Protein-dependent regulation of feeding and metabolism

Morrison, Christopher D.; Laeger, Thomas

doi:10.1016/j.tem.2015.02.008

Cited by 106Regulation of Appetite and ObesityNutrition, Health and Food BehaviorBiochemical Analysis and Sensing Techniques

Protein-dependent regulation of feeding and metabolism

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Morrison, Christopher D., Laeger, Thomas·2015·Trends in Endocrinology & Metabolism

DOI 10.1016/j.tem.2015.02.008PMC PMC4416985

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Abstract

Free-feeding animals often face complex nutritional choices that require the balancing of competing nutrients, but the mechanisms driving macronutrient-specific food intake are poorly defined. A large number of behavioral studies indicate that both the quantity and quality of dietary protein can markedly influence food intake and metabolism, and that dietary protein intake may be prioritized over energy intake. This review focuses on recent progress in defining the mechanisms underlying protein-specific feeding. Considering the evidence that protein powerfully regulates both food intake and metabolism, uncovering these protein-specific mechanisms may reveal new molecular targets for the treatment of obesity and diabetes while also offering a more complete understanding of how dietary factors shape both food intake and food choice.

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A large and growing literature clearly demonstrates that animals selectively detect and adaptively respond to the restriction of dietary protein.
“there is a large and growing literature that rather clearly demonstrates that animals selectively detect and adaptively respond to the restriction of dietary protein”
From FGF21 and the physiological regulation of macronutrient preference (2020) · cites this paper as [57]

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A Central Role for Neuronal AMP-Activated Protein Kinase (AMPK) and Mammalian Target of Rapamycin (mTOR) in High-Protein Diet–Induced Weight Loss
Ropelle, E. R., Pauli, J. R., Fernandes, M. F., Rocco, S. A., Marin, R. M., Morari, J., Souza, K. K., Dias, M. M., Gomes‐Marcondes, M. C. C., Gontijo, J. A. R., et al. (2007) · Diabetes · doi:10.2337/db07-0573 · Cited by 214 · see citing works
Retracted
Anorexigenic and Orexigenic Hormone Modulation of Mammalian Target of Rapamycin Complex 1 Activity and the Regulation of Hypothalamic Agouti-Related Protein mRNA Expression
Watterson, K. R., Bestow, D., Gallagher, J. R., Hamilton, D. L., Ashford, F. B., Meakin, P. J., & Ashford, M. L. J. (2012) · Neurosignals · doi:10.1159/000334144 · Cited by 3,395 · see citing works
A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance
Newgard, C. B., An, J., Bain, J. R., Muehlbauer, M. J., Stevens, R. D., Lien, L. F., Haqq, A. M., Shah, S. H., Arlotto, M., Slentz, C. A., et al. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2009.02.002 · Cited by 3,165 · see citing works
Muscles, exercise and obesity: skeletal muscle as a secretory organ
Pedersen, B. K., & Febbraio, M. A. (2012) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2012.49 · Cited by 2,909 · see citing works
FGF-21 as a novel metabolic regulator
Kharitonenkov, A., Shiyanova, T. L., Koester, A., Ford, A. M., Micanovic, R., Galbreath, E. J., Sandusky, G. E., Hammond, L. J., Moyers, J. S., Owens, R. A., et al. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23606 · Cited by 2,125 · see citing works
Endocrine Regulation of the Fasting Response by PPARα-Mediated Induction of Fibroblast Growth Factor 21
Inagaki, T., Dutchak, P., Zhao, G., Ding, X., Gautron, L., Parameswara, V., Li, Y., Goetz, R., Mohammadi, M., Esser, V., et al. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.05.003 · Cited by 1,504 · see citing works
Hepatic Fibroblast Growth Factor 21 Is Regulated by PPARα and Is a Key Mediator of Hepatic Lipid Metabolism in Ketotic States
Badman, M. K., Pissios, P., Kennedy, A. R., Koukos, G., Flier, J. S., & Maratos-Flier, E. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.05.002 · Cited by 1,495 · see citing works
FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis
Fisher, F. M., Kleiner, S., Douris, N., Fox, E. C., Mepani, R. J., Verdeguer, F., Wu, J., Kharitonenkov, A., Flier, J. S., Maratos-Flier, E., et al. (2012) · Genes & Development · doi:10.1101/gad.177857.111 · Cited by 1,478 · see citing works
Coping with stress: eIF2 kinases and translational control
Wek, R. C., Jiang, H.-Y., & Anthony, T. G. (2006) · Biochemical Society Transactions · doi:10.1042/bst0340007 · Cited by 1,290 · see citing works
Hypothalamic mTOR Signaling Regulates Food Intake
Cota, D., Proulx, K., Smith, K. A. B., Kozma, S. C., Thomas, G., Woods, S. C., & Seeley, R. J. (2006) · Science · doi:10.1126/science.1124147 · Cited by 1,278 · see citing works
Fibroblast growth factor 21 reverses hepatic steatosis, increases energy expenditure, and improves insulin sensitivity in diet-induced obese mice
Xu, J., Lloyd, D. J., Hale, C., Stanislaus, S., Chen, M., Sivits, G., Vonderfecht, S., Hecht, R., Li, Y.-S., Lindberg, R. A., et al. (2009) · Diabetes · doi:10.2337/db08-0392 · Cited by 1,151 · see citing works
Fibroblast Growth Factor 21 Corrects Obesity in Mice
Coskun, T., Bina, H. A., Schneider, M. A., Dunbar, J. D., Hu, C. C., Chen, Y., Moller, D. E., & Kharitonenkov, A. (2008) · Endocrinology · doi:10.1210/en.2008-0816 · Cited by 1,031 · see citing works
Low protein intake is associated with a major reduction in IGF-1, cancer, and overall mortality in the 65 and younger but not older population
Levine, M. E., Suarez, J. A., Brandhorst, S., Balasubramanian, P., Cheng, C.-W., Madia, F., Fontana, L., Mirisola, M. G., Guevara-Aguirre, J., Wan, J., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.02.006 · Cited by 910 · see citing works
The Ratio of Macronutrients, Not Caloric Intake, Dictates Cardiometabolic Health, Aging, and Longevity in Ad Libitum-Fed Mice
Solon-Biet, S. M., McMahon, A. C., Ballard, J. W. O., Ruohonen, K., Wu, L. E., Cogger, V. C., Warren, A., Huang, X., Pichaud, N., Melvin, R. G., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.02.009 · Cited by 904 · see citing works
FGF21 induces PGC-1α and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response
Potthoff, M. J., Inagaki, T., Satapati, S., Ding, X., He, T., Goetz, R., Mohammadi, M., Finck, B. N., Mangelsdorf, D. J., Kliewer, S. A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904187106 · Cited by 704 · see citing works
Critical role for peptide YY in protein-mediated satiation and body-weight regulation
Batterham, R. L., Heffron, H., Kapoor, S., Chivers, J. E., Chandarana, K., Herzog, H., le Roux, C. W., Thomas, E. L., Bell, J. D., & Withers, D. J. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.08.001 · Cited by 623 · see citing works
Effects of energy-restricted high-protein, low-fat compared with standard-protein, low-fat diets: a meta-analysis of randomized controlled trials
Wycherley, T. P., Moran, L. J., Clifton, P. M., Noakes, M., & Brinkworth, G. D. (2012) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.044321 · Cited by 606 · see citing works
FGF21 is an endocrine signal of protein restriction
Laeger, T., Henagan, T. M., Albarado, D. C., Redman, L. M., Bray, G. A., Noland, R. C., Münzberg, H., Hutson, S. M., Gettys, T. W., Schwartz, M. W., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci74915 · Cited by 593 · cited 2× · see citing works
“Finally, the role of FGF21 in the behavioral and metabolic responses to general dietary protein restriction was tested recently [14].”
