Insulin regulates astrocytic glucose handling through cooperation with IGF-I

Diabetes

Volumn 66, Issue 1, 2017, Pages 64-74

  Fernandez, Ana M ^a,b   Hernandez Garzón, Edwin ^a,b   Perez Domper, Paloma ^a,b   Perez Alvarez, Alberto ^a,c   Mederos, Sara ^a   Matsui, Takashi ^d   Santi, Andrea ^a,b   Trueba Saiz, Angel ^a,b   García Guerra, Lucía ^b,e   Pose Utrilla, Julia ^b,e   Fielitz, Jens ^f,g   Olson, Eric N ^h   De La Rosa, Ruben Fernandez ⁱ   Garcia, Luis Garcia ⁱ   Pozo, Miguel Angel ⁱ   Iglesias, Teresa ^b,e   Araque, Alfonso ^a   Soya, Hideaki ^d   Perea, Gertrudis ^a   Martin, Eduardo D ^j   Aleman, Ignacio Torres ^a,b   more..

^a INSTITUTO CAJAL   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^g Medical University Brandenburg   (Germany)

^h UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

ⁱ INSTITUTO PLURIDISCIPLINAR   (Spain)

^j UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; BETA ACTIN; BETA TUBULIN; COLLAGEN TYPE 4; COLLAGENASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; GLUCOSE TRANSPORTER 1; GUANOSINE TRIPHOSPHATASE; HYDROCORTISONE; INSULIN; INSULIN LIKE GROWTH FACTOR 1 RECEPTOR ALPHA; INSULIN LIKE GROWTH FACTOR 1 RECEPTOR BETA; INSULIN LIKE GROWTH FACTOR RECEPTOR BETA; INSULIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PARAFORMALDEHYDE; PENICILLIN DERIVATIVE; POLYCYSTIN 1; POLYCYSTIN 2; PROTEIN C; PROTEIN KINASE D; PUROMYCIN; RAC1 PROTEIN; SCAFFOLD PROTEIN; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; SOMATOMEDIN RECEPTOR; STREPTOMYCIN; UNCLASSIFIED DRUG; GLYCOGEN; LACTIC ACID; SLC2A1 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN METABOLISM; CELL ACTIVITY; CELL FUNCTION; CELL MEMBRANE; CONTROLLED STUDY; FOREBRAIN; GLUCOSE BRAIN LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HYPOGLYCEMIA; MOUSE; NEWBORN; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; ANIMAL; IMMUNOASSAY; MALE; METABOLISM; NERVE CELL; PHYSIOLOGY; PLASMID; POLYMERASE CHAIN REACTION; POSITRON EMISSION TOMOGRAPHY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ASTROCYTES; BIOLOGICAL TRANSPORT; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; GLYCOGEN; IMMUNOASSAY; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LACTIC ACID; MALE; MICE; NEURONS; PLASMIDS; POLYMERASE CHAIN REACTION; POSITRON-EMISSION TOMOGRAPHY;

EID: 85007393308     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db16-0861     Document Type: Article

References (50)

