Diffusion of d-glucose measured in the cytosol of a single astrocyte

Cellular and Molecular Life Sciences

Volumn 70, Issue 8, 2013, Pages 1483-1492

  Kreft, Marko ^a,b   Lukšič, Miha ^a   Zorec, Tomaž M ^a   Prebil, Mateja ^a   Zorec, Robert ^a,b  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b Celica Biomedical Sciences Center   (Slovenia)

Author keywords

Astrocytes; Diffusion; Glucose

Indexed keywords

GLUCOSE;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL LEVEL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; DIFFUSION COEFFICIENT; GLUCOSE TRANSPORT; INTRACELLULAR TRANSPORT; MATHEMATICAL MODEL; NONHUMAN; RAT; TRANSPORT KINETICS;

ANIMALS; ASTROCYTES; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CYTOSOL; DIFFUSION; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLUCOSE; KINETICS; MODELS, BIOLOGICAL; RATS; SINGLE-CELL ANALYSIS;

RATTUS;

EID: 84876680805     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1219-7     Document Type: Article

References (74)

1. Vesce S, Bezzi P, Volterra A (1999) The active role of astrocytes in synaptic transmission. Cell Mol Life Sci 56:991-1000 (Pubitemid 30019215)
2. Kacem K, Lacombe P, Seylaz J, Bonvento G (1998) Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia 23:1-10 (Pubitemid 28174041)
3. Tsacopoulos M, Magistretti P (1996) Metabolic coupling between glia and neurons. J Neurosci 16:877-885 (Pubitemid 26140843)
4. Murphy S (1993) Astrocytes: pharmacology and function. Academic Press, San Diego
5. Parpura V, Zorec R (2010) Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 63:83-92
6. Parpura V, Baker B, Jeras M, Zorec R (2010) Regulated exocytosis in astrocytic signal integration. Neurochem Int 57:451-459
7. Cohen Z, Ehret M, Maitre M, Hamel E (1995) Ultrastructural analysis of tryptophan hydroxylase immunoreactive nerve terminals in the rat cerebral cortex and hippocampus: their associations with local blood vessels. Neuroscience 66:555-569
8. Simpson IA, Carruthers A, Vannucci SJ (2007) Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 27:1766-1791 (Pubitemid 47624552)
9. Clarke D, Sokoloff L (1999) Circulation and energy metabolism of the brain. In: Siegel G, Agranoff B, Albers R, Fisher S, Uhler MD (eds) Basic neurochemistry. Lippincott-Raven, Philadelphia, pp 637-669
10. Zhao F, Keating A (2007) Functional properties and genomics of glucose transporters. Curr Genomics 8:113-128 (Pubitemid 46690959)
11. Maher F, Vannucci S, Simpson I (1994) Glucose transporter proteins in brain. FASEB J 8:1003-1011 (Pubitemid 24338544)
12. Morgello S, Uson R, Schwartz E, Haber R (1995) The human blood-brain barrier glucose transporter (GLUT1) is a glucose transporter of gray matter astrocytes. Glia 14:43-54
13. Leino R, Gerhart D, van Bueren A, McCall A, Drewes L (1997) Ultrastructural localization of GLUT 1 and GLUT 3 glucose transporters in rat brain. J Neurosci Res 49:617-626 (Pubitemid 27381249)
14. Leloup C, Arluison M, Lepetit N, Cartier N, Marfaing-Jallat P, Ferré P, Pénicaud L (1994) Glucose transporter 2 (GLUT 2): expression in specific brain nuclei. Brain Res 638:221-226 (Pubitemid 24063308)
15. Arluison M, Quignon M, Nguyen P, Thorens B, Leloup C, Penicaud L (2004) Distribution and anatomical localization of the glucose transporter 2 (GLUT2) in the adult rat brain-An immunohistochemical study. J Chem Neuroanat 28:117-136 (Pubitemid 39336524)
16. Griffin L, Gelb B, Adams V, McCabe E (1992) Developmental expression of hexokinase 1 in the rat. Biochim Biophys Acta 1129:309-317
