Acute effects of short-chain alkylglycerols on blood-brain barrier properties of cultured brain endothelial cells

British Journal of Pharmacology

Volumn 169, Issue 7, 2013, Pages 1561-1573

  Hulper P ^a   Veszelka, S ^b   Walter, F R ^b   Wolburg, H ^c   Fallier Becker, P ^c   Piontek, J ^d,e   Blasig, I E ^d   Lakomek, M ^a   Kugler, W ^a   Deli, M A ^b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

blood brain barrier; brain endothelial cells; claudin 5; electron microscopy; permeability; short chain alkylglycerols; tight junctions; transendothelial electrical resistance

Indexed keywords

1 O PENTYLGLYCEROL; 2 O HEXYLDIGLYCEROL; ALKYLGLYCEROL DERIVATIVE; BETA CATENIN; CLAUDIN 5; FLUORESCEIN; GLYCEROL DERIVATIVE; TIGHT JUNCTION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CELL ASSAY; CELL CULTURE; CELL SIZE; CELL STRUCTURE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; ELECTRON MICROSCOPY; EXPERIMENTAL RAT; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE PERMEABILITY; MEMBRANE POLARIZATION AND DEPOLARIZATION; MEMBRANE STRUCTURE; MEMBRANE TRANSPORT; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; TRANS ISOMER;

BLOOD-BRAIN BARRIER; BRAIN ENDOTHELIAL CELLS; CLAUDIN-5; ELECTRON MICROSCOPY; PERMEABILITY; SHORT-CHAIN ALKYLGLYCEROLS; TIGHT JUNCTIONS; TRANSENDOTHELIAL ELECTRICAL RESISTANCE;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELL SURVIVAL; CELLS, CULTURED; CLAUDIN-5; CYTOSKELETON; ENDOTHELIAL CELLS; GLYCEROL; HEK293 CELLS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; PERMEABILITY; RATS; RATS, WISTAR; TIGHT JUNCTIONS;

EID: 84880259537     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12218     Document Type: Article

References (54)

