Peroxisome proliferator-activated receptor-α activation protects brain capillary endothelial cells from oxygen-glucose deprivation-induced hyperpermeability in the blood-brain barrier

Current Neurovascular Research

Volumn 6, Issue 3, 2009, Pages 181-193

  Mysiorek, Caroline ^a,b,e   Culot, Maxime ^a,b,e   Dehouck, Lucie ^a,b,e   Derudas, Bruno ^a,c,d,e   Staels, Bart ^a,c,d,e   Bordet, Régis ^a,e   Cecchelli, Roméo ^a,b,e   Fenart, Laurence ^a,b,e   Berezowski, Vincent ^a,b,e,f  

^a UNIV LILLE   (France)

^b EA 2465   (France)

^c INSERM   (France)

^d IPL   (France)

^e IMPRT IFR114   (France)

^f UNIVERSITÉ D'ARTOIS   (France)

Author keywords

Blood brain barrier; Endothelium; In vitro model; Ischaemia; Neuroprotection; Peroxisome proliferator activated receptor alpha

Indexed keywords

ACYL COENZYME A; CARNITINE PALMITOYLTRANSFERASE I; ENDOTHELIN 1; FENOFIBRIC ACID; GLUCOSE; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; OXYGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PROTEIN PDK 4; PYRUVATE DEHYDROGENASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; CELL CULTURE; COCULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; GLIA CELL; IN VITRO STUDY; MEMBRANE PERMEABILITY; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; WILD TYPE;

EID: 68549107838     PISSN: 15672026     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720209788970081     Document Type: Article

References (50)