1. Hasselbalch SG, Knudsen GM, Videbaek C, et al. No effect of insulin on glucose blood-brain barrier transport and cerebral metabolism in humans. Diabetes 1999;48:1915.1921
2. Hirvonen J, Virtanen KA, Nummenmaa L, et al. Effects of insulin on brain glucose metabolism in impaired glucose tolerance. Diabetes 2011;60:443.447
3. Simpson IA, Vannucci SJ, Maher F. Glucose transporters in mammalian brain. Biochem Soc Trans 1994;22:671.675
4. Peters A, Schweiger U, Fruhwald-Schultes B, Born J, Fehm HL. The neuroendocrine control of glucose allocation. Exp Clin Endocrinol Diabetes 2002;110:199.211
5. Cheng CM, Reinhardt RR, Lee WH, Joncas G, Patel SC, Bondy CA. Insulinlike growth factor 1 regulates developing brain glucose metabolism. Proc Natl Acad Sci USA 2000;97:10236.10241
6. Fadel JR, Reagan LP. Stop signs in hippocampal insulin signaling: the role of insulin resistance in structural, functional and behavioral deficits. Curr Opin Behav Sci 2016;9:47.54
7. Busiguina S, Chowen JA, Argente J, Torres-Aleman I. Specific alterations of the insulin-like growth factor I system in the cerebellum of diabetic rats. Endocrinology 1996;137:4980.4987
8. Fielitz J, Kim MS, Shelton JM, et al. Requirement of protein kinase D1 for pathological cardiac remodeling. Proc Natl Acad Sci USA 2008;105:3059.3063
9. Fernandez AM, Fernandez S, Carrero P, Garcia-Garcia M, Torres-Aleman I. Calcineurin in reactive astrocytes plays a key role in the interplay between proinflammatory and anti-inflammatory signals. J Neurosci 2007;27:8745.8756
10. Jacob KK, Whittaker J, Stanley FM. Insulin receptor tyrosine kinase activity and phosphorylation of tyrosines 1162 and 1163 are required for insulinincreased prolactin gene expression. Mol Cell Endocrinol 2002;186:7.16
11. Wieman HL, Wofford JA, Rathmell JC. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol Biol Cell 2007;18:1437.1446
12. Gonzalez de la Vega A, Buno W, Pons S, Garcia-Calderat MS, Garcia-Galloway E, Torres-Aleman I. Insulin-like growth factor I potentiates kainate receptors through a phosphatidylinositol 3-kinase dependent pathway. Neuroreport 2001;12:1293.1296
13. Perriere N, Demeuse P, Garcia E, et al. Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J Neurochem 2005;93:279.289
14. Barros LF, Bittner CX, Loaiza A, et al. Kinetic validation of 6-NBDG as a probe for the glucose transporter GLUT1 in astrocytes. J Neurochem 2009;109(Suppl. 1):94.100
15. Schaffer L, Brand CL, Hansen BF, et al. A novel high-affinity peptide antagonist to the insulin receptor. Biochem Biophys Res Commun 2008;376:380. 383
16. Koshy S, Alizadeh P, Timchenko LT, Beeton C. Quantitative measurement of GLUT4 translocation to the plasma membrane by flow cytometry. J Vis Exp 2010; (45): e2429
17. Gonzalez S, Moreno-Delgado D, Moreno E, et al. Circadian-related heteromerization of adrenergic and dopamine D. receptors modulates melatonin synthesis and release in the pineal gland. PLoS Biol 2012;10:e1001347
18. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45
19. Nishijima T, Piriz J, Duflot S, et al. Neuronal activity drives localized bloodbrainbarrier transport of serum insulin-like growth factor-I into the CNS. Neuron 2010;67:834.846
20. Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012;9:676.682
21. Chuquet J, Quilichini P, Nimchinsky EA, Buzsaki G. Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex. J Neurosci 2010;30:15298.15303
22. Perez-Alvarez A, Araque A, Martin ED. Confocal microscopy for astrocyte in vivo imaging: recycle and reuse in microscopy. Front Cell Neurosci 2013;7:51
23. Hernandez-Garzon E, Fernandez AM, Perez-Alvarez A, et al. The insulin-like growth factor I receptor regulates glucose transport by astrocytes. Glia 2016;64:1962.1971
24. Roy CS, Sherrington CS. On the regulation of the blood-supply of the brain. J Physiol 1890;11:85.158.17
25. Kim WH, Lee J, Jung DW, Williams DR. Visualizing sweetness: increasingly diverse applications for fluorescent-tagged glucose bioprobes and their recent structural modifications. Sensors (Basel) 2012;12:5005.5027
26. Albrecht J, Wroblewska B, Mossakowski MJ. The binding of insulin to cerebral capillaries and astrocytes of the rat. Neurochem Res 1982;7:489.494