1. Abbott NJ, Rönnbäck L, Hansson E, (2006). Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7: 41-53.
2. Anderson JM, Van Itallie CM, (2009). Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 1: a002584.
3. Artursson P, Ungell AL, Löfroth JE, (1993). Selective paracellular permeability in two models of intestinal absorption: cultured monolayers of human intestinal epithelial cells and rat intestinal segments. Pharm Res 10: 1123-1129.
4. Blasig IE, Winkler L, Lassowski B, Mueller SL, Zuleger N, Krause E, et al. (2006). On the self-association potential of transmembrane tight junction proteins. Cell Mol Life Sci 63: 505-514.
5. Bruewer M, Hopkins AM, Hobert ME, Nusrat A, Madara JL, (2004). RhoA, Rac1, and Cdc42 exert distinct effects on epithelial barrier via selective structural and biochemical modulation of junctional proteins and F-actin. Am J Physiol Cell Physiol 287: C327-C335.
6. Dejana E, Orsenigo F, Lampugnani MG, (2008). The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci 121: 2115-2122.
7. Deli MA, (2009). Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery. Biochim Biophys Acta 1788: 892-910.
8. Deli MA, (2011). Drug transport and the blood-brain barrier. In:, Tihanyi K, Vastag M, (eds). Solubility, Delivery, and ADME Problems of Drugs and Drug-Candidates. Washington: Bentham Science Publ. Ltd., pp. 144-165.
9. Deli MA, Dehouck MP, Ábrahám CS, Cecchelli R, Joõ F, (1995). Penetration of small molecular weight substances through cultured bovine brain capillary endothelial cell monolayers: the early effects of cyclic adenosine 3′,5′-monophosphate. Exp Physiol 80: 675-678.
10. Deli MA, Ábrahám CS, Kataoka Y, Niwa M, (2005). Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell Mol Neurobiol 25: 59-127.
11. Demeule M, Regina A, Che C, Poirier J, Nguyen T, Gabathuler R, et al. (2008). Identification and design of peptides as a new drug delivery system for the brain. J Pharmacol Exp Ther 324: 1064-1072.
12. Dhanikula RS, Argaw A, Bouchard JF, Hildgen P, (2008). Methotrexate loaded polyether-copolyester dendrimers for the treatment of gliomas: enhanced efficacy and intratumoral transport capability. Mol Pharm 5: 105-116.
13. Dodelet-Devillers A, Cayrol R, van Horssen J, Haqqani AS, de Vries HE, Engelhardt B, et al. (2009). Functions of lipid raft membrane microdomains at the blood-brain barrier. J Mol Med (Berl) 87: 765-774.
14. Doolittle ND, Miner ME, Hall WA, Siegal T, Jerome E, Osztie E, et al. (2000). Safety and efficacy of a multicenter study using intraarterial chemotherapy in conjunction with osmotic opening of the blood-brain barrier for the treatment of patients with malignant brain tumors. Cancer 88: 637-647.
15. Erdlenbruch B, Jendrossek V, Eibl H, Lakomek M, (2000). Transient and controllable opening of the blood-brain barrier to cytostatic and antibiotic agents by alkylglycerols in rats. Exp Brain Res 135: 417-422.
16. Erdlenbruch B, Jendrossek V, Kugler W, Eibl H, Lakomek M, (2002). Increased delivery of erucylphosphocholine to C6 gliomas by chemical opening of the blood-brain barrier using intracarotid pentylglycerol in rats. Cancer Chemother Pharmacol 50: 299-304.
17. Erdlenbruch B, Alipour M, Fricker G, Miller DS, Kugler W, Eibl H, et al. (2003a). Opening of the blood-brain barrier to small and large fluorescence markers in normal and C6 glioma bearing rats and isolated capillaries using intracarotid short chain alkylglycerols. Br J Pharmacol 140: 1201-1210.
18. Erdlenbruch B, Schinkhof C, Kugler W, Heinemann DEH, Herms J, Eibl H, et al. (2003b). Intraarterial short chain alkylglycerols for increased delivery of methotrexate to the rat brain. Br J Pharmacol 139: 685-694.
19. Erdlenbruch B, Kugler W, Schinkhof C, Neurath H, Eibl H, Lakomek M, (2005). Blood-brain barrier opening with alkylglycerols: biodistribution of 1-O-pentylglycerol after intravenous and intracarotid administration in rats. J Drug Target 13: 143-150.
20. Farkas A, Szatmári E, Orbõk A, Wilhelm I, Wejksza K, Nagyoszi P, et al. (2005). Hyperosmotic mannitol induces Src kinase-dependent phosphorylation of beta-catenin in cerebral endothelial cells. J Neurosci Res 80: 855-861.
21. Fellner F, Bauer B, Miller DS, Schaffrik M, Fankhänel M, Spruß T, et al. (2002). Transport of paclitaxel (Taxol) across the blood-brain barrier in vitro and in vivo. J Clin Invest 110: 1309-1318.
22. Fukumoto K, Takagi N, Yamamoto R, Moriyama Y, Takeo S, Tanonaka K, (2010). Prostanoid EP1 receptor antagonist reduces blood-brain barrier leakage after cerebral ischemia. Eur J Pharmacol 640: 82-86.
23. Furuse M, Sasaki H, Fujimoto K, Tsukita S, (1998). A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 143: 391-401.
24. Golden PL, Pollack GM, (2003). Blood-brain barrier efflux transport. J Pharm Sci 92: 1739-1753.
25. Greenwood J, Luthert PJ, Pratt OE, Lantos PL, (1988). Hyperosmolar opening of the blood-brain barrier in the energy-depleted rat brain. Part 1. Permeability studies. J Cereb Blood Flow Metab 8: 9-15.
26. Hartsock A, Nelson WJ, (2008). Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778: 660-669.
