A role for astrocytes in the central control of metabolism

Neuroendocrinology

Volumn 93, Issue 3, 2011, Pages 143-149

  Yi, Chun Xia ^a   Habegger, Kirk M ^a   Chowen, Julie A ^c   Stern, Javier ^b   Tschöp, Matthias H ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c HOSPITAL INFANTIL UNIVERSITARIO NIÑO JESÚS   (Spain)

Author keywords

Astrogliosis; Blood brain barrier; Ca2+; Free fatty acid; Ketone body; Microglia

Indexed keywords

FATTY ACID; GLUCOSE; KETONE BODY; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA;

ASTROCYTE; ASTROCYTOSIS; BRAIN; BRAIN TISSUE; ENERGY RESOURCE; LIPID DIET; LIPID METABOLISM; METABOLIC REGULATION; METABOLISM; NERVE CELL; NEUROENDOCRINE SYSTEM; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW;

ANIMALS; ASTROCYTES; ENERGY INTAKE; ENERGY METABOLISM; HUMANS; NEURONS; OBESITY; SIGNAL TRANSDUCTION;

EID: 79953737147     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000324888     Document Type: Review

References (65)

1. Banks WA: Blood-brain barrier as a regulatory interface. Forum Nutr 2010;63:102-110.
2. Haydon PG, Carmignoto G: Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 2006;86:1009-1031. (Pubitemid 44033387)
3. Filosa JA, Blanco VM: Neurovascular coupling in the mammalian brain. Exp Physiol 2007;92:641-646. (Pubitemid 47024943)
4. Fields RD, Stevens-Graham B: New insights into neuron-glia communication. Science 2002;298:556-562.
5. Horvath TL, Sarman B, Garcia-Caceres C, Enriori PJ, Sotonyi P, Shanabrough M, Borok E, Argente J, Chowen JA, Perez-Tilve D, Pfluger PT, Bronneke HS, Levin BE, Diano S, Cowley MA, Tschöp MH: Synaptic input organization of the melanocortin system predicts diet-induced hypothalamic reactive gliosis and obesity. Proc Natl Acad Sci USA 2010;107:14875-14880.
6. Hawkins RA, Williamson DH, Krebs HA: Ketone-body utilization by adult and suckling rat brain in vivo. Biochem J 1971;122:13-18.
7. Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill GF Jr: Brain metabolism during fasting. J Clin Invest 1967;46:1589-1595.
8. Robinson AM, Williamson DH: Physiological roles of ketone bodies as substrates and signals in mammalian tissues. Physiol Rev 1980;60:143-187. (Pubitemid 10104513)
9. Gjedde A, Crone C: Induction processes in blood-brain transfer of ketone bodies during starvation. Am J Physiol 1975;229:1165-1169.
10. Zivin JA, Snarr JF: Glucose and D (-)-3-hydroxybutyrate uptake by isolated perfused rat brain. J Appl Physiol 1972;32:664-668.
11. Lopes-Cardozo M, Larsson OM, Schousboe A: Acetoacetate and glucose as lipid precursors and energy substrates in primary cultures of astrocytes and neurons from mouse cerebral cortex. J Neurochem 1986;46:773-778. (Pubitemid 16114391)
12. 14C]palmitate between oxidative and synthetic pathways. J Neurochem 1987;49:1507-1514.
13. Guzman M, Blazquez C: Is there an astrocyte-neuron ketone body shuttle? Trends Endocrinol Metab 2001;12:169-173.
14. Staub F, Winkler A, Peters J, Goerke U, Kempski O, Baethmann A: Clearance and metabolism of arachidonic acid by C6 glioma cells and astrocytes. Neurochem Res 1995;20:1449-1456. (Pubitemid 26029136)
15. Edmond J: Energy metabolism in developing brain cells. Can J Physiol Pharmacol 1992;70(suppl):S118-S129.
16. Cullingford TE, Dolphin CT, Bhakoo KK, Peuchen S, Canevari L, Clark JB: Molecular cloning of rat mitochondrial 3-hydroxy-3-methylglutaryl-CoA lyase and detection of the corresponding mRNA and of those encoding the remaining enzymes comprising the ketogenic 3-hydroxy-3-methylglutaryl-CoA cycle in central nervous system of suckling rat. Biochem J 1998;329:373-381.
17. Sunny NE, Satapati S, Fu X, He T, Mehdibeigi R, Spring-Robinson C, Duarte J, Potthoff MJ, Browning JD, Burgess SC: Progressive adaptation of hepatic ketogenesis in mice fed a high-fat diet. Am J Physiol Endocrinol Metab 2010;298:E1226-E1235.
18. Moore TJ, Lione AP, Sugden MC, Regen DM: Beta-hydroxybutyrate transport in rat brain: developmental and dietary modulations. Am J Physiol 1976;230:619-630.
19. Melo TM, Nehlig A, Sonnewald U: Neuronal-glial interactions in rats fed a ketogenic diet. Neurochem Int 2006;48:498-507.
20. Hasselbalch SG, Knudsen GM, Jakobsen J, Hageman LP, Holm S, Paulson OB: Bloodbrain barrier permeability of glucose and ketone bodies during short-term starvation in humans. Am J Physiol 1995;268:E1161-E1166.
