Uptake and metabolism of fructose by rat neocortical cells in vivo and by isolated nerve terminals in vitro

Journal of Neurochemistry

Volumn 133, Issue 4, 2015, Pages 572-581

  Hassel, Bjørnar ^a,b   Elsais, Ahmed ^a   Frøland, Anne Sofie ^a   Taubøll, Erik ^a   Gjerstad, Leif ^a   Quan, Yi ^c   Dingledine, Raymond ^c   Rise, Frode ^d  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b NORWEGIAN DEFENCE RESEARCH ESTABLISHMENT FFI   (Norway)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

Alzheimer's disease; brain metabolism; fructose; Glut5; glyceraldehyde; ketohexokinase

Indexed keywords

4 AMINOBUTYRIC ACID; ADVANCED GLYCATION END PRODUCT; ALANINE; ALDEHYDE REDUCTASE; ASPARTIC ACID; CARBON 14; FRUCTOSE; GLUCOSE; GLUCOSE TRANSPORTER 3; GLUCOSE TRANSPORTER 5; GLUTAMIC ACID; GLUTAMINE; GLYCERALDEHYDE; HEXOKINASE 1; IDITOL DEHYDROGENASE; POLYOL; AMINO ACID; CARBON; FRUCTOKINASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUTAMATE TRANSPORTER; HEXOKINASE; KETOHEXOKINASE;

AEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN METABOLISM; CARBOHYDRATE ANALYSIS; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CELL MEMBRANE TRANSPORT; CELL METABOLISM; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; EXTRACELLULAR SPACE; GLYCOLYSIS; IN VITRO STUDY; IN VIVO STUDY; ISOTOPE LABELING; MALE; NEOCORTEX; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN EXPRESSION; RAT; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVE CELL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SYNAPTOSOME; WISTAR RAT;

RATTUS;

AMINO ACID TRANSPORT SYSTEM X-AG; AMINO ACIDS; ANIMALS; CARBON ISOTOPES; FRUCTOKINASES; FRUCTOSE; FRUCTOSE-BISPHOSPHATE ALDOLASE; GENE EXPRESSION REGULATION; GLUCOSE; GLYCERALDEHYDE; HEXOKINASE; IN VITRO TECHNIQUES; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLIC NETWORKS AND PATHWAYS; NEOCORTEX; NEURONS; RATS; RATS, WISTAR; SYNAPTOSOMES;

EID: 84927625284     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13079     Document Type: Article

References (49)

