Astrocytic Insulin Signaling Couples Brain Glucose Uptake with Nutrient Availability

Cell

Volumn 166, Issue 4, 2016, Pages 867-880

  García Cáceres, Cristina ^a,b   Quarta, Carmelo ^a,b   Varela, Luis ^c   Gao, Yuanqing ^a,b   Gruber, Tim ^a,b   Legutko, Beata ^a,b   Jastroch, Martin ^a,b   Johansson, Pia ^a,d   Ninkovic, Jovica ^a,d   Yi, Chun Xia ^a,b   Le Thuc, Ophelia ^a,b   Szigeti Buck, Klara ^c   Cai, Weikang ^e   Meyer, Carola W ^a,b   Pfluger, Paul T ^a,b   Fernandez, Ana M ^f   Luquet, Serge ^g   Woods, Stephen C ^h   Torres Alemán, Ignacio ^f   Kahn, C Ronald ^e   Götz, Magdalena ^a,d   Horvath, Tamas L ^c   Tschöp, Matthias H ^a,b   more..

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MUNICH   (Germany)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f INSTITUTO CAJAL   (Spain)

^g UNIVERSITÉ PARIS DESCARTES   (France)

^h UNIVERSITY OF CINCINNATI   (United States)

Author keywords

astrocytes; glucose uptake; hypothalamus; insulin receptor

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; INSULIN; INSULIN RECEPTOR; PROOPIOMELANOCORTIN; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; GLUTAMATE TRANSPORTER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN MITOCHONDRION; CELL ACTIVATION; CELL FUNCTION; CELL STRUCTURE; CEREBROSPINAL FLUID ANALYSIS; CONTROLLED STUDY; GENE INACTIVATION; GLUCOSE BRAIN LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HYPOTHALAMUS; IN VITRO STUDY; IN VIVO STUDY; MALE; METABOLIC REGULATION; MOUSE; NERVE CELL NETWORK; NONHUMAN; NUTRIENT AVAILABILITY; PERINATAL PERIOD; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; ENDOPLASMIC RETICULUM; GENETICS; HOMEOSTASIS; METABOLISM; MITOCHONDRION; NERVE CELL;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; ENDOPLASMIC RETICULUM; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; HOMEOSTASIS; HYPOTHALAMUS; INSULIN; MICE; MITOCHONDRIA; NEURONS; PRO-OPIOMELANOCORTIN; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 84981295660     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.07.028     Document Type: Article

References (40)