Circulating FGF21 Is Liver Derived and Enhances Glucose Uptake During Refeeding and Overfeeding
Markan, K. R., Naber, M. C., Ameka, M. K., Anderegg, M. D., Mangelsdorf, D. J., Kliewer, S. A., Mohammadi, M., & Potthoff, M. J. (2014) · Diabetes · doi:10.2337/db14-0595 · Cited by 590 · see citing works
Dietary protein, weight loss, and weight maintenance
Westerterp-Plantenga, M. S., Nieuwenhuizen, A., Tomé, D., Soenen, S., & Westerterp, K. R. (2009) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-080508-141056 · Cited by 570 · see citing works
FGF21 regulates metabolism and circadian behavior by acting on the nervous system
Bookout, A. L., de Groot, M. H. M., Owen, B. M., Lee, S., Gautron, L., Lawrence, H. L., Ding, X., Elmquist, J. K., Takahashi, J. S., Mangelsdorf, D. J., et al. (2013) · Nature Medicine · doi:10.1038/nm.3249 · Cited by 545 · see citing works
FGF21 acts centrally to induce sympathetic nerve activity, energy expenditure, and weight loss
Owen, B. M., Ding, X., Morgan, D. A., Coate, K. C., Bookout, A. L., Rahmouni, K., Kliewer, S. A., & Mangelsdorf, D. J. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.07.012 · Cited by 523 · see citing works
Coping with stress: eIF2 kinases and translational control
Jiang, H.-Y., Wek, R. C., & Anthony, T. G. (2005) · Biochemical Society Transactions · doi:10.1042/bst20060007 · Cited by 522 · see citing works
The GCN2 eIF2α Kinase Is Required for Adaptation to Amino Acid Deprivation in Mice
Zhang, P., McGrath, B. C., Reinert, J., Olsen, D. S., Li, L., Gill, S., Wek, S. A., Vattem, K. M., Wek, R. C., Kimball, S. R., et al. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.19.6681-6688.2002 · Cited by 439 · see citing works
The starvation hormone, fibroblast growth factor-21, extends lifespan in mice
Zhang, Y., Xie, Y., Berglund, E. D., Coate, K. C., He, T. T., Katafuchi, T., Xiao, G., Potthoff, M. J., Wei, W., Wan, Y., et al. (2012) · eLife · doi:10.7554/elife.00065 · Cited by 420 · see citing works
βKlotho Is Required for Fibroblast Growth Factor 21 Effects on Growth and Metabolism
Ding, X., Boney-Montoya, J., Owen, B. M., Bookout, A. L., Coate, K. C., Mangelsdorf, D. J., & Kliewer, S. A. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.08.002 · Cited by 403 · see citing works
Uncharged tRNA and Sensing of Amino Acid Deficiency in Mammalian Piriform Cortex
Hao, S., Sharp, J. W., Ross‐Inta, C., McDaniel, B. J., Anthony, T. G., Wek, R. C., Cavener, D. R., McGrath, B. C., Rudell, J. B., Koehnle, T. J., et al. (2005) · Science · doi:10.1126/science.1104882 · Cited by 341 · see citing works
The GCN2 eIF2α Kinase Regulates Fatty-Acid Homeostasis in the Liver during Deprivation of an Essential Amino Acid
Guo, F., & Cavener, D. R. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.01.001 · Cited by 301 · see citing works
Fibroblast Growth Factor 21 Action in the Brain Increases Energy Expenditure and Insulin Sensitivity in Obese Rats
Sarruf, D. A., Thaler, J. P., Morton, G. J., German, J. P., Fischer, J. D., Ogimoto, K., & Schwartz, M. W. (2010) · Diabetes · doi:10.2337/db09-1878 · Cited by 287 · see citing works
The breadth of FGF21's metabolic actions are governed by FGFR1 in adipose tissue
Adams, A. C., Yang, C., Coskun, T., Cheng, C. C., Gimeno, R. E., Luo, Y., & Kharitonenkov, A. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2012.08.007 · Cited by 266 · see citing works
Testing Protein Leverage in Lean Humans: A Randomised Controlled Experimental Study
Gosby, A. K., Conigrave, A. D., Lau, N. S., Iglesias, M. A., Hall, R. M., Jebb, S. A., Brand-Miller, J. C., Caterson, I. D., Raubenheimer, D., & Simpson, S. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025929 · Cited by 254 · see citing works
Activating transcription factor 4-dependent induction of FGF21 during amino acid deprivation
De Sousa-Coelho, A. L., Marrero, P. F., & Haro, D. (2012) · Biochemical Journal · doi:10.1042/bj20111748 · Cited by 246 · see citing works
Interplay between FGF21 and insulin action in the liver regulates metabolism
Emanuelli, B., Vienberg, S. G., Smyth, G., Cheng, C., Stanford, K. I., Arumugam, M., Michael, M. D., Adams, A. C., Kharitonenkov, A., & Kahn, C. R. (2014) · Journal of Clinical Investigation · doi:10.1172/jci67353 · Cited by 243 · see citing works
Effect of a high-protein breakfast on the postprandial ghrelin response
Blom, W. A. M., Lluch, A., Stafleu, A., Vinoy, S., Holst, J. J., Schaafsma, G., & Hendriks, H. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.2.211 · Cited by 242 · see citing works
Mediobasal Hypothalamic Leucine Sensing Regulates Food Intake through Activation of a Hypothalamus-Brainstem Circuit
Blouet, C., Jo, Y., Li, X., & Schwartz, G. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1668-09.2009 · Cited by 240 · see citing works
The GCN2 kinase biases feeding behavior to maintain amino acid homeostasis in omnivores
Maurin, A., Jousse, C., Avérous, J., Parry, L., Bruhat, A., Chérasse, Y., Zeng, H., Zhang, Y., Harding, H. P., Ron, D., et al. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.03.004 · Cited by 240 · see citing works
Integrated Regulation of Hepatic Metabolism by Fibroblast Growth Factor 21 (FGF21) in Vivo
Fisher, F. M., Estall, J. L., Adams, A. C., Antonellis, P. J., Bina, H. A., Flier, J. S., Kharitonenkov, A., Spiegelman, B. M., & Maratos–Flier, E. (2011) · Endocrinology · doi:10.1210/en.2011-0281 · Cited by 229 · see citing works
Skeletal muscle mitochondrial uncoupling drives endocrine cross-talk through the induction of FGF21 as a myokine
Keipert, S., Ost, M., Johann, K., Imber, F., Jastroch, M., van Schothorst, E. M., Keijer, J., & Klaus, S. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00330.2013 · Cited by 221 · see citing works
Protein‐leverage in Mice: The Geometry of Macronutrient Balancing and Consequences for Fat Deposition
Sørensen, A., Mayntz, D., Raubenheimer, D., & Simpson, S. J. (2008) · Obesity · doi:10.1038/oby.2007.58 · Cited by 218 · see citing works
Methionine restriction restores a younger metabolic phenotype in adult mice with alterations in fibroblast growth factor 21
Lees, E. K., Król, E., Grant, L., Shearer, K., Wyse, C. A., Moncur, E. M., Bykowska, A. S., Mody, N., Gettys, T. W., & Delibegović, M. (2014) · Aging Cell · doi:10.1111/acel.12238 · Cited by 203 · see citing works
Mechanisms of Increased In Vivo Insulin Sensitivity by Dietary Methionine Restriction in Mice
Stone, K. P., Wanders, D., Orgeron, M., Cortez, C. C., & Gettys, T. W. (2014) · Diabetes · doi:10.2337/db14-0464 · Cited by 201 · see citing works
Protein leverage and energy intake
Gosby, A. K., Conigrave, A. D., Raubenheimer, D., & Simpson, S. J. (2014) · Obesity Reviews · doi:10.1111/obr.12131 · Cited by 196 · see citing works
Portal sensing of intestinal gluconeogenesis is a mechanistic link in the diminution of food intake induced by diet protein
Mithieux, G., Misery, P., Magnan, C., Pillot, B., Gautier‐Stein, A., Bernard, C., Rajas, F., & Zitoun, C. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.09.010 · Cited by 195 · see citing works