1. Aragno M., Mastrocola R., Medana C., Restivo F., Catalano M. G., Pons N., Danni O., and, Boccuzzi G., (2005) Up-regulation of advanced glycated products receptors in the brain of diabetic rats is prevented by antioxidant treatment. Endocrinology 146, 5561-5567.
2. Arakaki T. L., Pezza J. A., Cronin M. A., Hopkins C. E., Zimmer D. B., Tolan D. R., and, Allen K. N., (2004) Structure of human brain fructose 1,6-(bis)phosphate aldolase: linking isozyme structure with function. Protein Sci. 13, 3077-3084.
3. Augustin R., (2010) The protein family of glucose transport facilitators: it's not only about glucose after all. IUBMB Life 62, 315-333.
4. Bais R., James H. M., Rofe A. M., and, Conyers R. A., (1985) The purification and properties of human liver ketohexokinase. A role for ketohexokinase and fructose-bisphosphate aldolase in the metabolic production of oxalate from xylitol. Biochem. J. 230, 53-60.
5. Choei H., Sasaki N., Takeuchi M., Yoshida T., Ukai W., Yamagishi S., Kikuchi S., and, Saito T., (2004) Glyceraldehyde-derived advanced glycation end products in Alzheimer's disease. Acta Neuropathol. 108, 189-193.
6. 13C NMR spectroscopy at 14.1 T. J. Neurochem. 126, 579-590.
7. Fawver J. N., Schall H. E., Petrofes-Chapa R. D., Zhu X., and, Murray I. V., (2012) Amyloid-β metabolite sensing: biochemical linking of glycation modification and misfolding. J. Alzheimers Dis. 30, 63-73.
8. Funari V. A., Herrera V. L., Freeman D., and, Tolan D. R., (2005) Genes required for fructose metabolism are expressed in Purkinje cells in the cerebellum. Brain Res. Mol. Brain Res. 142, 115-122.
9. 14C]ribose and the levels of amino acids in rat brain. J. Neurochem. 22, 53-61.
10. Gray E. G., and, Whittaker V. P., (1962) The isolation of nerve endings from brain: an electron microscopic study of cell fragments derived by homogenization and centrifugation. J. Anat. 96, 79-88.
11. Hassel B., and, Bråthe A., (2000) Cerebral metabolism of lactate in vivo: evidence for neuronal pyruvate carboxylation. J. Cereb. Blood Flow Metab. 20, 327-336.
12. Hassel B., Westergaard N., Schousboe A., and, Fonnum F., (1995) Metabolic differences between primary cultures of astrocytes and neurons from cerebellum and cerebral cortex. Effects of fluorocitrate. Neurochem. Res. 20, 413-420.
13. Hassel B., Shaw R., Taubøll E., Gjerstad L., and, Dingledine R., (2010) Region-specific changes in gene expression in rat brain after chronic treatment with levetiracetam or phenytoin. Epilepsia 51, 1714-1720.
14. Imamura K., Taniuchi K., and, Tanaka T., (1972) Multimolecular forms of pyruvate kinase. II. Purification of M2 -type pyruvate kinase from Yoshida ascites hepatoma 130 cells and comparative studies on the enzymological and immunological properties of the three types of pyruvate kinases, L, M1, and M2. J. Biochem. (Tokyo) 72, 1001-1015.
15. Izumi Y., and, Zorumski C. F., (2009) Glial-neuronal interactions underlying fructose utilization in rat hippocampal slices. Neuroscience 161, 847-854.
16. Leicht W., Heinz F., and, Freimüller B., (1978) Purification and characterization of aldehyde dehydrogenase from bovine liver. Eur. J. Biochem. 83, 189-196.
17. Li Q., Manolescu A., Ritzel M., Yao S., Slugoski M., Young J. D., Chen X. Z., and, Cheeseman C. I., (2004) Cloning and functional characterization of the human GLUT7 isoform SLC2A7 from the small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G236-G242.
18. Lowry O. H., and, Passoneau J. V., (1972) A Flexible System of Enzymatic Analysis, pp. 174-177. Academic Press, New York.
19. Lustig R. H., Schmidt L. A., and, Brindis C. D., (2012) Public health: the toxic truth about sugar. Nature 482, 27-29.
20. Lüth H. J., Ogunlade V., Kuhla B., Kientsch-Engel R., Stahl P., Webster J., Arendt T., and, Münch G., (2005) Age- and stage-dependent accumulation of advanced glycation end products in intracellular deposits in normal and Alzheimer's disease brains. Cereb. Cortex 15, 211-220.
21. Lyssiotis C. A., and, Cantley L. C., (2013) Metabolic syndrome: f stands for fructose and fat. Nature 502, 181-182.
22. Maher F., Davies-Hill T. M., and, Simpson I. A., (1996) Substrate specificity and kinetic parameters of GLUT3 in rat cerebellar granule neurons. Biochem. J. 315, 827-831.
23. Martinez-Hernandez A., Bell K. P., and, Norenberg M. D., (1977) Glutamine synthetase: glial localization in brain. Science 195, 1356-1358.
24. Meakin P. J., Fowler M. J., Rathbone A. J., Allen L. M., Ransom B. R., Ray D. E., and, Brown A. M., (2007) Fructose metabolism in the adult mouse optic nerve, a central white matter tract. J. Cereb. Blood Flow Metab. 27, 86-99.
25. Morland C., Boldingh K. A., Iversen E. G., and, Hassel B., (2004) Valproate is neuroprotective against malonate toxicity in rat striatum: an association with augmentation of high-affinity glutamate uptake. J. Cereb. Blood Flow Metab. 24, 1226-1234.
26. Morris P., and, Bachelard H., (2003) Reflections on the application of 13C-MRS to research on brain metabolism. NMR Biomed. 16, 303-312.
