Physiological and pathophysiological implications of lipid sensing in the brain

Diabetes, Obesity and Metabolism

Volumn 16, Issue , 2014, Pages 49-55

  Picard, A ^a,b   Moulle V S ^a,b   Le Foll, C ^c,d   Cansell, C ^a,b   Veret J ^a,b   Coant, N ^a,b   Le Stunff, H ^a,b   Migrenne, S ^a,b   Luquet, S ^a,b   Cruciani Guglielmacci, C ^a,b   Levin, B E ^c,d   Magnan, C ^a,b  

^a Groupe Hospitalier Pitié Salpêtrière   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Energy balance; FAT CD36; Hypothalamus; Potassium channel

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CHLORIDE CHANNEL; FATTY ACID; LIPOPROTEIN LIPASE; NEUROPEPTIDE; NEUROTRANSMITTER; POTASSIUM CHANNEL; CD36 ANTIGEN; LPL PROTEIN, HUMAN; NERVE PROTEIN;

ARCUATE NUCLEUS; CELL SUBPOPULATION; FATTY ACID METABOLISM; FATTY ACID TRANSPORT; GLUCOSE HOMEOSTASIS; HUMAN; LIPID BRAIN LEVEL; MOLECULAR PATHOLOGY; NERVE CELL; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; THALAMUS VENTRAL NUCLEUS; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; BLOOD; CORPUS STRIATUM; CYTOLOGY; FEEDBACK SYSTEM; FOOD INTAKE; HIPPOCAMPUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; LIPID METABOLISM; METABOLISM;

ANIMALS; ANTIGENS, CD36; APPETITE REGULATION; CORPUS STRIATUM; FATTY ACIDS, NONESTERIFIED; FEEDBACK, PHYSIOLOGICAL; HIPPOCAMPUS; HUMANS; LIPID METABOLISM; LIPOPROTEIN LIPASE; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; NEURONS; ORGAN SPECIFICITY; VENTROMEDIAL HYPOTHALAMIC NUCLEUS;

EID: 84908506595     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12335     Document Type: Review

References (55)