17. Needels D, Wilson J (1983) The identity of hexokinase activities from mitochondrial and cytoplasmic fractions of rat brain homogenates. J Neurochem 40:1134-1143 (Pubitemid 13163347)
18. Wilkin G, Wilson J (1977) Localization of hexokinase in neural tissue: light microscopic studies with immunofluorescence and histochemical procedures. J Neurochem 29:1039-1051 (Pubitemid 8226894)
19. Lynch R, Fogarty K, Fay F (1991) Modulation of hexokinase association with mitochondria analyzed with quantitative three-dimensional confocal microscopy. J Cell Biol 112:385-395 (Pubitemid 21925994)
20. Nagamatsu S, Nakamichi Y, Inoue N, Inoue M, Nishino H, Sawa H (1996) Rat C6 glioma cell growth is related to glucose transport and metabolism. Biochem J 319(Pt 2):477-482 (Pubitemid 26372206)
21. Ben-Yoseph O, Boxer P, Ross B (1994) Oxidative stress in the central nervous system: monitoring the metabolic response using the pentose phosphate pathway. Dev Neurosci 16:328-336
22. Leo G, Driscoll B, Shank R, Kaufman E (1993) Analysis of [1-13C] D-glucose metabolism in cultured astrocytes and neurons using nuclear magnetic resonance spectroscopy. Dev Neurosci 15:282-288 (Pubitemid 24258161)
23. Wiesinger H, Hamprecht B, Dringen R (1997) Metabolic pathways for glucose in astrocytes. Glia 21:22-34 (Pubitemid 27389637)
24. Pellerin L, Magistretti P (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilisation. Proc Natl Acad Sci USA 91:10625-10629 (Pubitemid 24329051)
25. Cataldo A, Broadwell R (1986) Cytochemical identification of cerebral glycogen and glucose-6-phosphatase activity under normal and experimental conditions. II. Choroid plexus and ependymal epithelia, endothelia and pericytes. J Neurocytol 15:511-524 (Pubitemid 16045887)
26. Wender R, Brown A, Fern R, Swanson R, Farrell K, Ransom B (2000) Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci 20:6804-6810
27. Fillenz M, Lowry J, Boutelle M, Fray A (1999) The role of astrocytes and noradrenaline in neuronal glucose metabolism. Acta Physiol Scand 167:275-284 (Pubitemid 30037868)
28. Walls A, Heimbürger C, Bouman S, Schousboe A, Waagepetersen H (2009) Robust glycogen shunt activity in astrocytes: effects of glutamatergic and adrenergic agents. Neuroscience 158:284-292
29. Marrif H, Juurlink B (1999) Astrocytes respond to hypoxia by increasing glycolytic capacity. J Neurosci Res 57:255-260 (Pubitemid 29300328)
30. Niitsu Y, Hori O, Yamaguchi A, Bando Y, Ozawa K, Tamatani M, Ogawa S, Tohyama M (1999) Exposure of cultured primary rat astrocytes to hypoxia results in intracellular glucose depletion and induction of glycolytic enzymes. Brain Res Mol Brain Res 74:26-34 (Pubitemid 30038176)
31. Kahlert S, Reiser G (2004) Glial perspectives of metabolic states during cerebral hypoxia - calcium regulation and metabolic energy. Cell Calcium 36:295-302 (Pubitemid 38996758)
32. Bekar LK, He W, Nedergaard M (2008) Locus coeruleus a-Adrenergic - mediated activation of cortical astrocytes in vivo. Cereb Cortex 18:2789-2795
33. Prebil M, Vardjan N, Jensen J, Zorec R, Kreft M (2011) Dynamic monitoring of cytosolic glucose in single astrocytes. Glia 59:903-913
34. Forsyth R, Bartlett K, Burchell A, Scott H, Eyre J (1993) Astrocytic glucose-6-phosphatase and the permeability of brain microsomes to glucose 6-phosphate. Biochem J 294(Pt 1):145-151 (Pubitemid 23251923)
35. Dringen R, Hamprecht B (1993) Differences in glycogen metabolism in astroglia-rich primary cultures and sorbitol-selected astroglial cultures derived from mouse brain. Glia 8:143-149