27. Hülper P, Dullin C, Kugler W, Lakomek M, Erdlenbruch B, (2011). Monitoring proteins using in vivo near-infrared time-domain optical imaging after 2-O-hexyldiglycerol-mediated transfer to the brain. Mol Imaging Biol 13: 275-283.
28. Ivanov AI, Hunt D, Utech M, Nusrat A, Parkos CA, (2005). Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol Biol Cell 16: 2636-2650.
29. Kemper EM, Boogerd W, Thuis E, Beijnen JH, van Tellingen O, (2004). Modulation of the blood-brain barrier in oncology: therapeutic opportunities for the treatment of brain tumors. Cancer Treat Rev 30: 415-423.
30. Knipp GT, Ho NF, Barsuhn CL, Borchardt RT, (1997). Paracellular diffusion in Caco-2 cell monolayers: effect of perturbation on the transport of hydrophilic compounds that vary in charge and size. J Pharm Sci 86: 1105-1110.
31. Krause G, Winkler L, Mueller SL, Haseloff RF, Piontek J, Blasig IE, (2008). Structure and function of claudins. Biochim Biophys Acta 1778: 631-645.
32. Krause G, Winkler L, Piehl C, Blasig I, Piontek J, Müller SL, (2009). Structure and function of extracellular claudin domains. Ann N Y Acad Sci 1165: 34-43.
33. Lai CH, Kuo KH, Leo JM, (2005). Critical role of actin in modulating BBB permeability. Brain Res Brain Res Rev 50: 7-13.
34. Madara JL, (1998). Regulation of the movement of solutes across tight junctions. Annu Rev Physiol 60: 143-159.
35. Neuwelt EA, Barnett PA, McCormick CI, Frenkel EP, Minna JD, (1985). Osmotic blood-brain barrier modification: monoclonal antibody, albumin, and methotrexate delivery to cerebrospinal fluid and brain. Neurosurgery 17: 419-423.
36. Noda K, Zhang J, Fukuhara S, Kunimoto S, Yoshimura M, Mochizuki N, (2010). Vascular endothelial-cadherin stabilizes at cell-cell junctions by anchoring to circumferential actin bundles through alpha- and beta-catenins in cyclic AMP-Epac-Rap1 signal-activated endothelial cells. Mol Biol Cell 21: 584-596.
37. O'Brien FE, Clarke G, Fitzgerald P, Dinan TG, Griffin BT, Cryan JF, (2012). Inhibition of P-glycoprotein enhances transport of imipramine across the blood-brain barrier: microdialysis studies in conscious freely moving rats. Br J Pharmacol 166: 1333-1343.
38. Pardridge WM, (2002). Drug and gene targeting to brain with molecular Trojan horses. Nat Rev Drug Discov 1: 131-139.
39. Perrière N, Demeuse PH, Garcia E, Regina A, Debray M, Andreux JP, et al. (2005). Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J Neurochem 93: 279-289.
40. Piehl C, Piontek J, Cording J, Wolburg H, Blasig IE, (2010). Participation of the second extracellular loop of claudin-5 in paracellular tightening against ions, small and large molecules. Cell Mol Life Sci 67: 2131-2140.
41. Piontek J, Winkler L, Wolburg H, Müller SL, Zuleger N, Piehl C, et al. (2008). Formation of tight junction: determinants of homophilic interaction between classic claudins. FASEB J 22: 146-158.
42. Piontek J, Fritzsche S, Cording JD, Richter S, Hartwig J, Walter M, et al. (2011). Elucidating the principles of the molecular organization of heteropolymeric tight junction strands. Cell Mol Life Sci 68: 3903-3918.
43. 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.
44. Rapoport SI, (2000). Osmotic opening of the blood-brain barrier: principles, mechanisms, and therapeutic applications. Cell Mol Neurobiol 20: 217-230.
45. Reardon DA, Rich JN, Friedman HS, Bigner DD, (2006). Recent advances in the treatment of malignant astrocytoma. J Clin Oncol 24: 1253-1265.
46. Reese TS, Karnovsky MJ, (1967). Fine structural localization of a blood-brain barrier to exogenous peroxidase. J Cell Biol 34: 207-217.
47. Rubin LL, Staddon JM, (1999). The cell biology of the blood-brain barrier. Annu Rev Neurosci 22: 11-28.
48. Siegal T, Rubinstein R, Bokstein F, Schwartz A, Lossos A, Shalom E, et al. (2000). In vivo assessment of the window of barrier opening after osmotic blood-brain barrier disruption in humans. J Neurosurg 92: 599-605.
49. Taddei A, Giampietro C, Conti A, Orsenigo F, Breviario F, Pirazzoli V, et al. (2008). Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat Cell Biol 10: 923-934.
50. Unger C, Eibl H, von Heyden HW, Kirsch B, Nagel GA, (1985). Blut-Hirn-Schranke und Penetration von Zytostatika. Klin Wochenschr 63: 565-571.
51. Veszelka S, Pásztõi M, Farkas AE, Krizbai I, Ngo TK, Niwa M, et al. (2007). Pentosan polysulfate protects brain endothelial cells against bacterial lipopolysaccharide-induced damages. Neurochem Int 50: 219-228.
52. Veszelka S, Kittel A, Deli MA, (2011). Tools of modelling blood-brain barrier penetrability. In:, Tihanyi K, Vastag M, (eds). Solubility, Delivery, and ADME Problems of Drugs and Drug-Candidates. Washington: Bentham Science Publ. Ltd., pp. 144-165.
53. van Vliet EA, Zibell G, Pekcec A, Schlichtiger J, Edelbroek PM, Holtman L, et al. (2010). COX-2 inhibition controls P-glycoprotein expression and promotes brain delivery of phenytoin in chronic epileptic rats. Neuropharmacology 58: 404-412.
54. Wolburg H, Neuhaus J, Kniesel U, Krauss B, Schmid EM, Öcalan M, (1994). Modulation of tight junction structure in blood-brain barrier endothelial cells. Effects of tissue culture, second messengers and cocultured astrocytes. J Cell Sci 107: 1347-1357.