27. Mortensen O. H., Larsen L. H., Orstrup L. K., Hansen L. H., Grunnet N., and, Quistorff B., (2014) Developmental programming by high fructose decreases phosphorylation efficiency in aging offspring brain mitochondria, correlating with enhanced UCP5 expression. J. Cereb. Blood Flow Metab. 34, 1205-1211.
28. O'Brien M. M., Schofield P. J., and, Edwards M. R., (1983) Polyol-pathway enzymes of human brain. Partial purification and properties of sorbitol dehydrogenase. Biochem. J. 211, 81-90.
29. Oldendorf W. H., (1971) Brain uptake of radiolabeled amino acids, amines, and hexoses after arterial injection. Am. J. Physiol. 221, 1629-1639.
30. Ottersen O. P., and, Storm-Mathisen J., (1985) Different neuronal localization of aspartate-like and glutamate-like immunoreactivities in the hippocampus of rat, guinea-pig and Senegalese baboon (Papio papio), with a note on the distribution of gamma-aminobutyrate. Neuroscience 16, 589-606.
31. Page K. A., Chan O., Arora J., et al,. (2013) Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. JAMA 309, 63-70.
32. Payne J., Maher F., Simpson I., Mattice L., and, Davies P., (1997) Glucose transporter Glut 5 expression in microglial cells. Glia 21, 327-331.
33. Pezza J. A., Stopa J. D., Brunyak E. M., Allen K. N., and, Tolan D. R., (2007) Thermodynamic analysis shows conformational coupling and dynamics confer substrate specificity in fructose-1,6-bisphosphate aldolase. Biochemistry 46, 13010-13018.
34. Rand E. B., Depaoli A. M., Davidson N. O., Bell G. I., and, Burant C. F., (1993) Sequence, tissue distribution, and functional characterization of the rat fructose transporter GLUT5. Am. J. Physiol. 264, G1169-G1176.
35. Ronne-Engström E., Carlson H., Liu Y., Ungerstedt U., and, Hillered L., (1995) Influence of perfusate glucose concentration on dialysate lactate, pyruvate, aspartate, and glutamate levels under basal and hypoxic conditions: a microdialysis study in rat brain. J. Neurochem. 65, 257-262.
36. Saitoh M., Okada Y., and, Nabetani M., (1994) Effect of mannose, fructose and lactate on the preservation of synaptic potentials in hippocampal slices. Neurosci. Lett. 171, 125-128.
37. Schalkwijk C. G., Stehouwer C. D., and, van Hinsbergh V. W., (2004) Fructose-mediated non-enzymatic glycation: sweet coupling or bad modification. Diabetes Metab. Res. Rev. 20, 369-382.
38. Scheepers A., Schmidt S., Manolescu A., Cheeseman C. I., Bell A., Zahn C., Joost H. G., and, Schürmann A., (2005) Characterization of the human SLC2A11 (GLUT11) gene: alternative promoter usage, function, expression, and subcellular distribution of three isoforms, and lack of mouse orthologue. Mol. Membr. Biol. 22, 339-351.
39. Seatter M. J., De la Rue S. A., Porter L. M., and, Gould G. W., (1998) QLS motif in transmembrane helix VII of the glucose transporter family interacts with the C-1 position of D-glucose and is involved in substrate selection at the exofacial binding site. Biochemistry 37, 1322-1326.
40. Shu H. J., Isenberg K., Cormier R. J., Benz A., and, Zorumski C. F., (2006) Expression of fructose sensitive glucose transporter in the brains of fructose-fed rats. Neuroscience 140, 889-895.
41. Srikanth V., Maczurek A., Phan T., Steele M., Westcott B., Juskiw D., and, Münch G., (2011) Advanced glycation endproducts and their receptor RAGE in Alzheimer's disease. Neurobiol. Aging 32, 763-777.
42. Stewart M. A., Sherman W. R., Kurien M. M., Moonsammy G. I., and, Wisgerhof M., (1967) Polyol accumulations in nervous tissue of rats with experimental diabetes and galactosaemia. J. Neurochem. 14, 1057-1066.
43. Suárez G., Rajaram R., Bhuyan K. C., Oronsky A. L., and, Goidl J. A., (1988) Administration of an aldose reductase inhibitor induces a decrease of collagen fluorescence in diabetic rats. J. Clin. Invest. 82, 624-627.
44. Takakura Y., Kuentzel S. L., Raub T. J., Davies A., Baldwin S. A., and, Borchardt R. T., (1991) Hexose uptake in primary cultures of bovine brain microvessel endothelial cells. I. Basic characteristics and effects of D-glucose and insulin. Biochim. Biophys. Acta 1070, 1-10.
45. Thurston J. H., Levy C. A., Warren S. K., and, Jones E. M., (1972) Permeability of the blood-brain barrier to fructose and the anaerobic use of fructose in the brains of young mice. J. Neurochem. 19, 1685-1696.
46. Ueno M., Nishi N., Nakagawa T., Chiba Y., Tsukamoto I., Kusaka T., Miki T., Sakamoto H., Yamaguchi F., and, Tokuda M., (2014) Immunoreactivity of glucose transporter 5 is located in epithelial cells of the choroid plexus and ependymal cells. Neuroscience 260, 149-157.
47. Vander Jagt D. L., Robinson B., Taylor K. K., and, Hunsaker L. A., (1992) Reduction of trioses by NADPH-dependent aldo-keto reductases. Aldose reductase, methylglyoxal, and diabetic complications. J. Biol. Chem. 267, 4364-4369.
48. Wada H., Okada Y., Uzuo T., and, Nakamura H., (1998) The effects of glucose, mannose, fructose and lactate on the preservation of neural activity in the hippocampal slices from the guinea pig. Brain Res. 788, 144-1450.
49. Wiesinger H., Thiess U., and, Hamprecht B., (1990) Sorbitol pathway activity and utilization of polyols in astroglia-rich primary cultures. Glia 3, 277-282.