Effects of fat, protein, and carbohydrate and protein load on appetite, plasma cholecystokinin, peptide YY, and ghrelin, and energy intake in lean and obese men
Brennan, I. M., Luscombe‐Marsh, N. D., Seimon, R. V., Otto, B., Horowitz, M., Wishart, J. M., & Feinle‐Bisset, C. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00478.2011 · Cited by 190 · see citing works
Metabolic Evidence for Adaptation to a High Protein Diet in Rats
Jean, C., Rome, S., Mathé, V., Huneau, J.-F., Aattouri, N., Fromentin, G., Achagiotis, C. L., & Tomé, D. (2001) · The Journal of Nutrition · doi:10.1093/jn/131.1.91 · Cited by 189 · see citing works
Beneficial effects of a higher-protein breakfast on the appetitive, hormonal, and neural signals controlling energy intake regulation in overweight/obese, “breakfast-skipping,” late-adolescent girls
Leidy, H. J., Ortinau, L. C., Douglas, S. M., & Hoertel, H. A. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.053116 · Cited by 187 · see citing works
Amino acids inhibit <i>Agrp</i> gene expression via an mTOR-dependent mechanism
Morrison, C. D., Xi, X., White, C. L., Ye, J., & Martin, R. J. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00675.2006 · Cited by 183 · see citing works
Self-citation
Peripheral and central mechanisms involved in the control of food intake by dietary amino acids and proteins
Fromentin, G., Darcel, N., Chaumontet, C., Marsset‐Baglieri, A., Nadkarni, N. A., & Tomé, D. (2012) · Nutrition Research Reviews · doi:10.1017/s0954422411000175 · Cited by 181 · see citing works
Contribution of gastroenteropancreatic appetite hormones to protein-induced satiety
Belza, A., Ritz, C., Sørensen, M. Q., Holst, J. J., Rehfeld, J. F., & Astrup, A. V. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.047563 · Cited by 171 · see citing works
Fibroblast growth factor 21 is induced by endoplasmic reticulum stress
Schaap, F. G., Kremer, A. E., Lamers, W. H., Jansen, P. L. M., & Gaemers, I. C. (2012) · Biochimie · doi:10.1016/j.biochi.2012.10.019 · Cited by 164 · see citing works
Adaptation of rats to diets containing different levels of protein: effects on food intake, plasma and brain amino acid concentrations and brain neurotransmitter metabolism
Peters, J. C., & Harper, A. E. (1985) · The Journal of Nutrition · doi:10.1093/jn/115.3.382 · Cited by 163 · see citing works
Protein status elicits compensatory changes in food intake and food preferences
Griffioen-Roose, S., Mars, M., Siebelink, E., Finlayson, G., Tomé, D., & de Graaf, C. (2012) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.020503 · Cited by 163 · see citing works
A long-term high-protein diet markedly reduces adipose tissue without major side effects in Wistar male rats
Lacroix, M., Gaudichon, C., Martin, A., Morens, C., Mathé, V., Tomé, D., & Huneau, J.-F. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00100.2004 · Cited by 161 · see citing works
Restoration of leptin responsiveness in diet‐induced obese mice using an optimized leptin analog in combination with exendin‐4 or FGF21
Müller, T. D., Sullivan, L. M., Habegger, K., Yi, C., Kabra, D., Grant, E., Ottaway, N., Krishna, R., Holland, J., Hembree, J., et al. (2012) · Journal of Peptide Science · doi:10.1002/psc.2408 · Cited by 156 · see citing works
Food Intake, Energy Balance and Serum Leptin Concentrations in Rats Fed Low-Protein Diets
Du, F., Higginbotham, D. A., & White, B. D. (2000) · Journal of Nutrition · doi:10.1093/jn/130.3.514 · Cited by 156 · see citing works
Brainstem Nutrient Sensing in the Nucleus of the Solitary Tract Inhibits Feeding
Blouet, C., & Schwartz, G. J. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.10.003 · Cited by 145 · see citing works
The Transcription Factor Network Associated With the Amino Acid Response in Mammalian Cells
Kilberg, M. S., Balasubramanian, M. N., Fu, L., & Shan, J. (2012) · Advances in Nutrition · doi:10.3945/an.112.001891 · Cited by 143 · see citing works
Protein, amino acids, vagus nerve signaling, and the brain
Tomé, D., Schwarz, J., Darcel, N., & Fromentin, G. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.27462w · Cited by 138 · see citing works
Remodeling the Integration of Lipid Metabolism Between Liver and Adipose Tissue by Dietary Methionine Restriction in Rats
Hasek, B. E., Boudreau, A., Shin, J., Feng, D., Hulver, M. W., Van, N. T., Laque, A., Stewart, L. K., Stone, K. P., Wanders, D., et al. (2013) · Diabetes · doi:10.2337/db13-0501 · Cited by 136 · see citing works
Normal Protein Intake Is Required for Body Weight Loss and Weight Maintenance, and Elevated Protein Intake for Additional Preservation of Resting Energy Expenditure and Fat Free Mass
Soenen, S., Martens, E. A. P., Hochstenbach‐Waelen, A., Lemmens, S. G. T., & Westerterp‐Plantenga, M. S. (2013) · Journal of Nutrition · doi:10.3945/jn.112.167593 · Cited by 133 · see citing works
Metformin-induced inhibition of the mitochondrial respiratory chain increases FGF21 expression via ATF4 activation
Kim, K. H., Jeong, Y. T., Kim, S. H., Jung, H. S., Park, K. S., Lee, H.-Y., & Lee, M.-S. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.09.026 · Cited by 112 · see citing works
Geometric analysis of macronutrient selection in the rat
SIMPSON, S. J., & RAUBENHEIMER, D. (1997) · Appetite · doi:10.1006/appe.1996.0077 · Cited by 110 · see citing works
mTOR, AMPK, and GCN2 coordinate the adaptation of hepatic energy metabolic pathways in response to protein intake in the rat
Chotechuang, N., Azzout‐Marniche, D., Bos, C., Chaumontet, C., Gausserès, N., Steiler, T. L., Gaudichon, C., & Tomé, D. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.91000.2008 · Cited by 107 · see citing works
Leucine Supplementation of Drinking Water Does Not Alter Susceptibility to Diet-Induced Obesity in Mice
Nairizi, A., She, P., Vary, T. C., & Lynch, C. J. (2009) · Journal of Nutrition · doi:10.3945/jn.108.100081 · Cited by 102 · see citing works
A high-protein diet enhances satiety without conditioned taste aversion in the rat
Bensaı̈d, A., Tomé, D., L'Heureux-Bourdon, D., Even, P., Gietzen, D., Morens, C., Gaudichon, C., Larue-Achagiotis, C., & Fromentin, G. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00977-0 · Cited by 100 · see citing works
Homeostatic regulation of protein intake: in search of a mechanism
Morrison, C. D., Reed, S. D., & Henagan, T. M. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00609.2011 · Cited by 99 · see citing works
Protein selection, food intake, and body composition in response to the amount of dietary protein
White, B. D., Porter, M. H., & Martin, R. J. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00232-2 · Cited by 91 · see citing works
Neural and metabolic regulation of macronutrient intake and selection
Berthoud, H.-R., Münzberg, H., Richards, B. K., & Morrison, C. D. (2012) · Proceedings of The Nutrition Society · doi:10.1017/s0029665112000559 · Cited by 87 · see citing works
Human protein status modulates brain reward responses to food cues
Griffioen-Roose, S., Smeets, P. A., van den Heuvel, E., Boesveldt, S., Finlayson, G., & de Graaf, C. (2014) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.079392 · Cited by 87 · see citing works
