Cited by 189Animal Nutrition and PhysiologyDiet, Metabolism, and DiseaseMuscle metabolism and nutrition

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Metabolic Evidence for Adaptation to a High Protein Diet in Rats

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Jean, Clémentine, Rome, Sophie, Mathé, Véronique, Huneau, Jean-François, Aattouri, Najat, Fromentin, Gilles, Achagiotis, Christiane Larue, Tomé, Daniel·2001·The Journal of Nutrition

DOI 10.1093/jn/131.1.91

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Abstract

This study was designed to assess the effects of long-term adaptation to a high protein diet on energy intake, body weight gain, body composition and splanchnic metabolic indicators in rats. For this purpose, adult male Wistar rats were fed either a 50 g/100 g dry matter (DM) protein diet (P50 group) or a 14 g/100 g DM protein diet (P14 group) for 21 d. These two groups were compared with a P14 pair-fed (P14-pf) group that consumed the same daily energy as the P50 group. The energy intake of the P50 group was 16 +/- 1% less than that of the P14 group (P < 0.05), and the P50 group had significantly lower body weight. The P50 group had significantly less adipose tissue compared with both P14 and P14-pf rats. The activities of the brush border membrane enzymes, neutral aminopeptidase and gamma-glutamyl transferase, were significantly higher in the P50 group than in the P14 rats. Similarly, the activities of alanine aminotransferase, arginase and serine dehydratase were significantly higher in the liver of P50 rats compared with P14 rats. Both amino acid transporter system A and X(A,G-) activities, measured in freshly isolated hepatocytes, were significantly higher in the P50 group (8- and 1.5-fold, P < 0.05, respectively) compared with the P14 group. The 1.5-fold increase in the steady-state activity of X(A,G-) was accompanied by a doubling of EAAT2 mRNA, involved in the system X(A,G-). This study provides confirmation that specific biochemical and molecular adaptive processes of the splanchnic area are involved in the response to variations in the protein content of the diet.