36. Forsyth R (1996) Astrocytes and the delivery of glucose from plasma to neurons. Neurochem Int 28:231-241 (Pubitemid 26063013)
37. Fehr M, Lalonde S, Lager I, Wolff M, Frommer W (2003) In vivo imaging of the dynamics of glucose uptake in the cytosol of COS-7 cells by fluorescent nanosensors. J Biol Chem 278:19127-19133 (Pubitemid 36799301)
38. Takanaga H, Chaudhuri B, Frommer W (2008) GLUT1 and GLUT9 as major contributors to glucose influx in HepG2 cells identified by a high sensitivity intramolecular FRET glucose sensor. Biochim Biophys Acta 1778:1091-1099
39. Schwartz J, Wilson D (1992) Preparation and characterization of type 1 astrocytes cultured from adult rat cortex, cerebellum, and striatum. Glia 5:75-80
40. Kreft M, Stenovec M, Rupnik M, Grilc S, Krzan M, Potokar M, Pangrsic T, Haydon P, Zorec R (2004) Properties of Ca (2 +)-dependent exocytosis in cultured astrocytes. Glia 46:437-445 (Pubitemid 38679201)
41. John S, Ottolia M, Weiss J, Ribalet B (2008) Dynamic modulation of intracellular glucose imaged in single cells using a FRET-based glucose nanosensor. Pflugers Arch 456:307-322
42. Bittner C, Loaiza A, Ruminot I, Larenas V, Sotelo-Hitschfeld T, Gutiérrez R, Córdova A, Valdebenito R, Frommer W, Barros L (2010) High-resolution measurement of the glycolytic rate. Front Neuroenergetics 2:26. doi: 10.3389/fnene.2010.00026
43. Marucci M, Ragnarsson G, Axelsson A (2006) Electronic speckle pattern interferometry: a novel non-invasive tool for studying drug transport rate through free films. J Control Release 114:369-380 (Pubitemid 44310819)
44. Silver I, Erecińska M (1994) Extracellular glucose concentration in mammalian brain: continuous monitoring of changes during increased neuronal activity and upon limitation in oxygen supply in normo-, hypo-, and hyperglycemic animals. J Neurosci 14:5068-5076
45. Fellows L, Boutelle M, Fillenz M (1992) Extracellular brain glucose levels reflect local neuronal activity: a microdialysis study in awake, freely moving rats. J Neurochem 59:2141-2147
46. Cameron IL, Ord VA (1983) Parenteral level of glucose intake on glucose homeostasis, tumor growth, gluconeogenesis, and body composition in normal and tumor-bearing rats. Cancer Res 43:5228-5234 (Pubitemid 14227505)
47. Huang BW, Chiang MT, Yao HT, Chiang W (2004) The effect of high-fat and high-fructose diets on glucose tolerance and plasma lipid and leptin levels in rats. Diabetes Obes Metab 6:120-126 (Pubitemid 38220104)
48. Prebil M, Chowdhury HH, Zorec R, Kreft M (2011) Changes in cytosolic glucose level in ATP stimulated live astrocytes. Biochem Biophys Res Commun 405:308-313
49. Loaiza A, Porras O, Barros L (2003) Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. J Neurosci 23:7337-7342 (Pubitemid 36999523)
50. Lai J, Behar K, Liang B, Hertz L (1999) Hexokinase in astrocytes: kinetic and regulatory properties. Metab Brain Dis 14:125-133 (Pubitemid 29418695)
51. Giaume C, Koulakoff A, Roux L, Holcman D, Rouach N (2010) Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat Rev Neurosci 11:87-99
52. Nagy JI, Dudek FE, Rash JE (2004) Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res Brain Res Rev 47:191-215 (Pubitemid 39574320)
53. Langer J, Stephan J, Theis M, Rose CR (2012) Gap junctions mediate intercellular spread of sodium between hippocampal astrocytes in situ. Glia 60:239-252
54. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322:1551-1555