1. Luquet S, Magnan C. The central nervous system at the core of the regulation of energy homeostasis. Front Biosci 2009; 1: 448-465.
2. Blouet C, Schwartz GJ. Hypothalamic nutrient sensing in the control of energy homeostasis. Behav Brain Res 2010; 209: 1-12.
3. Levin BE, Magnan C, Dunn-Meynell A, Le Foll C. Metabolic sensing and the brain: who, what, where, and how? Endocrinology 2011; 152: 2552-2557.
4. Oomura Y, Nakamura T, Sugimori M, Yamada Y. Effect of free fatty acid on the rat lateral hypothalamic neurons. Physiol Behav 1975; 14: 483-486.
5. Cruciani-Guglielmacci C, Hervalet A, Douared L et al. Beta oxidation in the brain is required for the effects of non-esterified fatty acids on glucose-induced insulin secretion in rats. Diabetologia 2004; 47: 2032-2038.
6. Lam TK, Pocai A, Gutierrez-Juarez R et al. Hypothalamic sensing of circulating fatty acids is required for glucose homeostasis. Nat Med 2005; 11: 320-327.
7. Le Foll C, Dunn-Meynell A, Musatov S, Magnan C, Levin BE. FAT/CD36: a major regulator of neuronal fatty acid sensing and energy homeostasis in rats and mice. Diabetes 2013; 62: 2709-2716.
8. Obici S, Feng Z, Morgan K, Stein D, Karkanias G, Rossetti L. Central administration of oleic acid inhibits glucose production and food intake. Diabetes 2002; 51: 271-275.
9. Migrenne S, Le Foll C, Levin BE, Magnan C. Brain lipid sensing and nervous control of energy balance. Diabetes Metab 2011; 37: 83-88.
10. Wang H, Astarita G, Taussig MD et al. Deficiency of lipoprotein lipase in neurons modifies the regulation of energy balance and leads to obesity. Cell Metab 2011; 13: 105-113.
11. Cansell C, Castel J, Denis RG et al. Dietary triglycerides act on mesolimbic structures to regulate the rewarding and motivational aspects of feeding. Mol Psychiatry 2014; DOI: 10.1038/mp.2014.31 [Epub ahead of print].
12. Velloso LA, Schwartz MW. Altered hypothalamic function in diet-induced obesity. Int J Obes 2011; 35: 1455-1465.
13. Yue JT, Lam TK. Lipid sensing and insulin resistance in the brain. Cell Metab 2012; 15: 646-655.
14. Edmond J. Essential polyunsaturated fatty acids and the barrier to the brain: the components of a model for transport. J Mol Neurosci 2001; 16: 181-193 discussion 215-121.
15. Watkins PA, Hamilton JA, Leaf A et al. Brain uptake and utilization of fatty acids: applications to peroxisomal biogenesis diseases. J Mol Neurosci 2001; 16: 87-92 discussion 151-157.
16. Rapoport SI, Chang MC, Spector AA. Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. J Lipid Res 2001; 42: 678-685.
17. Smith QR, Nagura H. Fatty acid uptake and incorporation in brain: studies with the perfusion model. J Mol Neurosci 2001; 16: 167-172 discussion 215-121.
18. Le Foll C, Irani BG, Magnan C, Dunn-Meynell AA, Levin BE. Characteristics and mechanisms of hypothalamic neuronal fatty acid sensing. Am J Physiol Regul Integr Comp Physiol 2009; 297: R655-664.
19. Escartin C, Pierre K, Colin A et al. Activation of astrocytes by CNTF induces metabolic plasticity and increases resistance to metabolic insults. J Neurosci 2007; 27: 7094-7104.
20. Picard A, Rouch C, Kassis N et al. Hippocampal lipoprotein lipase regulates energy balance in rodents. Mol Metab 2013; 3: 167-176.
21. Wang H, Eckel RH. Lipoprotein lipase in the brain and nervous system. Annu Rev Nutr 2012; 32: 147-160.
22. Wang H, Eckel RH. What are lipoproteins doing in the brain? Trends Endocrinol Metab 2014; 25: 8-14.
23. Obici S, Feng Z, Arduini A, Conti R, Rossetti L. Inhibition of hypothalamic carnitine palmitoyltransferase-1 decreases food intake and glucose production. Nat Med 2003; 9: 756-761.
24. Ross RA, Rossetti L, Lam TK, Schwartz GJ. Differential effects of hypothalamic long-chain fatty acid infusions on suppression of hepatic glucose production. Am J Physiol Endocrinol Metab 2010; 299: E633-639.
25. Auestad N, Korsak RA, Morrow JW, Edmond J. Fatty acid oxidation and ketogenesis by astrocytes in primary culture. J Neurochem 1991; 56: 1376-1386.
26. Magnan C, Collins S, Berthault MF et al. Lipid infusion lowers sympathetic nervous activity and leads to increased beta-cell responsiveness to glucose. J Clin Invest 1999; 103: 413-419.
27. Lam TK, Schwartz GJ, Rossetti L. Hypothalamic sensing of fatty acids. Nat Neurosci 2005; 8: 579-584.
28. Ruge T, Hodson L, Cheeseman J et al. Fasted to fed trafficking of fatty acids in human adipose tissue reveals a novel regulatory step for enhanced fat storage. J Clin Endocrinol Metab 2009; 94: 1781-1788.