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Background
Increasing the Protein Content in a Carbohydrate-Free Diet Enhances Fat Loss during 35% but Not 75% Energy Restriction in Rats
Fromentin, G., Tomé, D., Bensaı̈d, A., Makarios-Lahham, L., Even, P. C., & Marsset‐Baglieri, A. (2004) · Journal of Nutrition · doi:10.1093/jn/134.10.2646 · Cited by 44
“This hypothesis is reinforced by numerous previous observations of carbohydratecontaining diets, showing that rats fed high-protein diets, or spontaneously selecting a high-protein intake during dietary self-selection, were leaner than rats fed or selecting lower levels of protein, a phenomenon observed whatever the f…”
ResultSelf-citation
Dietary protein restriction and excess of pregnant German Landrace sows induce changes in hepatic gene expression and promoter methylation of key metabolic genes in the offspring
Altmann, S., Muráni, E., Schwerin, M., Metges, C. C., Wimmers, K., & Ponsuksili, S. (2012) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2012.01.011 · Cited by 42
“Amino acid catabolism including urea synthesis, ketogenesis and gluconeogenesis is increased by high-protein diet [71,72].”
Background
When fed foods with similar palatability, healthy adult dogs and cats choose different macronutrient compositions
Hall, J. A., Vondran, J. C., Vanchina, M. A., & Jewell, D. E. (2018) · Journal of Experimental Biology · doi:10.1242/jeb.173450 · Cited by 48
“Specific adaptive processes, including increased activities of catabolic pathways such as the urea cycle, are involved in rats adapting to a long-term high-protein diet (Jean et al., 2001).”
Background
High Protein Intake Affects Lean Body Mass but Not Energy Expenditure in Nonobese Neutered Cats
Nguyen, P., Leray, V., Dumon, H., Martin, L. J. M., Siliart, B. S., Diez, M., & Biourge, V. C. (2004) · Journal of Nutrition · doi:10.1093/jn/134.8.2084s · Cited by 40
Effect of oral oleoyl-estrone on adipose tissue composition in male rats
Remesar, X., Fernández–Löpez, J., Blay, M., Savall, P., Salas, A., Díaz-Silva, M., Esteve, M., Grasa, M., & Alemany, M. (2002) · International Journal of Obesity · doi:10.1038/sj.ijo.0802056 · Cited by 39
Intestinal gluconeogenesis: metabolic benefits make sense in the light of evolution
Gautier‐Stein, A., & Mithieux, G. (2022) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-022-00707-6 · Cited by 40
Protein metabolism and related body function: mechanistic approaches and health consequences
Tomé, D., Benoit, S., & Azzout‐Marniche, D. (2020) · Proceedings of The Nutrition Society · doi:10.1017/s0029665120007880 · Cited by 39
Self-citation
The Calcium-Sensing Receptor Affects Fat Accumulation via Effects on Antilipolytic Pathways in Adipose Tissue of Rats Fed Low-Calcium Diets
He, Y., Song, Y., Liao, X.-L., Wang, L., Li, G., Alima, Li, Y., & Sun, C. (2011) · Journal of Nutrition · doi:10.3945/jn.111.141762 · Cited by 39
Characterization of dietary protein-dependent amino acid metabolism by linking free amino acids with transcriptional profiles through analysis of correlation
Noguchi, Y., Shikata, N., Furuhata, Y., Kimura, T., & Takahashi, M. (2008) · Physiological Genomics · doi:10.1152/physiolgenomics.00007.2008 · Cited by 37
Long–term dietary high protein intake up–regulates tissue specific gene expression of uncoupling proteins 1 and 2 in rats
Petzke, K. J., Friedrich, M., Metges, C. C., & Klaus, S. (2004) · European Journal of Nutrition · doi:10.1007/s00394-004-0545-4 · Cited by 36
Long-term high-protein diet intake reverts weight gain and attenuates metabolic dysfunction on high-sucrose-fed adult rats
de Sousa, R. M. L., Ribeiro, N. L. X., Pinto, B., Sanches, J. R., da Silva, M. U., Coêlho, C. F. F., França, L. M., Neto, J. A. D. F., & Paes, A. M. D. A. (2018) · Nutrition & Metabolism · doi:10.1186/s12986-018-0290-y · Cited by 34
Fos-Positive Neurons Are Increased in the Nucleus of the Solitary Tract and Decreased in the Ventromedial Hypothalamus and Amygdala by a High-Protein Diet in Rats
Nicolas, D., Fromentin, G., Raybould Helen, E., Gougis, S., W., G., & Tomé, D. (2005) · Journal of Nutrition · doi:10.1093/jn/135.6.1486 · Cited by 35
Self-citation
Long-Term Intake of a High-Protein Diet Affects Body Phenotype, Metabolism, and Plasma Hormones in Mice
Vu, J. P., Luong, L., Parsons, W. F., Oh, S., Sanford, D., Gabalski, A. H., Lighton, J. R. B., Pisegna, J. R., & Germano, P. M. (2017) · Journal of Nutrition · doi:10.3945/jn.117.257873 · Cited by 35
“In the literature, there is a lack of studies on the effects of long-term HPD regimens on energy intake and body weight and only 2 studies extended the experimental observations to a period of 3 (11) or 8 (23) wk.”
Background
Yeast Proteins Enhance Satiety in Rats
Faipoux, R., Tomé, D., Bensaı̈d, A., Morens, C., Oriol, E., Bonanno, L. M., & Fromentin, G. (2006) · Journal of Nutrition · doi:10.1093/jn/136.9.2350 · Cited by 34
“45% P/E) leads to a decrease in food intake, weight gain, and white adipose tissue (4,5).”
BackgroundSelf-citation
The Relationship Between Socioeconomic Factors and Food Security in Pregnant Women
