Uptake and transport of high-density lipoprotein (HDL) and HDL-associated α-tocopherol by an in vitro blood-brain barrier model

Journal of Neurochemistry

Volumn 89, Issue 4, 2004, Pages 939-950

  Balazs, Zoltan ^a,c   Panzenboeck, Ute ^a   Hammer, Astrid ^a   Sovic, Andrea ^a   Quehenberger, Oswald ^b   Malle, Ernst ^a   Sattler, Wolfgang ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

Author keywords

Brain capillary endothelial cells; Caveolin 1; Scavenger receptor class B type I; Transcytosis; Vitamin E

Indexed keywords

ALPHA TOCOPHEROL; APOLIPOPROTEIN A1; CAVEOLIN 1; HIGH DENSITY LIPOPROTEIN; METHYL BETA CYCLODEXTRIN; SCAVENGER RECEPTOR; BETA CYCLODEXTRIN DERIVATIVE; CAVEOLIN; CD36 ANTIGEN; CYCLODEXTRIN; IMMUNOGLOBULIN RECEPTOR; METHYL-BETA-CYCLODEXTRIN; SCAVENGER RECEPTOR B;

ANIMAL CELL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BIOTINYLATION; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; CAPILLARY ENDOTHELIUM; CAVEOLA; CULTURE MEDIUM; ENDOTHELIUM CELL; IN VITRO STUDY; LIPID TRANSPORT; NONHUMAN; PRIORITY JOURNAL; SWINE; ANIMAL; BIOLOGICAL MODEL; BRAIN; BRAIN LEVEL; CAPILLARY; CELL CULTURE; CELL FRACTIONATION; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALIA; SUIDAE; SUS SCROFA;

ALPHA-TOCOPHEROL; ANIMALS; ANTIGENS, CD36; APOLIPOPROTEIN A-I; BETA-CYCLODEXTRINS; BIOLOGICAL TRANSPORT; BIOTINYLATION; BLOOD-BRAIN BARRIER; BRAIN; BRAIN CHEMISTRY; CAPILLARIES; CAVEOLAE; CAVEOLIN 1; CAVEOLINS; CELL MEMBRANE; CELLS, CULTURED; CYCLODEXTRINS; ENDOTHELIAL CELLS; LIPOPROTEINS, HDL; MODELS, BIOLOGICAL; RECEPTORS, IMMUNOLOGIC; RECEPTORS, SCAVENGER; SCAVENGER RECEPTORS, CLASS B; SUBCELLULAR FRACTIONS; SWINE;

EID: 2542485364     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02373.x     Document Type: Article

References (61)