27. Baron-Van Evercooren A, Olichon-Berthe C, Kowalski A, Visciano G, Van Obberghen E. Expression of IGF-I and insulin receptor genes in the rat central nervous system: a developmental, regional, and cellular analysis. J Neurosci Res 1991;28:244.253
28. Leino RL, Gerhart DZ, van Bueren AM, McCall AL, Drewes LR. Ultrastructural localization of GLUT 1 and GLUT 3 glucose transporters in rat brain. J Neurosci Res 1997;49:617.626
29. Wiesinger H, Hamprecht B, Dringen R. Metabolic pathways for glucose in astrocytes. Glia 1997;21:22.34
30. Heni M, Hennige AM, Peter A, et al. Insulin promotes glycogen storage and cell proliferation in primary human astrocytes. PLoS One 2011;6:e21594
31. Gray SM, Meijer RI, Barrett EJ. Insulin regulates brain function, but how does it get there? Diabetes 2014;63:3992.3997
32. Kuwabara T, Kagalwala MN, Onuma Y, et al. Insulin biosynthesis in neuronal progenitors derived from adult hippocampus and the olfactory bulb. EMBO Mol Med 2011;3:742.754
33. Reinhardt RR, Bondy CA. Insulin-like growth factors cross the blood-brain barrier. Endocrinology 1994;135:1753.1761
34. Rotwein P, Burgess SK, Milbrandt JD, Krause JE. Differential expression of insulin-like growth factor genes in rat central nervous system. Proc Natl Acad Sci USA 1988;85:265.269
35. Nagase M, Takahashi Y, Watabe AM, Kubo Y, Kato F. On-site energy supply at synapses through monocarboxylate transporters maintains excitatory synaptic transmission. J Neurosci 2014;34:2605.2617
36. Clarke DW, Mudd L, Boyd FT Jr, Fields M, Raizada MK. Insulin is released from rat brain neuronal cells in culture. J Neurochem 1986;47:831.836
37. Cao P, Maximov A, Sudhof TC. Activity-dependent IGF-1 exocytosis is controlled by the Ca (2+)-sensor synaptotagmin-10. Cell 2011;145:300.311
38. Celil AB, Campbell PG. BMP-2 and insulin-like growth factor-I mediate Osterix (Osx) expression in human mesenchymal stem cells via the MAPK and protein kinase D signaling pathways. J Biol Chem 2005;280:31353-31359
39. Chen J, Lu G, Wang QJ. Protein kinase C-independent effects of protein kinase D3 in glucose transport in L6 myotubes. Mol Pharmacol 2005;67:152-162
40. Hermanto U, Zong CS, Li W, Wang LH. RACK1, an insulin-like growth factor I (IGF-I) receptor-interacting protein, modulates IGF-I-dependent integrin signaling and promotes cell spreading and contact with extracellular matrix. Mol Cell Biol 2002;22:2345-2365
41. Booth RA, Cummings C, Tiberi M, Liu XJ. GIPC participates in G protein signaling downstream of insulin-like growth factor 1 receptor. J Biol Chem 2002;277:6719-6725
42. Bunn RC, Jensen MA, Reed BC. Protein interactions with the glucose transporter binding protein GLUT1CBP that provide a link between GLUT1 and the cytoskeleton. Mol Biol Cell 1999;10:819-832
43. Elfenbein A, Rhodes JM, Meller J, Schwartz MA, Matsuda M, Simons M. Suppression of RhoG activity is mediated by a syndecan 4-synectin-RhoGDI1 complex and is reversed by PKCalpha in a Rac1 activation pathway. J Cell Biol 2009;186:75-83
44. Sylow L, Jensen TE, Kleinert M, et al. Rac1 is a novel regulator of contractionstimulated glucose uptake in skeletal muscle. Diabetes 2013;62:1139-1151
45. Reed BC, Cefalu C, Bellaire BH, et al. GLUT1CBP (TIP2/GIPC1) interactions with GLUT1 and myosin VI: evidence supporting an adapter function for GLUT1CBP. Mol Biol Cell 2005;16:4183-4201
46. Csajbók EA, Tamás G. Cerebral cortex: a target and source of insulin? Diabetologia 2016;59:1609-1615
47. Grillo CA, Piroli GG, Hendry RM, Reagan LP. Insulin-stimulated translocation of GLUT4 to the plasma membrane in rat hippocampus is PI3-kinase dependent. Brain Res 2009;1296:35-45
48. Allaman I, Bélanger M, Magistretti PJ. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 2011;34:76-87
49. Strachan MW, Reynolds RM, Marioni RE, Price JF. Cognitive function, dementia and type 2 diabetes mellitus in the elderly. Nat Rev Endocrinol 2011;7:108-114
50. Trueba-Saiz A, Torres Aleman I. Insulin-like peptides signaling in Alzheimer's disease: on the road to alternative therapeutics. Curr Opin Behav Sci 2016;9:15-25