Yadegari, L., Dolatian, M., Mahmoodi, Z., Shahsavari, S., & Sharifi, N. (2017) · Shiraz E-Medical Journal · doi:10.17795/semj41483 · Cited by 33
The Potential Application of Cupriavidus necator as Polyhydroxyalkanoates Producer and Single Cell Protein: A Review on Scientific, Cultural and Religious Perspectives
Chee, J. Y., Lakshmanan, M., Jeepery, I. F., Hairudin, N. H. B. M., & Sudesh, K. (2019) · Applied food biotechnology · doi:10.22037/afb.v6i1.22234 · Cited by 32
“The consumption of a high-protein diet initiated a depression in energy intake, causing a reduction in body fat and achieving a higher ratio of lean to fat mass [66].”
Background
The protein status of rats affects the rewarding value of meals due to their protein content
Chaumontet, C., Recio, I., Fromentin, G., Benoit, S., Piedcoq, J., Darcel, N., & Tomé, D. (2018) · The Journal of Nutrition · doi:10.1093/jn/nxy060 · Cited by 30
Self-citation
L-arginine increases postprandial circulating GLP-1 and PYY levels in humans
Amin, A., Neophytou, C., Thein, S., Martin, N. M., Alamshah, A., Spreckley, E., Bloom, S. R., & Murphy, K. G. (2018) · Obesity · doi:10.1002/oby.22323 · Cited by 29
“High-protein diets reduce food intake, facilitate weight loss, and improve body composition in animal models and humans (5-8).”
Background
High-protein diet selectively reduces fat mass and improves glucose tolerance in Western-type diet-induced obese rats
Stengel, A., Goebel‐Stengel, M., Wang, L., Hu, E., Karasawa, H., Pisegna, J. R., & Taché, Y. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00598.2012 · Cited by 31
Total Subdiaphragmatic Vagotomy Does Not Suppress High Protein Diet–Induced Food Intake Depression in Rats
L’Heureux-Bouron, D., Tomé, D., Even, P. C., Larue‐Achagiotis, C., Fromentin, G., & Rampin, O. (2003) · Journal of Nutrition · doi:10.1093/jn/133.8.2639 · Cited by 29
Self-citation
Impaired branched chain amino acid metabolism alters feeding behavior and increases orexigenic neuropeptide expression in the hypothalamus
Purpera, M. N., Li, S., Taghavi, M., Münzberg, H., Martin, R. J., Hutson, S. M., & Morrison, C. D. (2011) · Journal of Endocrinology · doi:10.1530/joe-11-0270 · Cited by 29
“2000, Jean et al .”
Effects of high-fat diets with different carbohydrate-to-protein ratios on energy homeostasis in rats with impaired brain melanocortin receptor activity
Morens, C., Keijzer, M., de Vries, K., Scheurink, A. J. W., & van Dijk, G. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00774.2004 · Cited by 27
“Because anorexigenic effects of high dietary protein levels have been documented (4, 15, 23, 25), one possibility might be that the elevated absolute amount of ingested proteins as a result of i3vt SHU9119 treatment reduced appetite in the LC-HF-HP group.”
Background
Impact of high-protein diets with either moderate or low carbohydrate on weight loss, body composition, blood pressure and glucose tolerance in rats
Lobley, G. E., Bremner, D. M., Holtrop, G., Johnstone, A. M., & Maloney, C. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507691934 · Cited by 27
“Rats switched to the two highprotein diets (HPLC and HPMC) showed modest reduced food intake, by 9 and 3 % as g/d, less than the 13–16 % observed in other studies (Jean et al. 2001; Mithieux et al. 2005) with diets that included an even higher proportion of gross energy as protein (50 %, compared with 36 % in the curr…”
Result
A Very High 70%-Protein Diet Does Not Induce Conditioned Taste Aversion in Rats
L’Heureux-Bouron, D., Tomé, D., Bensaı̈d, A., Morens, C., Gaudichon, C., & Fromentin, G. (2004) · Journal of Nutrition · doi:10.1093/jn/134.6.1512 · Cited by 26
“Rats fed the P14 diet were heavier, but this was due mainly to a higher fat mass (3).”
BackgroundMethodResultInfluentialSelf-citation
A high-protein diet or combination exercise training to improve metabolic health in individuals with long-standing spinal cord injury: a pilot randomized study
Li, J., Polston, K. F. L., Eraslan, M., Bickel, C. S., Windham, S. T., McLain, A., Oster, R. A., Bamman, M. M., & Yarar‐Fisher, C. (2018) · Physiological Reports · doi:10.14814/phy2.13813 · Cited by 24
“1999), as well as the roles of protein in preservation of fat-free mass (Jean et al. 2001) and insulin sensitization (Piatti et al.”
Background
Protein status modulates the rewarding value of foods and meals to maintain an adequate protein intake
Tomé, D., Chaumontet, C., Even, P. C., Darcel, N., & Azzout-Marniche, D. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.03.012 · Cited by 24
Rats Free to Select between Pure Protein and a Fat-Carbohydrate Mix Ingest High-Protein Mixed Meals during the Dark Period and Protein Meals during the Light Period
Makarios-Lahham, L., Roseau, S. M., Fromentin, G., Tomé, D., & Even, P. C. (2004) · Journal of Nutrition · doi:10.1093/jn/134.3.618 · Cited by 25
Self-citation
Whey protein boosts the antioxidant profile of rats by enhancing the activities of crucial antioxidant enzymes in a tissue-specific manner
Veskoukis, A. S., Kerasioti, E., Skaperda, Z., Papapostolou, P. A., Nepka, C., Spandidos, D. A., Asprodini, E. K., Taitzoglou, I., & Kouretas, D. (2020) · Food and Chemical Toxicology · doi:10.1016/j.fct.2020.111508 · Cited by 21
