N-3 long-chain fatty acids and regulation of glucose transport in two models of rat brain endothelial cells

Neurochemistry International

Volumn 56, Issue 5, 2010, Pages 703-710

  Pifferi, Fabien ^a   Jouin, Mélanie ^a   Alessandri, Jean Marc ^a   Roux, Françoise ^b   Perrière, Nicolas ^c   Langelier, Bénédicte ^a   Lavialle, Monique ^a   Cunnane, Stephen ^d   Guesnet, Philippe ^a  

^a INRA   (France)

^b HÔPITAL FERNAND WIDAL   (France)

^c Université de Sherbrooke ^*  (France)

^d UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

Brain endothelial cells; Docosahexaenoic acid; Eicosapentaenoic acid; Glucose uptake; GLUT1; Omega 3 fatty acids

Indexed keywords

3 METHYLGLUCOSE; ARACHIDONIC ACID; GLUCOSE TRANSPORTER 1; ICOSAPENTAENOIC ACID; ISOPROTEIN; LONG CHAIN FATTY ACID; MEMBRANE PHOSPHOLIPID; MESSENGER RNA; N 3 LONG CHAIN FATTY ACID; OMEGA 6 FATTY ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN CELL; CELL IMMORTALIZATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FATTY ACID METABOLISM; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; HYPOTHESIS; LIPID COMPOSITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

3-O-METHYLGLUCOSE; ANIMALS; BLOTTING, WESTERN; BRAIN CHEMISTRY; CAPILLARIES; CELLS, CULTURED; DNA PRIMERS; DNA, COMPLEMENTARY; ENDOTHELIAL CELLS; FATTY ACIDS; FATTY ACIDS, OMEGA-3; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 3; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; MALE; RATS; RATS, WISTAR;

RATTUS;

EID: 77949569994     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2010.02.006     Document Type: Article

References (43)