55. Tabernero A, Medina JM, Giaume C (2006) Glucose metabolism and proliferation in glia: role of astrocytic gap junctions. J Neurochem 99:1049-1061 (Pubitemid 44655272)
56. Retamal MA, Froger N, Palacios-Prado N, Ezan P, Sáez PJ, Sáez JC, Giaume C (2007) Cx43 hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia. J Neurosci 27:13781-13792 (Pubitemid 350278255)
57. Ball KK, Gandhi GK, Thrash J, Cruz NF, Dienel GA (2007) Astrocytic connexin distributions and rapid, extensive dye transfer via gap junctions in the inferior colliculus: implications for [(14)C]glucose metabolite trafficking. J Neurosci Res 85:3267-3283 (Pubitemid 350058515)
58. Nie X, Olsson Y (1996) Endothelin peptides in brain diseases. Rev Neurosci 7:177-186 (Pubitemid 26397658)
59. Sánchez-Alvarez R, Tabernero A, Medina J (2004) Endothelin-1 stimulates the translocation and upregulation of both glucose transporter and hexokinase in astrocytes: relationship with gap junctional communication. J Neurochem 89:703-714 (Pubitemid 38534156)
60. Northam W, Bedoy C, Mobley P (1989) Pharmacological identification of the alpha-Adrenergic receptor type which inhibits the beta-Adrenergic activated adenylate cyclase system in cultured astrocytes. Glia 2:129-133
61. Hertz L, Lovatt D, Goldman S, Nedergaard M (2010) Adrenoceptors in brain: cellular gene expression and effects on astrocytic metabolism and [Ca(2 +)]i. Neurochem Int 57:411-420
62. Fray A, Forsyth R, Boutelle M, Fillenz M (1996) The mechanisms controlling physiologically stimulated changes in rat brain glucose and lactate: a microdialysis study. J Physiol 496(Pt 1):49-57 (Pubitemid 26345575)
63. Subbarao K, Hertz L (1991) Stimulation of energy metabolism by alpha-Adrenergic agonists in primary cultures of astrocytes. J Neurosci Res 28:399-405
64. Subbarao K, Hertz L (1990) Effect of adrenergic agonists on glycogenolysis in primary cultures of astrocytes. Brain Res 536:220-226
65. Gibbs M, Hutchinson D, Hertz L (2008) Astrocytic involvement in learning and memory consolidation. Neurosci Biobehav Rev 32:927-944
66. Shulman R, Hyder F, Rothman D (2001) Cerebral energetics and the glycogen shunt: neurochemical basis of functional imaging. Proc Natl Acad Sci USA 98:6417-6422 (Pubitemid 32488252)
67. Ghosh A, Cheung Y, Mansfield B, Chou J (2005) Brain contains a functional glucose-6-phosphatase complex capable of endogenous glucose production. J Biol Chem 280:11114-11119 (Pubitemid 40418416)
68. DiNuzzo M, Mangia S, Maraviglia B, Giove F (2010) Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: evidence from mathematical modeling. J Cereb Blood Flow Metab 30:586-602
69. Hrabetová S, Nicholson C (2004) Contribution of dead-space microdomains to tortuosity of brain extracellular space. Neurochem Int 45:467-477 (Pubitemid 38739473)
70. Andersson M, Axelsson A, Zacchi G (1997) Diffusion of glucose and insulin in a swelling N-isopropylacrylamide gel. Int J Pharm 157:199-208 (Pubitemid 27471172)
71. Groebe K, Erz S, Mueller-Klieser W (1994) Glucose diffusion coefficients determined from concentration profiles in EMT6 tumor spheroids incubated in radioactively labeled l-glucose. Adv Exp Med Biol 361:619-625
72. Bashkatov AN, Genina EA, Sinichkin YP, Kochubey VI, Lakodina NA, Tuchin VV (2003) Glucose and mannitol diffusion in human dura mater. Biophys J 85:3310-3318 (Pubitemid 37345819)
73. Gerhardt GA, Adams RN (1982) Determination of diffusion coefficients by flow injection analysis. Anal Chem 54:2618-2620
74. Nicholson C (2001) Diffusion and related transport mechanisms in brain tissue. Rep Prog Phys 64:815-884 (Pubitemid 32657274)