Metabolic and Genomic Response to Dietary Isocaloric Protein Restriction in the Rat
Kalhan, S. C., Uppal, S. O., Moorman, J. L., Bennett, C. D., Gruca, L. L., Parimi, P. S., Dasarathy, S., Serre, D., & Hanson, R. W. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.185991 · Cited by 80 · see citing works
Specific amino acids inhibit food intake via the area postrema or vagal afferents
Jordi, J., Herzog, B., Camargo, S. M. R., Boyle, C. N., Lutz, T. A., & Verrey, F. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.258947 · Cited by 79 · see citing works
Unlearned specific appetite for protein
Deutsch, J. A., Moore, B. O., & Heinrichs, S. C. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90341-7 · Cited by 77 · see citing works
Protein-induced satiety is abolished in the absence of intestinal gluconeogenesis
Penhoat, A., Mutel, E., Amigó-Correig, M., Pillot, B., Stefanutti, A., Rajas, F., & Mithieux, G. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.03.012 · Cited by 65 · see citing works
Leucine acts in the brain to suppress food intake but does not function as a physiological signal of low dietary protein
Laeger, T., Reed, S. D., Henagan, T. M., Fernandez, D. H., Taghavi, M., Addington, A. K., Münzberg, H., Martin, R. J., Hutson, S. M., & Morrison, C. D. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00116.2014 · Cited by 63 · see citing works
Effects of age on the feeding response to moderately low dietary protein in rats
White, B. D., Porter, M. H., & Martin, R. J. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00229-2 · Cited by 63 · see citing works
Control of protein and energy intake - brain mechanisms
Davidenko, O., Darcel, N., Fromentin, G., & Tomé, D. (2013) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2013.73 · Cited by 63 · see citing works
A systems biology analysis of the unique and overlapping transcriptional responses to caloric restriction and dietary methionine restriction in rats
Ghosh, S., Wanders, D., Stone, K. P., Van, N. T., Cortez, C. C., & Gettys, T. W. (2014) · The FASEB Journal · doi:10.1096/fj.14-249458 · Cited by 54 · see citing works
Protein leverage effects of beef protein on energy intake in humans
Martens, E. A. P., Tan, S., Dunlop, M. V., Mattes, R. D., & Westerterp‐Plantenga, M. S. (2014) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.078774 · Cited by 53 · see citing works
Remodeling of lipid metabolism by dietary restriction of essential amino acids
Anthony, T. G., Morrison, C. D., & Gettys, T. W. (2013) · Diabetes · doi:10.2337/db12-1613 · Cited by 52 · see citing works
GCN2 is required to increase fibroblast growth factor 21 and maintain hepatic triglyceride homeostasis during asparaginase treatment
Wilson, G. J., Lennox, B. A., She, P., Mirek, E. T., Al Baghdadi, R. J. T., Fusakio, M. E., Dixon, J. L., Henderson, G. C., Wek, R. C., & Anthony, T. G. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00361.2014 · Cited by 52 · see citing works
Detection of amino acid deprivation in the central nervous system
Anthony, T. G., & Gietzen, D. W. (2012) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32835b618b · Cited by 51 · see citing works
Effect of lysine on afferent activity of the hepatic branch of the vagus nerve in normal and l-lysine-deficient rats
Torii, K., & Niijima, A. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00426-7 · Cited by 50 · see citing works
Protein diets, body weight loss and weight maintenance
Martens, E. A. P., & Westerterp‐Plantenga, M. S. (2013) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000006 · Cited by 50 · see citing works
S6K1 in the Central Nervous System Regulates Energy Expenditure via MC4R/CRH Pathways in Response to Deprivation of an Essential Amino Acid
Xia, T., Cheng, Y., Zhang, Q., Xiao, F., Liu, B., Chen, S., & Guo, F. (2012) · Diabetes · doi:10.2337/db11-1278 · Cited by 48 · see citing works
Small Changes in Essential Amino Acid Concentrations Alter Diet Selection in Amino Acid–Deficient Rats
Hrupka, B. J., Lin, Y. M., Gietzen, D. W., & Rogers, Q. R. (1997) · Journal of Nutrition · doi:10.1093/jn/127.5.777 · Cited by 36 · see citing works
Oral Leucine Supplementation Is Sensed by the Brain but neither Reduces Food Intake nor Induces an Anorectic Pattern of Gene Expression in the Hypothalamus
Zampieri, T. T., Pedroso, J. A. B., Furigo, I. C., Tirapegui, J., & Donato, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0084094 · Cited by 35 · see citing works
Central Leucine Sensing in the Control of Energy Homeostasis
Schwartz, G. J. (2012) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2012.12.001 · Cited by 33 · see citing works
Three-Dimensional Macronutrient-Associated Fos Expression Patterns in the Mouse Brainstem
Schwarz, J., Burguet, J., Rampin, O., Fromentin, G., Andrey, P., Tomé, D., Maurin, Y., & Darcel, N. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008974 · Cited by 32 · see citing works
The Rapid Anorectic Response to a Threonine Imbalanced Diet is decreased by Injection of Threonine into the Anterior Piriform Cortex of Rats
Russell, M., Koehnle, T. J., Barrett, J. A., Blevins, J. E., & Gietzen, D. W. (2003) · Nutritional Neuroscience · doi:10.1080/1028415031000151567 · Cited by 30 · see citing works
Rats Treated with Somatotropin Select Diets Higher in Protein
Roberts, T. J., Azain, M. J., White, B. D., & Martin, R. J. (1995) · Journal of Nutrition · doi:10.1093/jn/125.10.2669 · Cited by 29 · see citing works
Dietary branched-chain amino acids and protein selection by rats
Anderson, S. A., Tews, J. K., & Harper, A. E. (1990) · The Journal of Nutrition · doi:10.1093/jn/120.1.52 · Cited by 22 · see citing works
Nutrient control of hunger by extrinsic gastrointestinal neurons
Mithieux, G. (2013) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2013.04.005 · Cited by 19 · see citing works
Effect of central and peripheral leucine on energy metabolism in the Djungarian hamster (Phodopus sungorus)
Koch, C. E., Göddeke, S., Krüger, M., & Tups, A. (2012) · Journal of Comparative Physiology B · doi:10.1007/s00360-012-0699-y · Cited by 14 · see citing works
CREB/TRH pathway in the central nervous system regulates energy expenditure in response to deprivation of an essential amino acid
Xia, T., Zhang, Q., Xiao, Y., Wang, C., Yu, J., Liu, H., Liu, B., Zhang, Y., Chen, S., Liu, Y., et al. (2014) · International Journal of Obesity · doi:10.1038/ijo.2014.65 · Cited by 11 · see citing works

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FGF21 mediates endocrine control of simple sugar intake and sweet taste preference by the liver
von Holstein-Rathlou, S., BonDurant, L. D., Peltekian, L., Naber, M. C., Yin, T. C., Claflin, K. E., Urizar, A. I., Madsen, A. N., Ratner, C., Holst, B., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2015.12.003 · Cited by 347 · see citing works
Hepatokines and metabolism: Deciphering communication from the liver
Jensen-Cody, S. O., & Potthoff, M. J. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101138 · Cited by 252 · see citing works
FGF21 Signals Protein Status to the Brain and Adaptively Regulates Food Choice and Metabolism