1. Aas V., Rokling-Andersen M.H., Kase E.T., Thoresen G.H., Rustan A.C. Eicosapentaenoic acid (20:5 n-3) increases fatty acid and glucose uptake in cultured human skeletal muscle cells. J. Lipid Res. 2006, 47:366-374.
2. Achard F., Benistant C., Lagarde M. Interconversions and distinct metabolic fate of eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in bovine aortic endothelial cells. Biochim. Biophys. Acta 1995, 1255:260-266.
3. Aid S., Vancassel S., Poumes-Ballihaut C., Chalon S., Guesnet P., Lavialle M. Effect of a diet-induced n-3 PUFA depletion on cholinergic parameters in the rat hippocampus. J. Lipid Res. 2003, 44:1545-1551.
4. Alessandri J.M., Poumès-Ballihaut C., Langelier B., Perruchot M.H., Raguénez G., Lavialle M., Guesnet P. Incorporation of docosahexaenoic acid into nerve membrane phospholipids: bridging the gap between animals and cultured cells. Am. J. Clin. Nutr. 2003, 78:702-710.
5. Alessandri J.M., Guesnet P., Vancassel S., Astorg P., Denis I., Langelier B., Aid S., Poumes-Ballihaut C., Champeil-Potokar G., Lavialle M. Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life. Reprod. Nutr. Dev. 2004, 44:509-538.
6. Benistant C., Dehouck M.P., Fruchart J.C., Cecchelli R., Lagarde M. Fatty acid composition of brain capillary endothelial cells: effect of the coculture with astrocytes. J. Lipid Res. 1995, 36:2311-2319.
7. Bernoud N., Fenart L., Benistant C., Pageaux J.F., Dehouck M.P., Moliere P., Lagarde M., Cecchelli R., Lecerf J. Astrocytes are mainly responsible for the polyunsaturated fatty acid enrichment in blood-brain barrier endothelial cells in vitro. J. Lipid Res. 1998, 39:1816-1824.
8. Chalon S., Vancassel S., Zimmer L., Guilloteau D., Durand G. Polyunsaturated fatty acids and cerebral function: focus on monoaminergic neurotransmission. Lipids 2001, 36:937-944.
9. Dello Russo C., Gavrilyuk V., Weinberg G., Almeida A., Bolanos J.P., Palmer J., Pelligrino D., Galea E., Feinstein D.L. Peroxisome proliferator-activated receptor gamma thiazolidinedione agonists increase glucose metabolism in astrocytes. J. Biol. Chem. 2003, 278:5828-5836.
10. Delton-Vandenbroucke I., Grammas P., Anderson R.E. Polyunsaturated fatty acid metabolism in retinal and cerebral microvascular endothelial cells. J. Lipid Res. 1997, 38:147-159.
11. Duelli R., Kuschinsky W. Brain glucose transporters: relationship to local energy demand. News Physiol. Sci. 2001, 16:71-76.
12. Dyall S.C., Michael-Titus A.T. Neurological benefits of omega-3 fatty acids. Neuromol. Med. 2008, 10:219-235.
13. Extier A., Perruchot M.H., Baudry C., Guesnet P., Lavialle M., Alessandri J.M. Differential effects of steroids on the synthesis of polyunsaturated fatty acids by human neuroblastoma cells. Neurochem. Int. 2009, 55:295-301.
14. Freemantle E., Vandal M., Tremblay-Mercier J., Tremblay S., Blachère J.C., Bégin M.E., Brenna J.T., Windust A., Cunnane S.C. Omega-3 fatty acids, energy substrates, and brain function during aging. Prostaglandins Leukot. Essent. Fatty Acids 2007, 75:213-220.
15. Grintal B., Champeil-Potokar G., Lavialle M., Vancassel S., Breton S., Denis I. Inhibition of astroglial glutamate transport by polyunsaturated fatty acids: evidence for a signalling role of docosahexaenoic acid. Neurochem. Int. 2009, 54:535-543.
16. Hashimoto M., Hossain S., Yamasaki H., Yazawa K., Masumura S. Effects of eicosapentaenoic acid and docosahexaenoic acid on plasma membrane fluidity of aortic endothelial cells. Lipids 1999, 34:1297-1304.
17. Hawkins R.A., O'Kane R.L., Simpson I.A., Vina J.R. Structure of the blood-brain barrier and its role in the transport of amino acids. J. Nutr. 2006, 136:218S-226S.
18. Heird W.C., Lapillonne A. The role of essential fatty acids in development. Annu. Rev. Nutr. 2005, 25:549-571.
19. Kalman J., Gecse A., Farkas T., Joo F., Telegdy G., Lajtha A. Dietary manipulation with high marine fish oil intake of fatty acid composition and arachidonic acid metabolism in rat cerebral microvessels. Neurochem. Res. 1992, 17:167-172.
20. Kis B., Szabo C.A., Pataricza J., Krizbai I.A., Mezei Z., Gecse A., Telegdy G., Papp J.G., Deli M.A. Vasoactive substances produced by cultured rat brain endothelial cells. Eur. J. Pharmacol. 1999, 368:35-42.
21. Kramer S.D., Hurley J.A., Abbott N.J., Begley D.J. Lipids in blood-brain barrier models in vitro. I. Thin-layer chromatography and high-performance liquid chromatography for the analysis of lipid classes and long-chain polyunsaturated fatty acids. In Vitro Cell Dev. Biol. Anim. 2002, 38:557-565.