1. Abbott, N.J., Rönnbäck, L., Hansson, E., Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7 (2006), 41–53.
2. Alvarez, J.I., Katayama, T., Prat, A., Glial influence on the blood brain barrier. Glia 61 (2013), 1939–1958.
3. Armulik, A., Genové, G., Mäe, M., Nisancioglu, M.H., Wallgard, E., Niaudet, C., He, L., Norlin, J., Lindblom, P., Strittmatter, K., et al. Pericytes regulate the blood-brain barrier. Nature 468 (2010), 557–561.
4. Baltzer, C., Tiefenböck, S.K., Frei, C., Mitochondria in response to nutrients and nutrient-sensitive pathways. Mitochondrion 10 (2010), 589–597.
5. Barros, L.F., Bittner, C.X., Loaiza, A., Porras, O.H., A quantitative overview of glucose dynamics in the gliovascular unit. Glia 55 (2007), 1222–1237.
6. Brown, A.M., Ransom, B.R., Astrocyte glycogen and brain energy metabolism. Glia 55 (2007), 1263–1271.
7. Brüning, J.C., Gautam, D., Burks, D.J., Gillette, J., Schubert, M., Orban, P.C., Klein, R., Krone, W., Müller-Wieland, D., Kahn, C.R., Role of brain insulin receptor in control of body weight and reproduction. Science 289 (2000), 2122–2125.
8. Buffo, A., Rite, I., Tripathi, P., Lepier, A., Colak, D., Horn, A.P., Mori, T., Götz, M., Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc. Natl. Acad. Sci. USA 105 (2008), 3581–3586.
9. Cranston, I., Marsden, P., Matyka, K., Evans, M., Lomas, J., Sonksen, P., Maisey, M., Amiel, S.A., Regional differences in cerebral blood flow and glucose utilization in diabetic man: the effect of insulin. J. Cereb. Blood Flow Metab. 18 (1998), 130–140.
10. De Felice, F.G., Ferreira, S.T., Inflammation, defective insulin signaling, and mitochondrial dysfunction as common molecular denominators connecting type 2 diabetes to Alzheimer disease. Diabetes 63 (2014), 2262–2272.
11. Dietrich, M.O., Liu, Z.W., Horvath, T.L., Mitochondrial dynamics controlled by mitofusins regulate Agrp neuronal activity and diet-induced obesity. Cell 155 (2013), 188–199.
12. Ferreira, S.T., Clarke, J.R., Bomfim, T.R., De Felice, F.G., Inflammation, defective insulin signaling, and neuronal dysfunction in Alzheimer's disease. Alzheimers Dement. 10:1, Suppl (2014), S76–S83.
13. Frank, H.J., Pardridge, W.M., Morris, W.L., Rosenfeld, R.G., Choi, T.B., Binding and internalization of insulin and insulin-like growth factors by isolated brain microvessels. Diabetes 35 (1986), 654–661.
14. Fuente-Martín, E., García-Cáceres, C., Granado, M., de Ceballos, M.L., Sánchez-Garrido, M.A., Sarman, B., Liu, Z.W., Dietrich, M.O., Tena-Sempere, M., Argente-Arizón, P., et al. Leptin regulates glutamate and glucose transporters in hypothalamic astrocytes. J. Clin. Invest. 122 (2012), 3900–3913.
15. Ganat, Y.M., Silbereis, J., Cave, C., Ngu, H., Anderson, G.M., Ohkubo, Y., Ment, L.R., Vaccarino, F.M., Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J. Neurosci. 26 (2006), 8609–8621.
16. García-Cáceres, C., Fuente-Martín, E., Argente, J., Chowen, J.A., Emerging role of glial cells in the control of body weight. Mol. Metab. 1 (2012), 37–46.
17. Goldman, S., Glia as neural progenitor cells. Trends Neurosci. 26 (2003), 590–596.
18. Hasselbalch, S.G., Knudsen, G.M., Videbaek, C., Pinborg, L.H., Schmidt, J.F., Holm, S., Paulson, O.B., No effect of insulin on glucose blood-brain barrier transport and cerebral metabolism in humans. Diabetes 48 (1999), 1915–1921.
19. Havrankova, J., Roth, J., Brownstein, M., Insulin receptors are widely distributed in the central nervous system of the rat. Nature 272 (1978), 827–829.
20. Kim, J.G., Suyama, S., Koch, M., Jin, S., Argente-Arizon, P., Argente, J., Liu, Z.W., Zimmer, M.R., Jeong, J.K., Szigeti-Buck, K., et al. Leptin signaling in astrocytes regulates hypothalamic neuronal circuits and feeding. Nat. Neurosci. 17 (2014), 908–910.
21. Kleinridders, A., Ferris, H.A., Cai, W., Kahn, C.R., Insulin action in brain regulates systemic metabolism and brain function. Diabetes 63 (2014), 2232–2243.