Whey Protein Concentrate WPC-80 Intensifies Glycoconjugate Catabolism and Induces Oxidative Stress in the Liver of Rats
Żebrowska-Gamdzyk, M., Maciejczyk, M., Zalewska, A., Guzińska-Ustymowicz, K., Tokajuk, A., & Car, H. (2018) · Nutrients · doi:10.3390/nu10091178 · Cited by 20
“It has been demonstrated that high-protein diet may result in a positive nitrogen balance, which causes increased production of urea and ammonia in the urea cycle [7].”
BackgroundInfluential
Effects of spaced feeding on gene expression of hepatic transaminase and gluconeogenic enzymes in rats
Kobayashi, A., Yokoyama, H., Kataoka, J., Ishida, T., Kuno, H., Sugai, S., Sakakibara, H., & Shimoi, K. (2011) · The Journal of Toxicological Sciences · doi:10.2131/jts.36.325 · Cited by 20
Metabolomic analysis reveals distinct profiles in the plasma and urine of rats fed a high-protein diet
Mu, C., Yang, Y., Luo, Z., & Zhu, W. (2015) · Amino Acids · doi:10.1007/s00726-015-1949-6 · Cited by 19
“In agreement with previous studies (Chevalier et al. 2013; Jean et al. 2001; Lacroix et al. 2004), our research demonstrated some hyperproteic dietrelated changes, including persistent weight loss and lower food intake, an obvious reduction of plasma triglyceride and adipose tissue weight, and a…”
BackgroundResultInfluential
Dietary macronutrient composition affects hypothalamic appetite regulation in chicks
McConn, B. R., Matias, J., Wang, G., Cline, M. A., & Gilbert, E. R. (2016) · Nutritional Neuroscience · doi:10.1080/1028415x.2016.1219103 · Cited by 18
Preabsorptive factors are not the main determinants of intake depression induced by a high-protein diet in the rat
L’Heureux-Bouron, D., Tomé, D., Bensaı̈d, A., Morens, C., LACROIX, M., Huneau, J., & Fromentin, G. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.02.029 · Cited by 18
Self-citation
Effects of Thai native chicken breast meat consumption on serum uric acid level, biochemical parameters, and antioxidant activities in rats
Potue, P., Chiangsaen, P., Maneesai, P., Khamseekaew, J., Pakdeechote, P., Chankitisakul, V., Boonkum, W., Duanghaklang, N., & Duangjinda, M. (2022) · Scientific Reports · doi:10.1038/s41598-022-18484-2 · Cited by 17
Postprandial Nutrient Partitioning but Not Energy Expenditure Is Modified in Growing Rats during Adaptation to a High-Protein Diet
Stępień, M., Gaudichon, C., Azzout‐Marniche, D., Fromentin, G., Tomé, D., & Even, P. C. (2010) · Journal of Nutrition · doi:10.3945/jn.109.120139 · Cited by 19
Self-citation
Utilizing a low-carbohydrate/high-protein diet to improve metabolic health in individuals with spinal cord injury (DISH): study protocol for a randomized controlled trial
Yarar‐Fisher, C., Li, J., McLain, A., Gower, B. A., Oster, R. A., & Morrow, C. D. (2019) · Trials · doi:10.1186/s13063-019-3520-3 · Cited by 17
Protein Status Modulates an Appetite for Protein To Maintain a Balanced Nutritional State—A Perspective View
Tomé, D., Chaumontet, C., Even, P. C., Darcel, N., Thornton, S. N., & Azzout‐Marniche, D. (2019) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.9b05990 · Cited by 19
Self-citation
Protein-Restricted Diets and Their Impact on Metabolic Health and Aging
Kim, S. Q., Spann, R. A., Hill, C. M., Berryman, C. E., Berthoud, H., McDougal, D. H., He, Y., Münzberg, H., Yu, S., & Morrison, C. D. (2025) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-121624-114918 · Cited by 17
Effect of administration of high-protein diet in rats submitted to resistance training
Lima, T. D. R., Ávila, E. T. P., Fraga, G. A., Sena, M. D. S., Dias, A. B. D. S., de Almeida, P. C., Trombeta, J. C. D. S., Vieira, R. C., Damazo, A. S., Navalta, J. W., et al. (2017) · European Journal of Nutrition · doi:10.1007/s00394-017-1391-5 · Cited by 17
Effect of High Protein Diet and ProbioticLactobacillus caseiShirota Supplementation in Aflatoxin B1-Induced Rats
Adilah, Z. N., Liew, W.-P.-P., Sabran, M. R., & Amin, I. (2018) · BioMed Research International · doi:10.1155/2018/9568351 · Cited by 16
“Following anHP diet, the liver enzymes enhance the catabolism of amino acid [35].”
Background
Sustained protein intake for bodyweight management
Westerterp‐Plantenga, M. S., Smeets, A. J. P. G., & Nieuwenhuizen, A. G. (2007) · Nutrition Bulletin · doi:10.1111/j.1467-3010.2007.00602.x · Cited by 17
Hepatic expression of the GH/JAK/STAT/IGF pathway, acute-phase response signalling and complement system are affected in mouse offspring by prenatal and early postnatal exposure to maternal high-protein diet
Vanselow, J., Kucia, M., Langhammer, M., Koczan, D., Rehfeldt, C., & Metges, C. C. (2011) · European Journal of Nutrition · doi:10.1007/s00394-011-0168-5 · Cited by 15
Energy restriction only slightly influences protein metabolism in obese rats, whatever the level of protein and its source in the diet
Chevalier, L., Bos, C., Azzout‐Marniche, D., Fromentin, G., Mosoni, L., Hafnaoui, N., Piedcoq, J., Tomé, D., & Gaudichon, C. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.19 · Cited by 18
Self-citation