Hill, C. M., Laeger, T., Dehner, M., Albarado, D. C., Clarke, B., Wanders, D., Burke, S. J., Collier, J. J., Qualls-Creekmore, E., Solon-Biet, S. M., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.022 · Cited by 229 · see citing works
Quinoa (Chenopodium quinoa Willd), from Nutritional Value to Potential Health Benefits: An Integrative Review
Gordillo‐Bastidas, E., & Díaz‐Rizzolo, D. A. (2016) · Journal of Nutrition & Food Sciences · doi:10.4172/2155-9600.1000497 · Cited by 227 · see citing works
Fibroblast Growth Factor 21: A Versatile Regulator of Metabolic Homeostasis
BonDurant, L. D., & Potthoff, M. J. (2018) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071816-064800 · Cited by 222 · see citing works
Defining the Nutritional and Metabolic Context of FGF21 Using the Geometric Framework
Solon-Biet, S. M., Cogger, V. C., Pulpitel, T., Heblinski, M., Wahl, D., McMahon, A. C., Warren, A., Durrant-Whyte, J., Walters, K. A., Krycer, J. R., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.09.001 · Cited by 212 · see citing works
Metabolic Responses to Dietary Protein Restriction Require an Increase in FGF21 that Is Delayed by the Absence of GCN2
Laeger, T., Albarado, D. C., Burke, S. J., Trosclair, L., Hedgepeth, J. W., Berthoud, H.-R., Gettys, T. W., Collier, J. J., Münzberg, H., & Morrison, C. D. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.044 · Cited by 206 · see citing works
Self-citation
FGF21 Signals to Glutamatergic Neurons in the Ventromedial Hypothalamus to Suppress Carbohydrate Intake
Jensen-Cody, S. O., Flippo, K. H., Claflin, K. E., Yavuz, Y., Sapouckey, S. A., Walters, G. C., Usachev, Y. M., Atasoy, D., Gillum, M. P., & Potthoff, M. J. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.06.008 · Cited by 166 · see citing works
Central regulation of food intake in fish: an evolutionary perspective
Soengas, J. L., Cerdá‐Reverter, J. M., & Delgado, M. J. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0320 · Cited by 165 · see citing works
New developments in the biology of fibroblast growth factors
Ornitz, D. M., & Itoh, N. (2022) · WIREs Mechanisms of Disease · doi:10.1002/wsbm.1549 · Cited by 143 · see citing works
Hepatic circadian clock oscillators and nuclear receptors integrate microbiome-derived signals
Montagner, A., Korecka, A., Polizzi, A., Lippi, Y., Blum, Y., Canlet, C., Tremblay-Franco, M., Gautier-Stein, A., Burcelin, R., Yen, Y.-C., et al. (2016) · Scientific Reports · doi:10.1038/srep20127 · Cited by 137 · see citing works
“FGF21 is a nutritionally regulated hormone that induces a broad range of beneficial metabolic effects and emerges as a key player in a mechanism coordinating behaviour, growth, and metabolism during periods of reduced dietary protein intake 19 .”
Revisiting the role of protein-induced satiation and satiety
Morell, P., & Fiszman, S. (2016) · Food Hydrocolloids · doi:10.1016/j.foodhyd.2016.08.003 · Cited by 117 · see citing works
FGF21 and the physiological regulation of macronutrient preference
Hill, C. M., Qualls-Creekmore, E., Berthoud, H.-R., Soto, P., Yu, S., McDougal, D. H., Münzberg, H., & Morrison, C. D. (2020) · Endocrinology · doi:10.1210/endocr/bqaa019 · Cited by 99 · see citing works
Self-citation
Low protein-induced increases in FGF21 drive UCP1-dependent metabolic but not thermoregulatory endpoints
Hill, C. M., Laeger, T., Albarado, D. C., McDougal, D. H., Berthoud, H.-R., Münzberg, H., & Morrison, C. D. (2017) · Scientific Reports · doi:10.1038/s41598-017-07498-w · Cited by 97 · see citing works
Fibroblast Growth Factor 21 and the Adaptive Response to Nutritional Challenges
Martínez‐Garza, Ú., Torres‐Oteros, D., Yarritu, A., Marrero, P. F., Haro, D., & Relat, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20194692 · Cited by 87 · see citing works
Sustainable food protein supply reconciling human and ecosystem health: A Leibniz Position
Weindl, I., Ost, M., Wiedmer, P., Schreiner, M., Neugart, S., Klopsch, R., Kühnhold, H., Kloas, W., Henkel, I. M., Schlüter, O., et al. (2020) · Global Food Security · doi:10.1016/j.gfs.2020.100367 · Cited by 88 · see citing works
FGF19 and FGF21: In NASH we trust
Talukdar, S., & Kharitonenkov, A. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101152 · Cited by 82 · see citing works
Central Amino Acid Sensing in the Control of Feeding Behavior
Heeley, N., & Blouet, C. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00148 · Cited by 79 · see citing works
Triclosan leads to dysregulation of the metabolic regulator FGF21 exacerbating high fat diet-induced nonalcoholic fatty liver disease
Yueh, M., He, F., Chen, C., Vu, C., Tripathi, A., Knight, R. D., Karin, M., Chen, S., & Tukey, R. H. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2017129117 · Cited by 77 · see citing works
Nutritional Regulation of Gene Expression: Carbohydrate-, Fat- and Amino Acid-Dependent Modulation of Transcriptional Activity
Haro, D., Marrero, P., & Relat, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20061386 · Cited by 56 · see citing works
Type of infant formula increases early weight gain and impacts energy balance: a randomized controlled trial
Mennella, J. A., Inamdar, L., Pressman, N., Schall, J. I., Papas, M. A., Schoeller, D. A., Stallings, V. A., & Trabulsi, J. (2018) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy188 · Cited by 69 · see citing works
Homeostatic sensing of dietary protein restriction: a case for FGF21
Hill, C. M., Berthoud, H.-R., Münzberg, H., & Morrison, C. D. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.06.002 · Cited by 68 · see citing works
Fibroblast growth factor-21 controls dietary protein intake in male mice
Larson, K. R., Chaffin, A. T.-B., Goodson, M. L., Fang, Y., & Ryan, K. K. (2019) · Endocrinology · doi:10.1210/en.2018-01056 · Cited by 68 · see citing works
Low plasma adropin concentrations increase risks of weight gain and metabolic dysregulation in response to a high-sugar diet in male nonhuman primates
Butler, A. A., Zhang, J., Price, C. A., Stevens, J. R., Graham, J. L., Stanhope, K. L., King, S. M., Krauss, R. M., Bremer, A. A., & Havel, P. J. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.007528 · Cited by 69 · see citing works
Di- and tripeptide transport in vertebrates: the contribution of teleost fish models
Verri, T., Barca, A., Pisani, P., Piccinni, B., Storelli, C., & Romano, A. (2016) · Journal of Comparative Physiology B · doi:10.1007/s00360-016-1044-7 · Cited by 64 · see citing works
FGF21 improves glucose homeostasis in an obese diabetes-prone mouse model independent of body fat changes
Laeger, T., Baumeier, C., Wilhelmi, I., Würfel, J., Kamitz, A., & Schürmann, A. (2017) · Diabetologia · doi:10.1007/s00125-017-4389-x · Cited by 59 · see citing works
Amino acid transporters in the regulation of insulin secretion and signalling
Javed, K., & Fairweather, S. J. (2019) · Biochemical Society Transactions · doi:10.1042/bst20180250 · Cited by 59 · see citing works
Diet polyphenol curcumin stimulates hepatic Fgf21 production and restores its sensitivity in high fat diet fed male mice