22. Klepper, J., Voit, T., Facilitated glucose transporter protein type 1 (GLUT1) deficiency syndrome: impaired glucose transport into brain– a review. Eur. J. Pediatr. 161 (2002), 295–304.
23. Koch, L., Wunderlich, F.T., Seibler, J., Könner, A.C., Hampel, B., Irlenbusch, S., Brabant, G., Kahn, C.R., Schwenk, F., Brüning, J.C., Central insulin action regulates peripheral glucose and fat metabolism in mice. J. Clin. Invest. 118 (2008), 2132–2147.
24. Magistretti, P.J., Pellerin, L., Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354 (1999), 1155–1163.
25. Mandl, J., Mészáros, T., Bánhegyi, G., Hunyady, L., Csala, M., Endoplasmic reticulum: nutrient sensor in physiology and pathology. Trends Endocrinol. Metab. 20 (2009), 194–201.
26. McMinn, J.E., Liu, S.M., Liu, H., Dragatsis, I., Dietrich, P., Ludwig, T., Boozer, C.N., Chua, S.C. Jr., Neuronal deletion of Lepr elicits diabesity in mice without affecting cold tolerance or fertility. Am. J. Physiol. Endocrinol. Metab. 289 (2005), E403–E411.
27. Mori, T., Tanaka, K., Buffo, A., Wurst, W., Kühn, R., Götz, M., Inducible gene deletion in astroglia and radial glia–a valuable tool for functional and lineage analysis. Glia 54 (2006), 21–34.
28. Nedergaard, M., Ransom, B., Goldman, S.A., New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 26 (2003), 523–530.
29. Nolte, C., Matyash, M., Pivneva, T., Schipke, C.G., Ohlemeyer, C., Hanisch, U.K., Kirchhoff, F., Kettenmann, H., GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33 (2001), 72–86.
30. Pinto, S., Roseberry, A.G., Liu, H., Diano, S., Shanabrough, M., Cai, X., Friedman, J.M., Horvath, T.L., Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304 (2004), 110–115.
31. Schneeberger, M., Dietrich, M.O., Sebastián, D., Imbernón, M., Castaño, C., Garcia, A., Esteban, Y., Gonzalez-Franquesa, A., Rodríguez, I.C., Bortolozzi, A., et al. Mitofusin 2 in POMC neurons connects ER stress with leptin resistance and energy imbalance. Cell 155 (2013), 172–187.
32. Simpson, I.A., Appel, N.M., Hokari, M., Oki, J., Holman, G.D., Maher, F., Koehler-Stec, E.M., Vannucci, S.J., Smith, Q.R., Blood-brain barrier glucose transporter: effects of hypo- and hyperglycemia revisited. J. Neurochem. 72 (1999), 238–247.
33. Simpson, I.A., Vannucci, S.J., DeJoseph, M.R., Hawkins, R.A., Glucose transporter asymmetries in the bovine blood-brain barrier. J. Biol. Chem. 276 (2001), 12725–12729.
34. Smith, G.P., Epstein, A.N., Increased feeding in response to decreased glucose utilization in the rat and monkey. Am. J. Physiol. 217 (1969), 1083–1087.
35. Sofroniew, M.V., Vinters, H.V., Astrocytes: biology and pathology. Acta Neuropathol. 119 (2010), 7–35.
36. Toran-Allerand, C.D., Bentham, W., Miranda, R.C., Anderson, J.P., Insulin influences astroglial morphology and glial fibrillary acidic protein (GFAP) expression in organotypic cultures. Brain Res. 558 (1991), 296–304.
37. Tubbs, E., Theurey, P., Vial, G., Bendridi, N., Bravard, A., Chauvin, M.A., Ji-Cao, J., Zoulim, F., Bartosch, B., Ovize, M., et al. Mitochondria-associated endoplasmic reticulum membrane (MAM) integrity is required for insulin signaling and is implicated in hepatic insulin resistance. Diabetes 63 (2014), 3279–3294.
38. Winkler, E.A., Nishida, Y., Sagare, A.P., Rege, S.V., Bell, R.D., Perlmutter, D., Sengillo, J.D., Hillman, S., Kong, P., Nelson, A.R., et al. GLUT1 reductions exacerbate Alzheimer's disease vasculo-neuronal dysfunction and degeneration. Nat. Neurosci. 18 (2015), 521–530.
39. Woods, S.C., Lotter, E.C., McKay, L.D., Porte, D. Jr., Chronic intracerebroventricular infusion of insulin reduces food intake and body weight of baboons. Nature 282 (1979), 503–505.
40. Zeltser, L.M., Seeley, R.J., Tschöp, M.H., Synaptic plasticity in neuronal circuits regulating energy balance. Nat. Neurosci. 15 (2012), 1336–1342.