Coupling nutrient sensing to metabolic homoeostasis: The role of the mammalian target of rapamycin complex 1 pathway

Proceedings of the Nutrition Society

Volumn 71, Issue 4, 2012, Pages 502-510

  André, Caroline ^a,b   Cota, Daniela ^a,b  

^a INSTITUT FRANÇOIS MAGENDIE   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Hypothalamus; Mammalian target of rapamycin; Nutrient sensing; S6 kinase 1

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; AMINO ACID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FATTY ACID; GLUCOSE; INITIATION FACTOR 4E BINDING PROTEIN; INSULIN RECEPTOR SUBSTRATE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

BODY WEIGHT; CALCIUM CELL LEVEL; CELL DIFFERENTIATION; CELL SURVIVAL; CONFERENCE PAPER; DNA DAMAGE; DOWN REGULATION; ENERGY BALANCE; ENERGY EXPENDITURE; FATTY ACID METABOLISM; FOOD INTAKE; GENE EXPRESSION; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; GLYCEMIC CONTROL; HEMOSTASIS; HUMAN; HYPOTHALAMUS; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIFE EXTENSION; LIPID STORAGE; LIPOGENESIS; METABOLISM; MITOCHONDRIAL RESPIRATION; NEGATIVE FEEDBACK; NON INSULIN DEPENDENT DIABETES MELLITUS; NUTRIENT; OBESITY; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SCLEROSIS; SIGNAL TRANSDUCTION; TUBEROUS SCLEROSIS; WNT SIGNALING PATHWAY;

AMINO ACIDS; ANIMALS; DIET; ENERGY INTAKE; ENERGY METABOLISM; FATTY ACIDS; GLUCOSE; HOMEOSTASIS; HUMANS; HYPOTHALAMUS; METABOLIC DISEASES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

MAMMALIA;

EID: 84868288958     PISSN: 00296651     EISSN: 14752719     Source Type: Journal    
DOI: 10.1017/S0029665112000754     Document Type: Conference Paper

References (84)