Zeng, K., Tian, L., Patel, R., Shao, W., Song, Z., Liu, L., Manuel, J., Ma, X., McGilvray, I. D., Cummins, C. L., et al. (2016) · Endocrinology · doi:10.1210/en.2016-1596 · Cited by 57 · see citing works
A low aromatic amino-acid diet improves renal function and prevent kidney fibrosis in mice with chronic kidney disease
Barba, C., Benoit, B., Bres, É., Chanon, S., Vieille‐Marchiset, A., Pinteur, C., Pesenti, S., Glorieux, G., Picard, C., Fouque, D. P., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-98718-x · Cited by 57 · see citing works
Chronic leucine supplementation improves lipid metabolism in C57BL/6J mice fed with a high-fat/cholesterol diet
Jiao, J., Han, S.-F., Zhang, W., Xu, J., Tong, X., Yin, X.-B., Yuan, L., & Qin, L. (2016) · Food & Nutrition Research · doi:10.3402/fnr.v60.31304 · Cited by 56 · see citing works
Evidence for the presence in rainbow trout brain of amino acid-sensing systems involved in the control of food intake
Comesaña, S., Velasco, C., Ceinos, R. M., López‐Patiño, M. A., Míguez, J. M., Morais, S., & Soengas, J. L. (2017) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00283.2017 · Cited by 56 · see citing works
Neural Control of Energy Expenditure
Münzberg, H., Qualls‐Creekmore, E., Berthoud, H., Morrison, C. D., & Yu, S. (2015) · Handbook of experimental pharmacology · doi:10.1007/164_2015_33 · Cited by 53 · see citing works
The influence of developmental diet on reproduction and metabolism in Drosophila
Klepsatel, P., Knoblochová, D., Girish, T. N., Dircksen, H., & Gáliková, M. (2020) · BMC Evolutionary Biology · doi:10.1186/s12862-020-01663-y · Cited by 54 · see citing works
Raised FGF-21 and triglycerides accompany increased energy intake driven by protein leverage in lean, healthy individuals: a randomised trial
Gosby, A. K., Lau, N. S., Tam, C. S., Iglesias, M. A., Morrison, C. D., Caterson, I. D., Brand-Miller, J., Conigrave, A. D., Raubenheimer, D., & Simpson, S. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161003 · Cited by 51 · see citing works
Animal Models for the Study of the Relationships between Diet and Obesity: A Focus on Dietary Protein and Estrogen Deficiency
Chalvon‐Demersay, T., Blachier, F., Tomé, D., & Blais, A. (2017) · Frontiers in Nutrition · doi:10.3389/fnut.2017.00005 · Cited by 50 · see citing works
Effects of Long-Term Dietary Protein Restriction on Intestinal Morphology, Digestive Enzymes, Gut Hormones, and Colonic Microbiota in Pigs
Yu, D., Zhu, W., & Hang, S. (2019) · Animals · doi:10.3390/ani9040180 · Cited by 50 · see citing works
FGF21 signaling in glutamatergic neurons is required for weight loss associated with dietary protein dilution
Flippo, K. H., Jensen-Cody, S. O., Claflin, K. E., & Potthoff, M. J. (2020) · Scientific Reports · doi:10.1038/s41598-020-76593-2 · Cited by 49 · see citing works
Toward reconciling the roles of FGF21 in protein appetite, sweet preference, and energy expenditure
Solon‐Biet, S. M., Clark, X., Bell-Anderson, K. S., Rusu, P. M., Perks, R., Freire, T., Pulpitel, T., Senior, A. M., Hoy, A. J., Aung, O., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113536 · Cited by 41 · see citing works
The nutritional geometry of liver disease including non-alcoholic fatty liver disease
Simpson, S. J., Raubenheimer, D., Cogger, V. C., Macia, L., Solon‐Biet, S. M., Couteur, D. G. L., & George, J. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2017.10.005 · Cited by 42 · see citing works
Importance of Serum Amino Acid Profile for Induction of Hepatic Steatosis under Protein Malnutrition
Nishi, H., Yamanaka, D., Kamei, H., Goda, Y., Kumano, M., Toyoshima, Y., Takenaka, A., Masuda, M., NAKABAYASHI, Y., Shioya, R., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-23640-8 · Cited by 44 · see citing works
Restriction of dietary protein leads to conditioned protein preference and elevated palatability of protein-containing food in rats
Murphy, M., Peters, K. Z., Denton, B. S., Lee, K. A., Chadchankar, H., & McCutcheon, J. E. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.12.011 · Cited by 42 · see citing works
Symposium review: The dairy matrix—Bioaccessibility and bioavailability of nutrients and physiological effects
Turgeon, S. L., & Brisson, G. J. (2019) · Journal of Dairy Science · doi:10.3168/jds.2019-17308 · Cited by 42 · see citing works
Feeding Stimulation Ability and Central Effects of Intraperitoneal Treatment of L-Leucine, L-Valine, and L-Proline on Amino Acid Sensing Systems in Rainbow Trout: Implication in Food Intake Control
Comesaña, S., Velasco, C., Conde‐Sieira, M., Míguez, J. M., Soengas, J. L., & Morais, S. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01209 · Cited by 36 · see citing works
Hepatic autophagy contributes to the metabolic response to dietary protein restriction
Henagan, T. M., Laeger, T., Navard, A. M., Albarado, D., Noland, R. C., Stadler, K., Elks, C. M., Burk, D., & Morrison, C. D. (2016) · Metabolism · doi:10.1016/j.metabol.2016.02.015 · Cited by 36 · see citing works
Feed Intake Regulation in Fish: Implications for Aquaculture
Soengas, J. L., Comesaña, S., Blanco, A. M., & Conde‐Sieira, M. (2024) · Reviews in Fisheries Science & Aquaculture · doi:10.1080/23308249.2024.2374259 · Cited by 31 · see citing works
Protein-responsive gut hormone tachykinin directs food choice and impacts lifespan
Ahrentløv, N., Kubrak, O. I., Lassen, M., Malita, A., Koyama, T., Frederiksen, A. S., Sigvardsen, C. M., John, A., Madsen, P. S. M. S. M., Halberg, K. A., et al. (2025) · Nature Metabolism · doi:10.1038/s42255-025-01267-0 · Cited by 29 · see citing works
Protein Appetite Drives Macronutrient-Related Differences in Ventral Tegmental Area Neural Activity
Chiacchierini, G., Naneix, F., Peters, K. Z., Apergis‐Schoute, J., Snoeren, E. M. S., & McCutcheon, J. E. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.3082-20.2021 · Cited by 31 · see citing works
Comparative Proteomics Provides Insights into Metabolic Responses in Rat Liver to Isolated Soy and Meat Proteins
Song, S., Hooiveld, G. J. E. J., Zhang, W., Li, M., Zhao, F., Zhu, J. K., Xu, X., Müller, M. M., Li, C., & Zhou, G. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00922 · Cited by 28 · see citing works
A high-throughput assay for quantifying appetite and digestive dynamics
Jordi, J., Guggiana-Nilo, D., Soucy, E. R., Song, E. Y., Wee, C. L., & Engert, F. (2015) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00225.2015 · Cited by 25 · see citing works
Nutritional regulation of fibroblast growth factor 21: from macronutrients to bioactive dietary compounds
Pérez‐Martí, A., Sandoval, V., Marrero, P. F., Haro, D., & Relat, J. (2016) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2016-0034 · Cited by 24 · see citing works
Age-dependent effects of protein restriction on dopamine release
Naneix, F., Peters, K. Z., Young, A. M. J., & McCutcheon, J. E. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0783-z · Cited by 20 · see citing works
Obesity Impairs Oligopeptide/Amino Acid‐Induced Ghrelin Release and Smooth Muscle Contractions in the Human Proximal Stomach