21. Crane PD, Pardridge WM, Braun LD, Oldendorf WH: Two-day starvation does not alter the kinetics of blood-brain barrier transport and phosphorylation of glucose in rat brain. J Cereb Blood Flow Metab 1985;5:40-46. (Pubitemid 15146557)
22. Redies C, Hoffer LJ, Beil C, Marliss EB, Evans AC, Lariviere F, Marrett S, Meyer E, Diksic M, Gjedde A: Generalized decrease in brain glucose metabolism during fasting in humans studied by PET. Am J Physiol 1989;256:E805-E810.
23. Halestrap AP, Price NT: The proton-linked monocarboxylate transporter family: structure, function and regulation. Biochem J 1999;343:281-299. (Pubitemid 29511759)
24. Broer S, Rahman B, Pellegri G, Pellerin L, Martin JL, Verleysdonk S, Hamprecht B, Magistretti PJ: Comparison of lactate transport in astroglial cells and monocarboxylate transporter 1 (MCT-1) expressing Xenopus laevis oocytes. Expression of two different monocarboxylate transporters in astroglial cells and neurons. J Biol Chem 1997;272:30096-30102.
25. Lin T, Koustova E, Chen H, Rhee PM, Kirkpatrick J, Alam HB: Energy substrate-supplemented resuscitation affects brain monocarboxylate transporter levels and gliosis in a rat model of hemorrhagic shock. J Trauma 2005;59:1191-1202. (Pubitemid 43060978)
26. Leino RL, Gerhart DZ, Duelli R, Enerson BE, Drewes LR: Diet-induced ketosis increases monocarboxylate transporter (MCT-1) levels in rat brain. Neurochem Int 2001;38:519-527. (Pubitemid 32204362)
27. Schachtrup C, Ryu JK, Helmrick MJ, Vagena E, Galanakis DK, Degen JL, Margolis RU, Akassoglou K: Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-β after vascular damage. J Neurosci 2010;30:5843-5854.
28. 1-acid glycoprotein in obese women (in Spanish). Nutr Hosp 2010;25:72-79.
29. Ciofi P: The arcuate nucleus as a circumventricular organ in the mouse. Neurosci Lett 2010.
30. Ciofi P, Garret M, Lapirot O, Lafon P, Loyens A, Prevot V, Levine JE: Brain-endocrine interactions: a microvascular route in the mediobasal hypothalamus. Endocrinology 2009;150:5509-5519.
31. Mullier A, Bouret SG, Prevot V, Dehouck B: Differential distribution of tight junction proteins suggests a role for tanycytes in blood-hypothalamus barrier regulation in the adult mouse brain. J Comp Neurol 2010;518:943-962.
32. Cottrell GT, Ferguson AV: Sensory circumventricular organs: central roles in integrated autonomic regulation. Regul Pept 2004;117:11-23. (Pubitemid 37548394)
33. Schwartz MW, Seeley RJ, Campfield LA, Burn P, Baskin DG: Identification of targets of leptin action in rat hypothalamus. J Clin Invest 1996;98:1101-1106. (Pubitemid 26299921)
34. Unger J, McNeill TH, Moxley RT III, White M, Moss A, Livingston JN: Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience 1989;31:143-157. (Pubitemid 19209704)
35. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, Oldstone MB, Mucke L: Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin-6. Proc Natl Acad Sci USA 1993;90:10061-10065. (Pubitemid 23328251)
36. Hidalgo J, Florit S, Giralt M, Ferrer B, Keller C, Pilegaard H: Transgenic mice with astrocyte-targeted production of interleukin-6 are resistant to high-fat diet-induced increases in body weight and body fat. Brain Behav Immun 2010;24:119-126.
37. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ: Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 1990;247:470-473.
38. Parpura V, Zorec R: Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 2010;63:83-92.
39. Park JB, Skalska S, Stern JE: Characterization of a novel tonic γ-aminobutyric acid A receptor-mediated inhibition in magnocellular neurosecretory neurons and its modulation by glia. Endocrinology 2006;147:3746-3760. (Pubitemid 44079379)
40. Park JB, Jo JY, Zheng H, Patel KP, Stern JE: Regulation of tonic GABA inhibitory function, presympathetic neuronal activity and sympathetic outflow from the paraventricular nucleus by astroglial GABA transporters. J Physiol 2009;587:4645-4660.
41. Berger J, Moller DE: The mechanisms of action of PPARs. Annu Rev Med 2002;53:409-435. (Pubitemid 34177889)
42. Peters JM, Hennuyer N, Staels B, Fruchart JC, Fievet C, Gonzalez FJ, Auwerx J: Alterations in lipoprotein metabolism in peroxisome proliferator-activated receptor α-deficient mice. J Biol Chem 1997;272:27307-27312. (Pubitemid 27452695)