1. Aasum, E, Khalid, AM, Gudbrandsen, OA, How, OJ, Berge, RK, Larsen, TS. (2008) Fenofibrate modulates cardiac and hepatic metabolism and increases ischemic tolerance in diet-induced obese mice. J Mol Cell Cardiol 44: 201-209.
2. Abbott, NJ, Ronnback, L, Hansson, E. (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7: 41-53.
3. Amarenco, P. (2001) Hypercholesterolemia, lipid-lowering agents, and the risk for brain infarction. Neurology 57: S35-44.
4. Ayata, C, Ropper, AH. (2002) Ischaemic brain oedema. J Clin Neurosci 9: 113-124.
5. Benchenane, K, Berezowski, V, Fernandez-Monreal, M, Brillault, J, Valable, S, Dehouck, MP, Cecchelli, R, Vivien, D, Touzani, O, Ali, C. (2005a) Oxygen glucose deprivation switches the transport of tPA across the blood-brain barrier from an LRP-dependent to an increased LRP-independent process. Stroke 36: 1065-1070. (Pubitemid 40629303)
6. Benchenane, K, Berezowski, V, Ali, C, Fernandez-Monreal, M, Lopez- Atalaya, JP, Brillault, J, Chuquet, J, Nouvelot, A, MacKenzie, ET, Bu, G, Cecchelli, R, Touzani, O, Vivien, D. (2005b) Tissue-type plasminogen activator crosses the intact blood-brain barrier by lowdensity lipoprotein receptor-related protein-mediated transcytosis. Circulation 111: 2241-2249. (Pubitemid 40632441)
7. Berezowski, V, Landry, C, Dehouck, MP, Cecchelli, R, Fenart, L. (2004a) Contribution of glial cells and pericytes to the mRNA profiles of Pglycoprotein and multidrug resistance-associated proteins in an in vitro model of the blood-brain barrier. Brain Res 1018: 1-9. (Pubitemid 38942854)
8. Berezowski, V, Miecz, D, Marszalek, M, Broer, A, Broer, S, Cecchelli, R, Nalecz, KA. (2004b) Involvement of OCTN2 and B0,+ in the transport of carnitine through an in vitro model of the blood-brain barrier. J Neurochem 91: 860-872. (Pubitemid 39507363)
9. Betz, AL, Iannotti, F, Hoff, JT. (1989) Brain edema: a classification based on blood-brain barrier integrity. Cerebrovasc Brain Metab Rev 1: 133-154.
10. Bloomfield, RH, Davenport, J, Babikian, V, Brass, LM, Collins, D, Wexler, L, Wagner, S, Papademetriou, V, Rutan, G, Robins, SJ. (2001) Reduction in stroke with gemfibrozil in men with coronary heart disease and low HDL cholesterol: The Veterans Affairs HDL Intervention Trial (VA-HIT). Circulation 103: 2828-2833. (Pubitemid 32550072)
11. Booher, J, Sensenbrenner, M. (1972) Growth and cultivation of dissociated neurons and glial cells from embryonic chick, rat and human brain in flask cultures. Neurobiology 2: 97-105.
12. Bordet, R, Ouk, T, Petrault, O, Gele, P, Gautier, S, Laprais, M, Deplanque, D, Duriez, P, Staels, B, Fruchart, JC, Bastide, M. (2006) PPAR: a new pharmacological target for neuroprotection in stroke and neurodegenerative diseases. Biochem Soc Trans 34: 1341-1346. (Pubitemid 46769051)
13. Brillault, J, Berezowski, V, Cecchelli, R, Dehouck, MP. (2002) Intercommunications between brain capillary endothelial cells and glial cells increase the transcellular permeability of the blood-brain barrier during ischaemia. J Neurochem 83: 807-817. (Pubitemid 35316030)
14. Cecchelli, R, Berezowski, V, Lundquist, S, Culot, M, Renftel, M, Dehouck, MP, Fenart, L. (2007) Modelling of the blood-brain barrier in drug discovery and development. Nat Rev Drug Discov 6: 650-661. (Pubitemid 47202487)
15. Cecchelli, R, Dehouck, B, Descamps, L, Fenart, L, Buee-Scherrer, VV, Duhem, C, Lundquist, S, Rentfel, M, Torpier, G, Dehouck, MP. (1999) In vitro model for evaluating drug transport across the blood-brain barrier. Adv Drug Deliv Rev 36: 165-178.
16. Chen, J, Simon, R. (1997) Ischemic tolerance in the brain. Neurology 48: 306-311.
17. Coisne, C, Faveeuw, C, Delplace, Y, Dehouck, L, Miller, F, Cecchelli, R, Dehouck, B. (2006) Differential expression of selectins by mouse brain capillary endothelial cells in vitro in response to distinct inflammatory stimuli. Neurosci Lett 392: 216-220. (Pubitemid 41739628)
18. Coisne, C, Dehouck, L, Faveeuw, C, Delplace, Y, Miller, F, Landry, C, Morissette, C, Fenart, L, Cecchelli, R, Tremblay, P, Dehouck, B. (2005) Mouse syngenic in vitro blood-brain barrier model: a new tool to examine inflammatory events in cerebral endothelium. Lab Invest 85: 734-746. (Pubitemid 40799703)
19. Culman, J, Zhao, Y, Gohlke, P, Herdegen, T. (2007) PPAR-gamma: therapeutic target for ischemic stroke. Trends Pharmacol Sci 28: 244-249. (Pubitemid 46661003)
20. Culot, M, Lundquist, S, Vanuxeem, D, Nion, S, Landry, C, Delplace, Y, Dehouck, MP, Berezowski, V, Fenart, L, Cecchelli, R. (2008) An in vitro blood-brain barrier model for high throughput (HTS) toxicological screening. Toxicol In Vitro 22: 799-811.
21. Dehouck, B, Dehouck, MP, Fruchart, JC, Cecchelli, R. (1994) Upregulation of the low density lipoprotein receptor at the blood-brain barrier: intercommunications between brain capillary endothelial cells and astrocytes. J Cell Biol 126: 465-473. (Pubitemid 24226262)
22. Dehouck, MP, Meresse, S, Delorme, P, Fruchart, JC, Cecchelli, R. (1990) An easier, reproducible, and mass-production method to study the blood-brain barrier in vitro. J Neurochem 54: 1798-1801. (Pubitemid 20136746)
23. Dehouck, MP, Jolliet-Riant, P, Bree, F, Fruchart, JC, Cecchelli, R, Tillement, JP. (1992) Drug transfer across the blood-brain barrier: correlation between in vitro and in vivo models. J Neurochem 58: 1790-1797.