Vancleef, L., Thijs, T., Baert, F., Ceulemans, L. J., Canovai, E., Wang, Q., Steensels, S., Segers, A., Farré, R., Pirenne, J., et al. (2018) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201700804 · Cited by 20 · see citing works
Relationship between FGF21 and drug or nondrug therapy of type 2 diabetes mellitus
Guo, C. Y., Zhao, L., Li, Y., Deng, X., & Yuan, G. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29879 · Cited by 21 · see citing works
Dietary carbohydrates impair the protective effect of protein restriction against diabetes in NZO mice used as a model of type 2 diabetes
Laeger, T., Castaño-Martinez, T., Werno, M. W., Japtok, L., Baumeier, C., Jonas, W., Kleuser, B., & Schürmann, A. (2018) · Diabetologia · doi:10.1007/s00125-018-4595-1 · Cited by 17 · see citing works
Plant-based meat analogues aggravated lipid accumulation by regulating lipid metabolism homeostasis in mice
Xie, Y., Cai, L., Huang, Z., Shan, K., Xu, X., Zhou, G., & Li, C. (2023) · Food Science and Human Wellness · doi:10.26599/fshw.2022.9250081 · Cited by 16 · see citing works
Isolation of Primary Mouse Hepatocytes for Nascent Protein Synthesis Analysis by Non-radioactive L-azidohomoalanine Labeling Method
Salem, E., Murakami, K., Takahashi, T., Bernhard, E., Borra, V. J., Bethi, M., & Nakamura, T. (2018) · Journal of Visualized Experiments · doi:10.3791/58323 · Cited by 16 · see citing works
Liver GCN2 controls hepatic FGF21 secretion and modulates whole body postprandial oxidation profile under a low-protein diet
Chalvon‐Demersay, T., Moro, J., Even, P. C., Chaumontet, C., Tomé, D., Avérous, J., Piedcoq, J., Gaudichon, C., Maurin, A., Fafournoux, P., et al. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00022.2019 · Cited by 16 · see citing works
Presowing seed treatment with glycine betaine confers NaCl tolerance in quinoa by modulating some physiological processes and antioxidant machinery
Maqsood, M. F., Shahbaz, M., Arfan, M., & Basra, S. M. A. (2020) · TURKISH JOURNAL OF BOTANY · doi:10.3906/bot-2009-13 · Cited by 15 · see citing works
Diet Protein Content and Individual Phenotype Affect Food Intake and Protein Appetence in Rats
Champeil‐Potokar, G., Crossouard, L., Jérôme, N., Ouali, C., Darcel, N., Davidenko, O., Rampin, O., Bombail, V., & Denis, I. (2021) · Journal of Nutrition · doi:10.1093/jn/nxaa455 · Cited by 15 · see citing works
Circulating levels of fibroblast growth factor 21 in gestational diabetes mellitus: a meta-analysis
Jia, J., Wei, W., Fan, Y., Liu, R., Shen, Y., Zhang, R., Yuan, G., & Zhou, H. (2020) · Endocrine Journal · doi:10.1507/endocrj.ej20-0481 · Cited by 14 · see citing works
Hypothalamic integration of nutrient sensing in fish
Soengas, J. L., Comesaña, S., Conde‐Sieira, M., & Blanco, A. M. (2024) · Journal of Experimental Biology · doi:10.1242/jeb.247410 · Cited by 13 · see citing works
The Protein Leverage Hypothesis: A 2019 Update for Obesity
Hill, C. M., & Morrison, C. D. (2019) · Obesity · doi:10.1002/oby.22568 · Cited by 13 · see citing works
Dynamic effects of dietary protein restriction on body weights, food consumption, and protein preference in C57BL /6J and Fgf21 ‐KO mice
Torres, F., Khan, M. S. H., Fernandez‐Kim, S. O., Spann, R. A., Albarado, D. C., Wagner, T. J., Morrison, C. D., & Soto, P. L. (2022) · Journal of the Experimental Analysis of Behavior · doi:10.1002/jeab.745 · Cited by 12 · see citing works
The Nutritional Applications of Quinoa Seeds
Okon, O. G. (2021) · Springer eBooks · doi:10.1007/978-981-16-3832-9_3 · Cited by 11 · see citing works
A novel amino acid signaling process governs glucose-6-phosphatase transcription
Fukushima, S., Nishi, H., Kumano, M., Yamanaka, D., Kataoka, N., Hakuno, F., & Takahashi, S. (2021) · iScience · doi:10.1016/j.isci.2021.102778 · Cited by 11 · see citing works
A machine-learning approach to optimize nutritional properties and organic wastes recycling efficiency conversed by black soldier fly (Hermetia illucens)
Feng, S., Ma, H., Wu, C., Arunprasanna, V., Liang, X., Zhang, D., & Chen, B. (2025) · Bioresource Technology · doi:10.1016/j.biortech.2025.132254 · Cited by 9 · see citing works
Research progress on the role of FGF21 in insulin resistance
Zhang, H., Zhu, R., Sun, Q., & Du, L. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1619462 · Cited by 10 · see citing works
Hunger and Satiety: Linking Mechanisms, Behavior and Evolution
Raubenheimer, D., & Simpson, S. J. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.20881-9 · Cited by 9 · see citing works
One-Pot Time-Induced Proteome Integral Solubility Alteration Assay for Automated and Sensitive Drug–Target Identification
Meng, Z., Saei, A. A., Lyu, H., Gaetani, M., & Zubarev, R. A. (2024) · Analytical Chemistry · doi:10.1021/acs.analchem.4c05127 · Cited by 8 · see citing works
Untargeted metabolomics as a tool to assess the impact of dietary approaches on pig gut health: a review
Chen, L., Canibe, N., Curtasu, M. V., & Hedemann, M. S. (2025) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-025-01238-1 · Cited by 8 · see citing works
Purinergic signaling in tanycytes and its contribution to nutritional sensing
Salgado, M., García, M. D. L. Á., & Sáez, J. C. (2021) · Purinergic Signalling · doi:10.1007/s11302-021-09791-w · Cited by 8 · see citing works
Unveiling the microbiota-mediated impact of different dietary proteins on post-digestive processes: A simulated in vitro approach
Ma, X., Fan, M., Hannachi, K., Qian, H., Li, Y., & Li, Y. (2024) · Food Research International · doi:10.1016/j.foodres.2024.115381 · Cited by 8 · see citing works
Role of liver AMPK and GCN2 kinases in the control of postprandial protein metabolism in response to mid-term high or low protein intake in mice
Chalvon‐Demersay, T., Gaudichon, C., Moro, J., Even, P. C., Khodorova, N., Piedcoq, J., Viollet, B., Avérous, J., Maurin, A., Tomé, D., et al. (2022) · European Journal of Nutrition · doi:10.1007/s00394-022-02983-z · Cited by 7 · see citing works
Fibroblast growth factor 21/extracellular signal-regulated kinase 1/2 pathway as a key link mediates the effects of low-protein diet on skeletal muscle fiber type transformation in pigs
Li, S., Liang, P., Wang, B., Chen, J., You, J., & Zou, T. (2025) · Animal nutrition · doi:10.1016/j.aninu.2025.03.001 · Cited by 6 · see citing works
Dietary protein restriction in rats leads to a rapid within-session preference for protein
Chiacchierini, G., Naneix, F., Apergis‐Schoute, J., & McCutcheon, J. E. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.114882 · Cited by 6 · see citing works
Protein-carbohydrate interaction effects on energy balance, FGF21, IGF-1, and hypothalamic gene expression in rats
Gehring, J., Azzout‐Marniche, D., Chaumontet, C., Piedcoq, J., Gaudichon, C., & Even, P. C. (2021) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00246.2021 · Cited by 6 · see citing works
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Barba, C., Benoit, B., Bres, É., Chanon, S., Vieille‐Marchiset, A., Pinteur, C., Pesenti, S., Glorieux, G., Picard, C., Fouque, D. P., et al. (2020) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfaa142.p0922 · Cited by 5 · see citing works