43. Konig B, Koch A, Giggel K, Dordschbal B, Eder K, Stangl GI: Monocarboxylate transporter-1 is up-regulated by PPARα. Biochim Biophys Acta 2008;1780:899-904.
44. Mahley RW, Innerarity TL, Rall SC Jr, Weisgraber KH: Plasma lipoproteins: apolipoprotein structure and function. J Lipid Res 1984;25:1277-1294. (Pubitemid 15150638)
45. Weisgraber KH: Apolipoprotein E: structure-function relationships. Adv Protein Chem 1994;45:249-302.
46. Haft DE, Roheim PS, White A, Eder HA: Plasma lipoprotein metabolism in perfused rat livers. I. Protein synthesis and entry into the plasma. J Clin Invest 1962;41:842-849.
47. Boyles JK, Pitas RE, Wilson E, Mahley RW, Taylor JM: Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J Clin Invest 1985;76:1501-1513. (Pubitemid 16193568)
48. Shen L, Tso P, Woods SC, Clegg DJ, Barber KL, Carey K, Liu M: Brain apolipoprotein E: an important regulator of food intake in rats. Diabetes 2008;57:2092-2098.
49. Shen L, Tso P, Wang DQ, Woods SC, Davidson WS, Sakai R, Liu M: Up-regulation of apolipoprotein E by leptin in the hypothalamus of mice and rats. Physiol Behav 2009;98:223-228.
50. Young JK: Anatomical relationship between specialized astrocytes and leptin-sensitive neurones. J Anat 2002;201:85-90.
51. Leshan RL, Louis GW, Jo YH, Rhodes CJ, Munzberg H, Myers MG Jr: Direct innervation of GnRH neurons by metabolic- and sexual odorant-sensing leptin receptor neurons in the hypothalamic ventral premammillary nucleus. J Neurosci 2009;29:3138-3147.
52. Hsuchou H, Pan W, Barnes MJ, Kastin AJ: Leptin receptor mRNA in rat brain astrocytes. Peptides 2009;30:2275-2280.
53. Hsuchou H, He Y, Kastin AJ, Tu H, Markadakis EN, Rogers RC, Fossier PB, Pan W: Obesity induces functional astrocytic leptin receptors in hypothalamus. Brain 2009;132:889-902.
54. Lee MY, Deller T, Kirsch M, Frotscher M, Hofmann HD: Differential regulation of ciliary neurotrophic factor (CNTF) and CNTF receptor α expression in astrocytes and neurons of the fascia dentata after entorhinal cortex lesion. J Neurosci 1997;17:1137-1146. (Pubitemid 27043971)
55. Lanz TV, Ding Z, Ho PP, Luo J, Agrawal AN, Srinagesh H, Axtell R, Zhang H, Platten M, Wyss-Coray T, Steinman L: Angiotensin II sustains brain inflammation in mice via TGF-β. J Clin Invest 2010;120:2782-2794.
56. Steinberg GR, Watt MJ, Fam BC, Proietto J, Andrikopoulos S, Allen AM, Febbraio MA, Kemp BE: Ciliary neurotrophic factor suppresses hypothalamic AMP-kinase signaling in leptin-resistant obese mice. Endocrinology 2006;147:3906-3914. (Pubitemid 44079396)
57. Watt MJ, Dzamko N, Thomas WG, Rose-John S, Ernst M, Carling D, Kemp BE, Febbraio MA, Steinberg GR: CNTF reverses obesity-induced insulin resistance by activating skeletal muscle AMPK. Nat Med 2006;12:541-548.
58. Levin BE, Dunn-Meynell AA, Routh VH: Brain glucose sensing and body energy homeostasis: role in obesity and diabetes. Am J Physiol 1999;276:R1223-R1231. (Pubitemid 29249643)
59. Ngarmukos C, Baur EL, Kumagai AK: Colocalization of GLUT1 and GLUT4 in the blood-brain barrier of the rat ventromedial hypothalamus. Brain Res 2001;900:1-8. (Pubitemid 32452259)
60. Wang R, Liu X, Hentges ST, Dunn-Meynell AA, Levin BE, Wang W, Routh VH: The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feeding-relevant peptides. Diabetes 2004;53:1959-1965. (Pubitemid 38970742)
61. Wang X, Takano T, Nedergaard M: Astrocytic calcium signaling: mechanism and implications for functional brain imaging. Methods Mol Biol 2009;489:93-109.
62. 2+ oscillations: involvement of ATP release in astrocytes. FEBS J 2010;277:286-292.
63. Pistell PJ, Morrison CD, Gupta S, Knight AG, Keller JN, Ingram DK, Bruce-Keller AJ: Cognitive impairment following high-fat diet consumption is associated with brain inflammation. J Neuroimmunol 2010;219:25-32.
64. Zhang Y, Barres BA: Astrocyte heterogeneity: an underappreciated topic in neurobiology. Curr Opin Neurobiol 2010;20:588-594.
65. Middeldorp J, van den Berge SA, Aronica E, Speijer D, Hol EM: Specific human astrocyte subtype revealed by affinity purified GFAP antibody;unpurified serum cross-reacts with neurofilament-L in Alzheimer. PLoS ONE 2009;4:e7663.