwer and K Nakagawara), pp. 2134. Springer Press, Heidelberg, Germany.CrossRefGoogle Scholar
Rees, WD, Hay, SM, Antipatis, C 2006. The effect of dietary protein on the amino acid supply and threonine metabolism in the pregnant rat. Reproduction, Nutrition, Development 46, 227239.CrossRefGoogle ScholarPubMed
Robinson, GW, McKnight, RA, Smith, GH, Hennighausen, L 1995. Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development 121, 20792090.CrossRefGoogle ScholarPubMed
Rudolph, MC, Neville, MC, Anderson, SM 2007. Lipid synthesis in lactation: diet and the fatty acid switch. Journal of Mammary Gland Biology and Neoplasia 12, 269281.CrossRefGoogle ScholarPubMed
Schoknecht, PA, Pond, WG 1993. Short-term ingestion of a high protein diet increases liver and kidney mass and protein accretion but not cellularity in young pigs. Proceedings of the Society for Experimental Biology and Medicine 203, 251254.CrossRefGoogle Scholar
Schüler, L 1985. Der Mäuseauszuchtstamm Fzt: DU und seine Anwendung als Modell in der Tierzuchtforschung (Mouse strain Fzt: DU and its use as model in animal breeding research). Archives of Animal Breeding 28, 357363.Google Scholar
Stacey, A, Schnieke, A, Kerr, M, Scott, A, McKee, C, Cottingham, I, Binas, B, Wilde, C, Colman, A 1995. Lactation is disrupted by α-lactalbumin deficiency and can be restored by human α-lactalbumin gene replacement in mice. Proceedings of the National Academy of Sciences of the United States of America 92, 28352839.CrossRefGoogle ScholarPubMed
Stinnakre, MG, Villotte, JL, Soulier, S, Mercier, JC 1994. Creation and phenotypic analysis of a-lactalbumin-deficient mice. Proceedings of the National Academy of Sciences of the United States of America 91, 65446548.CrossRefGoogle ScholarPubMed
Thone-Reineke, C, Kalk, P, Dorn, M, Klaus, S, Simon, K, Pfab, T, Godes, M, Persson, P, Unger, T, Hocher, B 2006. High-protein nutrition during pregnancy and lactation programs blood pressure, food efficiency, and body weight of the offspring in a sex-dependent manner. American Journal of Physiology. Regulatory, Integrative, and Comparative Physiology 291, R1025R1030.CrossRefGoogle Scholar
Tilton, SL, Muller, PS, Lewis, AJ, Reese, DE, Ermer, PM 1999. Addition of fat to the diets of lactating sows: I. Effects on milk production and composition and carcass compostion of the litter at weaning. Journal of Animal Science 77, 24912500.CrossRefGoogle Scholar
Triplett, AA, Sakamoto, K, Matulka, LA, Shen, L, Smith, GH, Wagner, K-U 2005. Expression of the whey acidic protein (Wap) is necessary for adequate nourishment of the offspring but not functional differentiation of the mammary epithelial cells. Genesis 43, 111.CrossRefGoogle Scholar
Vorbach, C, Scriven, A, Capeccchi, C 2002. The housekeeping gene xanthine oxidoreductase is necessary for milk fat droplet enveloping and secretion: gene sharing in the lactating mammary gland. Genes & Development 16, 32233235.CrossRefGoogle ScholarPubMed
Zhang, J, Wang, C, Terroni, PL, Cagampang, FRA, Hanson, M, Byrne, CD 2005. High-unsaturated-fat, high-protein, and low-carbohydrate diet during pregnancy and lactation modulates hepatic lipid metabolism in female adult offspring. American Journal of Physiology. Regulatory, Integrative, and Comparative Physiology 288, R112R118.CrossRefGoogle ScholarPubMed