Allelopathic potential, nutritional qualities, and responses of Chenopodium quinoa (Willd.) to abiotic stress conditions-a review
SHAH, S., & KHAN, Y. (2022) · TURKISH JOURNAL OF BOTANY · doi:10.55730/1300-008x.2731 · Cited by 5 · see citing works
Stable isotope analysis of dietary arginine accrual and disposal efficiency in male rats fed diets with different protein content
Rotondo, F., Sanz, T., Fernández–Löpez, J., Alemany, M., & Remesar, X. (2016) · RSC Advances · doi:10.1039/c6ra11039h · Cited by 3 · see citing works
Structure and Composition of Fruits and Vegetables
Pandey, A. K., Shrivastava, A., Vashishth, R., & Chauhan, O. (2025) · Springer eBooks · doi:10.1007/978-981-96-8433-5_1 · Cited by 2 · see citing works
Protein appetite drives macronutrient-related differences in ventral tegmental area neural activity
(21471335), G. C., (8373876), F. N., Peters, K. Z., (7733501), J. A.-S., (21471338), E. S., & (8373882), J. M. (2025) · Figshare · Cited by 2 · see citing works
Meal-to-meal and day-to-day macronutrient variation in an ad libitum vending food paradigm
de Baca, T. C., Piaggi, P., Gluck, M. E., Krakoff, J. A., & Votruba, S. B. (2022) · Appetite · doi:10.1016/j.appet.2022.105944 · Cited by 2 · see citing works
Uses of multigrain for functional ice cream cone
Patil, U., & Singh, S. P. (2022) · International Journal of Horticulture and Food Science · doi:10.33545/26631067.2022.v4.i2c.121 · Cited by 1 · see citing works
Early-day Protein Intake Influences the Transition of Metabolic Health Phenotypes Among Adults with Obesity
Mazri, F. H., Jun, T. M., Al-Maswary, A. A. A., Kannan, D., Latif, N. H. A., Ramachandran, J., Keri, F. U. M., Besaiso, M., & Manaf, Z. A. (2024) · Current Research in Nutrition and Food Science Journal · doi:10.12944/crnfsj.12.3.22 · Cited by 1 · see citing works
Integrative unveiling of the effects of low dietary protein levels on grass carp (Ctenopharyngodon idella) fingerlings: Growth performance, antioxidant capacity, hepatic and intestinal function, and gut microbiota
Wan, J., Xu, X., Shao, J., Jiang, Q., Gu, X., Xia, A., & Li, J. (2025) · Aquaculture Reports · doi:10.1016/j.aqrep.2025.103044 · Cited by 1 · see citing works
Deoxycholic acid derived from the gut microbiota involved in the regulation of adaptive thermogenesis in response to dietary protein restriction in plateau pika
Shi, F., Yang, Z., Zhang, L., Zou, D., Yu, J., Guo, N., Ren, S., Tang, X., Gu, C. J., Xu, R., et al. (2025) · Microbiome · doi:10.1186/s40168-025-02233-4 · Cited by 1 · see citing works
Control of Food Intake by Dietary Amino Acids and Proteins
Fromentin, G., Darcel, N., Chaumontet, C., Even, P. C., Tomé, D., & Gaudichon, C. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802167-5.00016-5 · Cited by 1 · see citing works
Lipid Response to Amino Acid Starvation in Fat Cells: Role of FGF21
Pérez‐Martí, A., Marrero, P. F., Haro, D., & Relat, J. (2019) · Springer eBooks · doi:10.1007/978-3-319-55387-0_15 · Cited by 1 · see citing works
Protein appetite drives macronutrient-related differences in ventral tegmental area neural activityPreprint
Chiacchierini, G., Naneix, F., Peters, K. Z., Apergis-Schoute, J., Snoeren, E. M. S., & McCutcheon, J. E. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/542340 · Cited by 1 · see citing works
Age dependent effects of protein restriction on dopamine releasePreprint
Naneix, F., Peters, K. Z., Young, A. M. J., & McCutcheon, J. E. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.09.033985 · Cited by 1 · see citing works
Lipid Response to Amino Acid Starvation in Fat Cells: Role of FGF21
Pérez‐Martí, A., Marrero, P. F., Haro, D., & Relat, J. (2017) · Springer eBooks · doi:10.1007/978-3-319-40007-5_15-1
INFLUENCE OF LOW-PROTEIN DIET IN PREGNANT RATS ON MORPHOFUNCTIONAL STATE OF THE LIVER IN THEIR OFFSPRING
Kyznetsova, M. O. (2018) · Bulletin of Problems Biology and Medicine · doi:10.29254/2077-4214-2018-4-2-147-151-156
Experimental research of garden spinach extract as a potential anabolic medicinal product
Nykyforuk, A., Степанівна, Ф. Л., Lykhatskyі, P. H., & Пида, В. П. (2020) · Pharmacia · doi:10.3897/pharmacia.67.e56880
Development of a fibroblast growth factor 21 assay
Tamassia, G. V. (2017) · doi:10.32469/10355/62371
Food insecurity, macronutrient intake and patterns of eating in a sample of UK adultsPreprint
Shinwell, J., Melissa Bateson, B., Nettle, D., & Pepper, G. V. (2021) · doi:10.31219/osf.io/f9hnk
One-Pot Time-Induced Proteome Integral Solubility Alteration (OPTI-PISA) assay for automated and sensitive drug target identificationPreprint
Meng, Z., Saei, A. A., Lyu, H., Gaetani, M., & Zubarev, R. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.13.607299
Hunger and satiety: Linking mechanisms, behavior, ecology and evolution
Raubenheimer, D., & Simpson, S. J. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-29068-8.00088-x
Increased sucrose pellet consumption in mice with access to a protein-restricted diet, relative to mice with access to a non-restricted control diet, after prolonged (7 weeks) protein restriction
Larsson, C. M., Mercer, W. D., Inamdar, S. M., Connolly, N. E., Fisher, B. L., & Flippo, K. H. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.115132
Additional file 1 of The influence of developmental diet on reproduction and metabolism in Drosophila
Klepsatel, P., Knoblochová, D., Girish, T. N., Dircksen, H., & Gáliková, M. (2020) · Figshare · doi:10.6084/m9.figshare.12737523
Exposition périnatale à un régime maternel de quantité et de qualité variables en protéines chez le rat : préférences alimentaires et phénotype de la descendance du sevrage à l’âge adulte
Carlin, G. (2019) · doi:10.70675/f0e91e1ezfdeaz4a51zb3bazed2cda935d5f

Authors: Morrison, C. D., & Laeger, T.
Affiliations: Pennington Biomedical Research Center (US)
Corresponding author: Morrison, Christopher D.
ORCID: Morrison, Christopher D.
Laeger, Thomas
Venue: Trends in Endocrinology & Metabolism
Publisher: Elsevier BV
Published: 2015-05
Volume: 26
Issue: 5
Pages: 256-262
ISSN: 1043-2760 (ISSN-L)
DOI: 10.1016/j.tem.2015.02.008
PMC: PMC4416985
OpenAlex: W2068647583
Cited by: 106
References: 94
Citations by year: 2026: 5 · 2025: 12 · 2024: 6 · 2023: 2 · 2022: 6 · 2021: 9 · 2020: 16 · 2019: 13 · 2018: 11 · 2017: 8 · 2016: 15 · 2015: 3
FWCI: 1.34
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Endocrinology and Metabolism (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute for Health and Care Research
Deutsche Forschungsgemeinschaft
National Institutes of Health
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK081563, P30DK072476)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Health Sciences › Nursing › Nutrition and Dietetics › Nutrition, Health and Food Behavior
Health Sciences › Nursing › Nutrition and Dietetics › Biochemical Analysis and Sensing Techniques
Keywords: dietary protein, food intake regulation, energy metabolism, food choice, obesity, diabetes mellitus
MeSH terms: Amino Acids, Animals, Brain, Energy Intake, Diet, Dietary Proteins, Eating, Feeding Behavior, Food Preferences, Homeostasis, Metabolism, Obesity, Satiation

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