22. Kramer S.D., Schutz Y.B., Wunderli-Allenspach H., Abbott N.J., Begley D.J. Lipids in blood-brain barrier models in vitro. II. Influence of glial cells on lipid classes and lipid fatty acids. In Vitro Cell Dev. Biol. Anim. 2002, 38:566-571.
23. Langelier B., Alessandri J.M., Perruchot M.H., Guesnet P., Lavialle M. Changes of the transcriptional and fatty acid profiles in response to n-3 fatty acids in SH-SY5Y neuroblastoma cells. Lipids 2005, 40:719-728.
24. Lennon R., Welsh G.I., Singh A., Satchell S.C., Coward R.J., Tavaré J.M., Mathieson P.W., Saleem M.A. Rosiglitazone enhances glucose uptake in glomerular podocytes using the glucose transporter GLUT1. Diabetologia 2009, 52:1944-1952.
25. Leybaert L. Neurobarrier coupling in the brain: a partner of neurovascular and neurometabolic coupling?. J. Cereb. Blood Flow Metab. 2005, 25:2-16.
26. Moore S.A. Polyunsaturated fatty acid synthesis and release by brain-derived cells in vitro. J. Mol. Neurosci. 2001, 16:195-201.
27. Nakagawa S., Deli M.A., Kawaguchi H., Shimizudani T., Shimono T., Kittel A., Tanaka K., Niwa M. A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes. Neurochem. Int. 2009, 54:253-263.
28. Oudot F., Cordelet C., Sergiel J.P., Grynberg A. Polyunsaturated fatty acids influence prostanoid synthesis in vascular endothelial cells under hypoxia and reoxygenation. Int. J. Vitam. Nutr. Res. 1998, 68:263-271.
29. Ouellet M., Emond V., Chen C.T., Julien C., Bourasset F., Oddo S., Laferla F., Bazinet R.P., Calon F. Diffusion of docosahexaenoic and eicosapentaenoic acids through the blood-brain barrier: an in situ cerebral perfusion study. Neurochem. Int. 2009, 55:476-482.
30. Pardridge W.M. Drug delivery to the brain. J. Cereb. Blood Flow Metab. 1997, 17:713-731.
31. Pawlosky R.J., Ward G., Salem N. Essential fatty acid uptake and metabolism in the developing rodent brain. Lipids 1996, 31(Suppl):S103-S107.
32. Perriere N., Demeuse P., Garcia E., Regina A., Debray M., Andreux J.P., Couvreur P., Scherrmann J.M., Temsamani J., Couraud P.O., Deli M.A., Roux F. 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.
33. Pifferi F., Roux F., Langelier B., Alessandri J.M., Vancassel S., Jouin M., Lavialle M., Guesnet P. (n-3) polyunsaturated fatty acid deficiency reduces the expression of both isoforms of the brain glucose transporter GLUT1 in rats. J. Nutr. 2005, 135:2241-2246.
34. Pifferi F., Jouin M., Alessandri J.M., Haedke U., Roux F., Perrière N., Denis I., Lavialle M., Guesnet P. n-3 fatty acids modulate brain glucose transport in endothelial cells of the blood-brain barrier. Prostaglandins Leukot. Essent. Fatty Acids 2007, 77:279-286.
35. Qutub A.A., Hunt C.A. Glucose transport to the brain: a systems model. Brain Res. 2005, 49:595-617.
36. Rajah T.T., Olson A.L., Grammas P. Differential glucose uptake in retina- and brain-derived endothelial cells. Microvasc. Res. 2001, 62:236-242.
37. Régina A., Roux F., Revest P.A. Glucose transport in immortalized rat brain capillary endothelial cells in vitro: transport activity and GLUT1 expression. Biochim. Biophys. Acta 1997, 1335:135-143.
38. Roux F., Durieu-Trautmann O., Chaverot N., Claire M., Mailly P., Bourre J.M., Strosberg A.D., Couraud P.O. Regulation of gamma-glutamyl transpeptidase and alkaline phosphatase activities in immortalized rat brain microvessel endothelial cells. J. Cell Physiol. 1994, 15:101-113.
39. Roux F., Couraud P.O. Rat brain endothelial cell lines for the study of blood-brain barrier permeability and transport functions. Cell. Mol. Neurobiol. 2005, 25:41-58.
40. Spector A.A., Kaduce T.L., Hoak J.C., Fry G.L. Utilization of arachidonic and linoleic acids by cultured human endothelial cells. J. Clin. Invest. 1981, 68:1003-1011.
41. Ximenes, da Silva A., Lavialle F., Gendrot G., Guesnet P., Alessandri J.M., Lavialle M. Glucose transport and utilization are altered in the brain of rats deficient in n-3 polyunsaturated fatty acids. J. Neurochem. 2002, 81:1328-1337.
42. Yerram N.R., Moore S.A., Spector A.A. Eicosapentaenoic acid metabolism in brain microvessel endothelium: effect on prostaglandin formation. J. Lipid Res. 1989, 30:1747-1757.
43. Ziylan Z.Y., Bernard G.C., Lefauconnier J.M., Durand G.A., Bourre J.M. Effect of dietary n-3 fatty acid deficiency on blood-to-brain transfer of sucrose, alpha-aminoisobutyric acid and phenylalanine in the rat. Neurosci. Lett. 1992, 137:9-13.