1. Heitman J, Movva NR & Hall MN (1991) Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253, 905-909.
2. Sabatini DM, Erdjument-Bromage H, Lui M et al. (1994) RAFT1: A mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 78, 35-43.
3. Sarbassov DD, Ali SM, Sengupta S et al. (2006) Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22:159-168.
4. Laplante M & Sabatini DM (2009) mTOR signaling at a glance. J Cell Sci 122, 3589-3594.
5. Zoncu R, Efeyan A & Sabatini DM (2011) mTOR: From growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 12, 21-35.
6. Cota D, Proulx K, Smith KA et al. (2006) Hypothalamic mTOR signaling regulates food intake. Science 312, 927-930.
7. Cota D, Matter EK, Woods SC et al. (2008) The role of hypothalamic mammalian target of rapamycin complex 1 signaling in diet-induced obesity. J Neurosci 28, 7202-7208.
8. Ropelle ER, Pauli JR, Fernandes MF et al. (2008) A central role for neuronal AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) in high-protein diet-induced weight loss. Diabetes 57, 594-605.
9. Morton GJ, Cummings DE, Baskin DG et al. (2006) Central nervous system control of food intake and body weight. Nature 443, 289-295.
10. Schwartz MW, Woods SC, Porte D Jr et al. (2000) Central nervous system control of food intake. Nature 404, 661-671.
11. Plum L, Belgardt BF & Bruning JC (2006) Central insulin action in energy and glucose homeostasis. J Clin Invest 116, 1761-1766.
12. Hill JW, Williams KW, Ye C et al. (2008) Acute effects of leptin require PI3 K signaling in hypothalamic proopiomelanocortin neurons in mice. J Clin Invest 118, 1796-1805.
13. Inoki K, Li Y, Zhu T et al. (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4, 648-657.
14. Sarbassov DD, Guertin DA, Ali SM et al. (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101.
15. Ma L, Chen Z, Erdjument-Bromage H et al. (2005) Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 121, 179-193.
16. Inoki K, Ouyang H, Zhu T et al. (2006) TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126, 955-968.
17. Hardie DG (2007) AMP-activated/SNF1 protein kinases: Conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8, 774-785.
18. Inoki K, Zhu T & Guan KL (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115, 577-590.
19. Gwinn DM, Shackelford DB, Egan DF et al. (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30, 214-226.
20. Hara K, Yonezawa K, Weng QP et al. (1998) Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J Biol Chem 273, 14484-14494.
21. Nicklin P, Bergman P, Zhang B et al. (2009) Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 136, 521-534.
22. Gulati P, Gaspers LD, Dann SG et al. (2008) Amino acids activate mTOR complex 1 via Ca2 + /CaM signaling to hVps34. Cell Metab 7, 456-465.
23. Byfield MP, Murray JT, Backer JM (2005) hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem 280, 33076-33082.
24. Han JM, Jeong SJ, Park MC et al. (2012) Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell 149, 410-424.
25. Dennis PB, Jaeschke A, Saitoh M et al. (2001) Mammalian TOR: A homeostatic ATP sensor. Science 294, 1102-1105.
26. Duvel K, Yecies JL, Menon S et al. (2010) Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 39, 171-183.
27. Castaneda TR, Abplanalp W, Um SH et al. (2012) Metabolic control by S6 kinases depends on dietary lipids. PLoS One 7, e32631.
28. Howell JJ & Manning BD (2011) mTOR couples cellular nutrient sensing to organismal metabolic homeostasis. Trends Endocrinol Metab 22, 94-102.
29. Um SH, Frigerio F, Watanabe M et al. (2004) Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431, 200-205.
30. Laplante M & Sabatini DM (2009) An emerging role of mTOR in lipid biosynthesis. Curr Biol 19, R1046-1052.
31. Bates SH, Stearns WH, Dundon TA et al. (2003) STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature 421, 856-859.
32. Wegrzyn J, Potla R, Chwae YJ et al. (2009) Function of mitochondrial Stat3 in cellular respiration. Science 323, 793-797.
33. Cunningham JT, Rodgers JT, Arlow DH et al. (2007) mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 450, 736-740.
34. Bentzinger CF, Romanino K, Cloetta D et al. (2008) Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab 8, 411-424.