29. Dowell P, Hu Z, Lane MD. Monitoring energy balance: metabolites of fatty acid synthesis as hypothalamic sensors. Annu Rev Biochem 2005; 74: 515-534.
30. Le Foll C, Dunn-Meynell A, Miziorko H, Levin B. Regulation of hypothalamic neuronal sensing and food intake by ketone bodies and fatty acids. Diabetes 2014; 63: 1259-1269.
31. Tewari KP, Malinowska DH, Sherry AM, Cuppoletti J. PKA and arachidonic acid activation of human recombinant ClC-2 chloride channels. Am J Physiol Cell Physiol 2000; 279: C40-50.
32. Honen BN, Saint DA, Laver DR. Suppression of calcium sparks in rat ventricular myocytes and direct inhibition of sheep cardiac RyR channels by EPA, DHA and oleic acid. J Membr Biol 2003; 196: 95-103.
33. Oishi K, Zheng B, Kuo JF. Inhibition of Na, K-ATPase and sodium pump by protein kinase C regulators sphingosine, lysophosphatidylcholine, and oleic acid. J Biol Chem 1990; 265: 70-75.
34. Jo YH, Su Y, Gutierrez-Juarez R, Chua S Jr. Oleic acid directly regulates POMC neuron excitability in the hypothalamus. J Neurophysiol 2009; 101: 2305-2316.
35. Wang R, Cruciani-Guglielmacci C, Migrenne S, Magnan C, Cotero VE, Routh VH. Effects of oleic acid on distinct populations of neurons in the hypothalamic arcuate nucleus are dependent on extracellular glucose levels. J Neurophysiol 2006; 95: 1491-1498.
36. Migrenne S, Cruciani-Guglielmacci C, Kang L et al. Fatty acid signaling in the hypothalamus and the neural control of insulin secretion. Diabetes 2006; 55(Suppl 2): S139-S144.
37. Proulx K, Cota D, Woods SC, Seeley RJ. Fatty acid synthase inhibitors modulate energy balance via mammalian target of rapamycin complex 1 signaling in the central nervous system. Diabetes 2008; 57: 3231-3238.
38. Proulx K, Seeley RJ. The regulation of energy balance by the central nervous system. Psychiatr Clin North Am 2005; 28: 25-38 vii.
39. Clegg DJ, Air EL, Woods SC, Seeley RJ. Eating elicited by orexin-a, but not melanin-concentrating hormone, is opioid mediated. Endocrinology 2002; 143: 2995-3000.
40. Tu Y, Thupari JN, Kim EK et al. C75 alters central and peripheral gene expression to reduce food intake and increase energy expenditure. Endocrinology 2005; 146: 486-493.
41. Ronnett GV, Kim EK, Landree LE, Tu Y. Fatty acid metabolism as a target for obesity treatment. Physiol Behav 2005; 85: 25-35.
42. Aja S, Landree LE, Kleman AM et al. Pharmacological stimulation of brain carnitine palmitoyl-transferase-1 decreases food intake and body weight. Am J Physiol Regul Integr Comp Physiol 2008; 294: R352-361.
43. Blazquez C, Woods A, de Ceballos ML, Carling D, Guzman M. The AMP-activated protein kinase is involved in the regulation of ketone body production by astrocytes. J Neurochem 1999; 73: 1674-1682.
44. Gaillard D, Laugerette F, Darcel N et al. The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse. FASEB J 2008; 22: 1458-1468.
45. Resh MD. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1999; 1451: 1-16.
46. Benoit SC, Kemp CJ, Elias CF et al. Palmitic acid mediates hypothalamic insulin resistance by altering PKC-theta subcellular localization in rodents. J Clin Invest 2009; 119: 2577-2589.
47. Ramos EJ, Romanova IV, Suzuki S et al. Effects of omega-3 fatty acids on orexigenic and anorexigenic modulators at the onset of anorexia. Brain Res 2005; 1046: 157-164.
48. Clement L, Cruciani-Guglielmacci C, Magnan C et al. Intracerebroventricular infusion of a triglyceride emulsion leads to both altered insulin secretion and hepatic glucose production in rats. Pflugers Arch 2002; 445: 375-380.
49. Levin BE, Triscari J, Sullivan AC. Altered sympathetic activity during development of diet-induced obesity in rat. Am J Physiol Regul Integr Comp Physiol 1983; 244: R347-355.
50. Young JB, Walgren MC. Differential effects of dietary fats on sympathetic nervous system activity in the rat. Metabolism 1994; 43: 51-60.
51. Cintra DE, Ropelle ER, Moraes JC et al. Unsaturated fatty acids revert diet-induced hypothalamic inflammation in obesity. PLoS One 2012; 7: e30571.
52. Karmi A, Iozzo P, Viljanen A et al. Increased brain fatty acid uptake in metabolic syndrome. Diabetes 2010; 59: 2171-2177.
53. Contreras C, López M. Ceramide sensing in the hippocampus: the lipostatic theory and Ockham's razor. Mol Metab 2013; 3: 90-91.
54. Elmquist JK, Marcus JN. Rethinking the central causes of diabetes. Nat Med 2003; 9: 645-647.
55. Le Stunff H, Coant N, Migrenne S, Magnan C. Targeting lipid sensing in the central nervous system: new therapy against the development of obesity and type 2 diabetes. Exp Opin Ther Targets 2013; 17: 545-555.