24. Deplanque, D, Gele, P, Petrault, O, Six, I, Furman, C, Bouly, M, Nion, S, Dupuis, B, Leys, D, Fruchart, JC, Cecchelli, R, Staels, B, Duriez, P, Bordet, R. (2003) Peroxisome proliferator-activated receptoralpha activation as a mechanism of preventive neuroprotection induced by chronic fenofibrate treatment. J Neurosci 23: 6264-6271. (Pubitemid 36875628)
25. Descamps, L, Dehouck, MP, Torpier, G, Cecchelli, R. (1996) Receptormediated transcytosis of transferrin through blood-brain barrier endothelial cells. Am J Physiol 270: H1149-1158. (Pubitemid 26135942)
26. Editorial (2005) Tackling the global burden of stroke. Lancet neurology 4: 689.
27. Fagan, SC, Hess, DC, Hohnadel, EJ, Pollock, DM, Ergul, A. (2004) Targets for vascular protection after acute ischemic stroke. Stroke 35: 2220-2225. (Pubitemid 39129589)
28. Fruchart, JC, Duriez, P, Staels, B. (1999) Peroxisome proliferator-activated receptor-alpha activators regulate genes governing lipoprotein metabolism, vascular inflammation and atherosclerosis. Curr Opin Lipidol 10: 245-257. (Pubitemid 29405915)
29. Gasche, Y, Copin, JC. (2003) [Blood-brain barrier pathophysiology and ischaemic brain oedema]. Ann Fr D'anesth Reanim 22: 312-319.
30. Green, AR. (2008) Pharmacological approaches to acute ischaemic stroke: reperfusion certainly, neuroprotection possibly. Br J Pharmacol 153 (Suppl 1): S325-338.
31. Hankey, GJ, Warlow, CP. (1999) Treatment and secondary prevention of stroke: evidence, costs, and effects on individuals and populations. Lancet 354: 1457-1463.
32. Huang, J, Upadhyay, UM, Tamargo, RJ. (2006) Inflammation in stroke and focal cerebral ischemia. Surg Neurol 66: 232-245. (Pubitemid 44279808)
33. Inoue, H, Jiang, XF, Katayama, T, Osada, S, Umesono, K, Namura S. (2003) Brain protection by resveratrol and fenofibrate against stroke requires peroxisome proliferator-activated receptor alpha in mice. Neurosci Lett 352: 203-206. (Pubitemid 38367603)
34. 2+-superoxide dismutase and decrease p22phox message expressions in primary endothelial cells. Metabolism 50: 3-11.
35. Iwashita, A, Muramatsu, Y, Yamazaki, T, Muramoto, M, Kita, Y, Yamazaki, S, Mihara, K, Moriguchi, A, Matsuoka, N. (2007) Neuroprotective efficacy of the peroxisome proliferator-activated receptor delta-selective agonists in vitro and in vivo. J Pharmacol Exp Ther 320: 1087-1096. (Pubitemid 46294065)
36. Jonas, S. (1995) Prophylactic pharmacologic neuroprotection against focal cerebral ischemia. Ann NY Acad Sci 765: 21-25; discussion 26-27.
37. Kuwabara, K, Murakami, K, Todo, M, Aoki, T, Asaki, T, Murai, M, Yano, J. (2004) A novel selective peroxisome proliferator-activated receptor alpha agonist, 2-methyl-c-5-[4-[5-methyl-2-(4-methylphenyl)-4- oxazolyl]butyl]-1,3- dioxane-r-2-carboxylic acid (NS-220), potently decreases plasma triglyceride and glucose levels and modifies lipoprotein profiles in KK-Ay mice. J Pharmacol Exp Ther 309: 970-977. (Pubitemid 38669682)
38. Lee, JM, Grabb, MC, Zipfel, GJ, Choi, DW. (2000) Brain tissue responses to ischemia. J Clin Invest 106: 723-731.
39. Liu, PC, Huber, R, Stow, MD, Schlingmann, KL, Collier, P, Liao, B, Link, J, Burn, TC, Hollis, G, Young, PR, Mukherjee, R. (2003) Induction of endogenous genes by peroxisome proliferator activated receptor alpha ligands in a human kidney cell line and in vivo. J Steroid Biochem Mol Biol 85: 71-79. (Pubitemid 36694279)
40. Lopez-Atalaya, JP, Roussel, BD, Ali, C, Maubert, E, Petersen, KU, Berezowski, V, Cecchelli, R, Orset, C, Vivien, D. (2007) Recombinant Desmodus rotundus salivary plasminogen activator crosses the blood-brain barrier through a low-density lipoprotein receptor-related protein-dependent mechanism without exerting neurotoxic effects. Stroke 38: 1036-1043. (Pubitemid 46568471)
41. Lundquist, S, Renftel, M, Brillault, J, Fenart, L, Cecchelli, R, Dehouck, MP. (2002) Prediction of drug transport through the blood-brain barrier in vivo: a comparison between two in vitro cell models. Pharm Res 19: 976-981. (Pubitemid 34804239)
42. NINDS (1995) Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med 333: 1581-1587.
43. NINDS (1997) Intracerebral hemorrhage after intravenous t-PA therapy for ischemic stroke. The NINDS t-PA Stroke Study Group. Stroke 28: 2109-2118.
44. Obrenovitch, TP. (2008) Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol Rev 88: 211-247.
45. Plateel, M, Teissier, E, Cecchelli, R. (1997) Hypoxia dramatically increases the nonspecific transport of blood-borne proteins to the brain. J Neurochem 68: 874-877. (Pubitemid 27044754)
46. Plateel, M, Dehouck, MP, Torpier, G, Cecchelli, R, Teissier, E. (1995) Hypoxia increases the susceptibility to oxidant stress and the permeability of the blood-brain barrier endothelial cell monolayer. J Neurochem 65: 2138-2145.
47. Savitz, SI, Fisher, M. (2007) Prophylactic neuroprotection. Curr Drug Targets 8: 846-849.
48. Simard, JM, Kent, TA, Chen, M, Tarasov, KV, Gerzanich, V. (2007) Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 6: 258-268. (Pubitemid 46228081)
49. Staels, B. (2007) PPAR agonists and the metabolic syndrome. Therapie 62: 319-326.
50. Zlokovic, BV. (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57: 178-201.