Authors: Jean, C., Rome, S., Mathé, V., Huneau, J.-F., Aattouri, N., Fromentin, G., Achagiotis, C. L., & Tomé, D.
Affiliations: Physiologie de la Nutrition et du Comportement Alimentaire (FR)
Corresponding author: Tomé, Daniel
ORCID: Rome, Sophie
Huneau, Jean-François
Tomé, Daniel
Venue: The Journal of Nutrition
Publisher: Elsevier BV
Published: 2001-01
Volume: 131
Issue: 1
Pages: 91-98
ISSN: 0022-3166 (ISSN-L)
DOI: 10.1093/jn/131.1.91
OpenAlex: W1918271356
Cited by: 189
References: 52
Citations by year: 2026: 1 · 2025: 8 · 2024: 4 · 2023: 6 · 2022: 5 · 2021: 9 · 2020: 9 · 2019: 7 · 2018: 10 · 2017: 11 · 2016: 9 · 2015: 4 · 2014: 2 · 2013: 6 · 2012: 13
FWCI: 13.79
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 8075 d)
Locations: Journal of Nutrition (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diet, Metabolism, and Disease
Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
Keywords: high-protein diet, energy intake, weight gain, body composition, adipose tissue, splanchnic metabolism, brush border enzymes, gamma-glutamyl transferase, amino acid transporters, system A, hepatocytes
MeSH terms: Adaptation, Physiological, Animals, Body Composition, Carrier Proteins, Dietary Proteins, Energy Metabolism, Enzymes, Intestines, Liver, Male, Metabolism, Weight Gain, Rats, Wistar, Receptors, Glutamate, Receptors, Neurotransmitter, Amino Acid Transport Systems, Amino Acid Transport System X-AG, Excitatory Amino Acid Transporter 2, Symporters, Glutamate Plasma Membrane Transport Proteins, Rats

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Metabolic Evidence for Adaptation to a High Protein Diet in Rats

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