35. Laplante M & Sabatini DM (2012) mTOR Signaling in growth control and disease. Cell 149, 274-293.
36. Proud CG (2007) Amino acids and mTOR signalling in anabolic function. Biochem Soc Trans 35, 1187-1190.
37. Laviano A, Muscaritoli M, Cascino A et al. (2005) Branched-chain amino acids: The best compromise to achieve anabolism? Curr Opin Clin Nutr Metab Care 8, 408-414.
38. Weitzel LR, Sandoval PA, Mayles WJ et al. (2009) Performance-enhancing sports supplements: Role in critical care. Crit Care Med 37, S400-409.
39. Greer BK, Woodard JL, White JP et al. (2007) Branchedchain amino acid supplementation and indicators of muscle damage after endurance exercise. Int J Sport Nutr Exerc Metab 17, 595-607.
40. Shin AC, Zheng H & Berthoud HR (2009) An expanded view of energy homeostasis: Neural integration of metabolic, cognitive, and emotional drives to eat. Physiol Behav 97, 572-580.
41. Myers MG, Cowley MA & Munzberg H (2008) Mechanisms of leptin action and leptin resistance. Annu Rev Physiol 70, 537-556.
42. Morrison CD, Xi X, White CL et al. (2007) Amino acids inhibit Agrp gene expression via an mTOR-dependent mechanism. Am J Physiol Endocrinol Metab 293, E165-E171.
43. Blouet C, Jo YH, Li X & Schwartz GJ (2009) Mediobasal hypothalamic leucine sensing regulates food intake through activation of a hypothalamus-brainstem circuit. J Neurosci 29, 8302-8311.
44. Lynch CJ, Gern B, Lloyd C et al. (2006) Leucine in food mediates some of the postprandial rise in plasma leptin concentrations. Am J Physiol Endocrinol Metab 291, E621-E630.
45. Zhang Y, Guo K, LeBlanc RE et al. (2007) Increasing dietary leucine intake reduces diet-induced obesity and improves glucose and cholesterol metabolism in mice via multimechanisms. Diabetes 56, 1647-1654.
46. Guo K, Yu YH, Hou J et al. (2010) Chronic leucine supplementation improves glycemic control in etiologically distinct mouse models of obesity and diabetes mellitus. Nutr Metab (Lond) 7, 57.
47. Macotela Y, Emanuelli B, Bang AM et al. (2011) Dietary leucineYan environmental modifier of insulin resistance acting on multiple levels of metabolism. PLoS One 6, e21187.
48. Nairizi A, She P, Vary TC et al. (2009) Leucine supplementation of drinking water does not alter susceptibility to diet-induced obesity in mice. J Nutr 139, 715-719.
49. She P, Reid TM, Bronson SK et al. (2007) Disruption of BCATm in mice leads to increased energy expenditure associated with the activation of a futile protein turnover cycle. Cell Metab 6, 181-194.
50. Qin LQ, Xun P, Bujnowski D et al. (2011) Higher branchedchain amino acid intake is associated with a lower prevalence of being overweight or obese in middle-aged East Asian and Western adults. J Nutr 141, 249-254.
51. Newgard CB, An J, Bain JR et al. (2009) A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 9, 311-326.
52. Wang TJ, Larson MG, Vasan RS et al. (2011) Metabolite profiles and the risk of developing diabetes. Nat Med 17, 448-453.
53. D'Antona G, Ragni M, Cardile A et al. (2010) Branchedchain amino acid supplementation promotes survival and supports cardiac and skeletal muscle mitochondrial biogenesis in middle-aged mice. Cell Metab 12, 362-372.
54. Selman C, Tullet JM, Wieser D et al. (2009) Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 326, 140-144.
55. Harrison DE, Strong R, Sharp ZD et al. (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460, 392-395.
56. Sipula IJ, Brown NF & Perdomo G (2006) Rapamycinmediated inhibition of mammalian target of rapamycin in skeletal muscle cells reduces glucose utilization and increases fatty acid oxidation. Metabolism 55, 1637-1644.
57. Yue T, Yin J, Li F et al. (2010) High glucose induces differentiation and adipogenesis in porcine muscle satellite cells via mTOR. BMB Rep 43, 140-145.
58. Patel J, Wang X & Proud CG (2001) Glucose exerts a permissive effect on the regulation of the initiation factor 4E binding protein 4E-BP1. Biochem J 358, 497-503.
59. Buller CL, Loberg RD, Fan MH et al. (2008) A GSK-3/TSC2/mTOR pathway regulates glucose uptake and GLUT1 glucose transporter expression. Am J Physiol Cell Physiol 295, C836-C843.
60. McDaniel ML, Marshall CA, Pappan KL et al. (2002) Metabolic and autocrine regulation of the mammalian target of rapamycin by pancreatic beta-cells. Diabetes 51, 2877-2885.
61. Fraenkel M, Ketzinel-Gilad M, Ariav Y et al. (2008) mTOR inhibition by rapamycin prevents beta-cell adaptation to hyperglycemia and exacerbates the metabolic state in type 2 diabetes. Diabetes 57, 945-957.
62. Zahr E, Molano RD, Pileggi A et al. (2008) Rapamycin impairs beta-cell proliferation in vivo. Transplant Proc 40, 436-437.
63. Rachdi L, Balcazar N, Osorio-Duque F et al. (2008) Disruption of Tsc2 in pancreatic beta cells induces beta cell mass expansion and improved glucose tolerance in a TORC1-dependent manner. Proc Natl Acad Sci USA 105, 9250-9255.
64. Fu A, Ng AC, Depatie C et al. (2009) Loss of Lkb1 in adult beta cells increases beta cell mass and enhances glucose tolerance in mice. Cell Metab 10, 285-295.
65. Zhang H, Zhang G, Gonzalez FJ et al. (2011) Hypoxiainducible factor directs POMC gene to mediate hypothalamic glucose sensing and energy balance regulation. PLoS Biol 9, e1001112.
66. Parton LE, Ye CP, Coppari R et al. (2007) Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity. Nature 449, 228-232.
67. Rivas DA, Yaspelkis BB 3rd, Hawley JA et al. (2009) Lipid-induced mTOR activation in rat skeletal muscle reversed by exercise and 50-aminoimidazole-4- carboxamide-1-beta-D-ribofuranoside. J Endocrinol 202, 441-451.
68. Mordier S & Iynedjian PB (2007) Activation of mammalian target of rapamycin complex 1 and insulin resistance induced by palmitate in hepatocytes. Biochem Biophys Res Commun 362, 206-211.
69. Wang X, Yu W, Nawaz A et al. (2010) Palmitate induced insulin resistance by PKCtheta-dependent activation of mTOR/S6 K pathway in C2C12 myotubes. Exp Clin Endocrinol Diabetes 118, 657-661.
70. Carnevalli LS, Masuda K, Frigerio F et al. (2010) S6K1 plays a critical role in early adipocyte differentiation. Dev Cell 18, 763-774.
71. Cota D, Proulx K & Seeley RJ (2007) The role of CNS fuel sensing in energy and glucose regulation. Gastroenterology 132, 2158-2168.
72. Sokoloff L (1977) Relation between physiological function and energy metabolism in the central nervous system. J Neurochem 29, 13-26.
73. Loftus TM, Jaworsky DE, Frehywot GL et al. (2000) Reduced food intake and body weight in mice treated with fatty acid synthase inhibitors. Science 288, 2379-2381.
74. Lam TK, Schwartz GJ & Rossetti L (2005) Hypothalamic sensing of fatty acids. Nat Neurosci 8, 579-584.
75. Wortman MD, Clegg DJ, D'Alessio D et al. (2003) C75 inhibits food intake by increasing CNS glucose metabolism. Nat Med 9, 483-485.
76. Lopez M, Lage R, Saha AK et al. (2008) Hypothalamic fatty acid metabolism mediates the orexigenic action of ghrelin. Cell Metab 7, 389-399.
77. Minokoshi Y, Alquier T, Furukawa N et al. (2004) AMPkinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428, 569-574.
78. Gao S, Kinzig KP, Aja S et al. (2007) Leptin activates hypothalamic acetyl-CoA carboxylase to inhibit food intake. Proc Natl Acad Sci USA 104, 17358-17363.
79. Proulx K, Cota D, Woods SC et al. (2008) Fatty acid synthase inhibitors modulate energy balance via mammalian target of rapamycin complex 1 signaling in the central nervous system. Diabetes 57, 3231-3238.
80. Khamzina L, Veilleux A, Bergeron S et al. (2005) Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: Possible involvement in obesity-linked insulin resistance. Endocrinology 146, 1473-1481.
81. Lamming DW, Ye L, Katajisto P et al. (2012) Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 335, 1638-1643.
82. Deldicque L, Cani PD, Philp A et al. (2010) The unfolded protein response is activated in skeletal muscle by highfat feeding: Potential role in the downregulation of protein synthesis. Am J Physiol Endocrinol Metab 299, E695-E705.
83. Anderson SR, Gilge DA, Steiber AL et al. (2008) Dietinduced obesity alters protein synthesis: Tissuespecific effects in fasted versus fed mice. Metabolism 57, 347-354.
84. Reed AS, Unger EK, Olofsson LE et al. (2010) Functional role of suppressor of cytokine signaling 3 upregulation in hypothalamic leptin resistance and long-term energy homeostasis. Diabetes 59, 894-906.