1. Acton S., Rigotti A., Landschulz K. T., Xu S., Hobbs H. H. and Krieger M. (1996) Identification of a scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271, 518-520.
2. Arlt S., Finckh B., Beisiegel U. and Kontush A. (2000) Time-course of oxidation of lipids in human cerebrospinal fluid in vitro. Free Radic. Res. 32, 103-114.
3. Assmann G., Schmitz G. and Brewer H. B. (1989) Familial high density lipoprotein deficiency: Tangier disease. In: The Metabolic Basis of Inherited Disease (Scriver C. R., Beaudet A. L., Sly W. S. and Valle D., eds), pp. 1267-1282. McGraw-Hill, New York.
4. Babitt J., Trigatti B., Rigotti A., Smart E. J., Anderson R. G. W., Xu S. and Krieger M. (1997) Murine SR-BI, a high density lipoprotein receptor that mediates selective lipid uptake, is N-glycosylated and fatty acid acylated and colocalizes with plasma membrane caveolae. J. Biol. Chem. 272, 13242-13249.
5. Ben Hamida C., Doerflinger N., Belal S. et al. (1993) Localization of Friedreichs ataxia phenotype with selective vitamin E deficiency to chromosome 8q by homozygosity mapping. Nat. Genet. 5, 195-200.
6. Bodzioch M., Orso E., Klucken J. et al. (1999) The gene encoding ATP-binding cassette transporter I is mutated in Tangier disease. Nat. Genet. 22, 347-351.
7. Borghini I., Barja F., Pometa D. and James R. W. (1995) Characterization of subpopulations of lipoprotein particles isolated from human cerebrospinal fluid. Biochim. Biophys. Acta 1255, 192-200.
8. Boyles J. K., Notterpek L. M. and Anderson L. J. (1990) Accumulation of apolipoproteins in the regenerating and remyelinating mammalian peripheral nerve. Identification of apolipoprotein D, apolipoprotein A-IV, apolipoprotein E, and apolipoprotein A-I. J. Biol. Chem. 265, 17805-17815.
9. Brooks-Wilson A., Marcil M., Clee S. M. et al. (1999) Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 22, 336-345.
10. Cavalier L., Ouahchi K., Kayden H. J., Di Donato S., Reutenauer L., Mandel J. L. and Koenig M. (1998) Ataxia with isolated vitamin E deficiency: heterogeneity of mutations and phenotypic variability in a large number of families. Am. J. Hum. Genet. 62, 301-310.
11. Danik M., Champagne D., Petit-Turcotte C., Beffert U. and Poirier J. (1999) Brain lipoprotein metabolism and its relation to neurodegenerative disease. Crit. Rev. Neurobiol. 13, 357-407.
12. Dehouck B., Dehouck M. P., Fruchart J. C. and Cecchelli R. (1994) Upregulation of the low-density lipoprotein receptor at the blood-brain barrier: intercommunications between capillary endothelial cells and astrocytes. J. Cell Biol. 126, 465-473.
13. Dehouck B., Fenart L., Dehouck M. P., Pierce A., Torpier G. and Cecchelli R. (1997) A new function for the LDL receptor: Transcytosis of LDL across the blood-brain barrier. J. Cell Biol. 138, 877-889.
14. Demeester N., Castro G., Desrumaux C. et al. (2000) Characterization and functional studies of lipoproteins, lipid transfer proteins, and lecithin: cholesterol acyltransferase in CSF of normal individuals and patients with Alzheimer's disease. J. Lipid Res. 41, 963-974.
15. Egger T., Hammer A., Wintersperger A., Goti D., Malle E. and Sattler W. (2001) Modulation of microglial superoxide production by α-tocopherol in vitro: attenuation of p67 (phox) translocation by a protein phosphatase-dependent pathway. J. Neurochem. 79, 1169-1182.
16. 3)-associated α-tocopherol is taken up by HepG2 cells via the selective uptake pathway and resecreted with endogenously synthesized apo-lipoprotein B-rich lipoprotein particles. Biochem. J. 332, 57-65.
17. Goti D., Hammer A., Galla H. J., Malle E. and Sattler W. (2000) Uptake of lipoprotein-associated α-tocopherol by primary porcine brain capillary endothelial cells. J. Neurochem. 74, 1374-1383.
18. Goti D., Hrzenjak A., Levak-Frank S., Frank S., van der Westhuyzen D. R., Malle E. and Sattler W. (2001) Porcine scavenger receptor class B, type I is expressed at the blood-brain barrier and contributes to selective uptake of HDL-associated Vitamin E. J. Neurochem. 76, 498-508.
19. Goti D., Balazs Z., Panzenboeck U., Hrzenjak A., Reicher H., Wagner E., Zechner R., Malle E. and Sattler W. (2002) Effects of lipoprotein lipase on uptake and transcytosis of low density lipoprotein (LDL) and LDL-associated αTocopherol in a porcine in vitro blood-brain barrier model. J. Biol. Chem. 277, 28537-28544.
20. Graf G. A., Connell P. M., van der Westhuyzen D. R. and Smart E. J. (1999) The class B, type I scavenger receptor promotes the selective uptake of high density lipoprotein cholesterol ethers into caveolae. J. Biol. Chem. 274, 12043-12048.
21. Husemann J. and Silverstein S. C. (2001) Expression of scavenger receptor class B, type I, by astrocytes and vascular smooth muscle cells in normal adult mouse and human brain and in Alzheimer's disease brain. Am. J. Pathol. 158, 825-832.
22. Jick H., Zornberg G. L., Jick S. S., Seshadri S. and Drachman D. A. (2000) Statins and the risk of dementia. Lancet 356, 1627-1631.
23. Kaempf-Rotzoll D. E., Traber M. G. and Arai H. (2003) Vitamin E and transfer proteins. Curr. Opin. Lipidol. 14, 249-254.
24. Koldamova R. P., Lefterov I. M., Lefterova M. I. and Lazo J. S. (2001) Apolipoprotein A-I directly interacts with amyloid precursor protein and inhibits A beta aggregation and toxicity. Biochemistry 40, 3553-3560.
25. Kontush A., Mann U., Arlt S., Ujeyl A., Luhrs C., Muller-Thomsen T. and Beisiegel U. (2001) Influence of vitamin E and C supplementation on lipoprotein oxidation in patients with Alzheimer's disease. Free Radic. Biol. Med. 31, 345-354.
26. Kozarsky K. F., Donahee M. H., Rigotti A., Iqbal S. N., Edelman E. R. and Krieger M. (1997) Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature 387, 414-417.
27. Liu P., Li W. P., Machleidt T. and Anderson R. G. W. (1999) Identification of caveolin-1 in lipoprotein particles secreted by exocrine cells. Nat. Cell Biol. 1, 369-375.
28. Liu P., Rudick M. and Anderson R. G. W. (2002) Multiple functions of caveolin-1. J. Biol. Chem. 277, 41295-41298.
29. Lowry O. H., Rosebrough N. J., Farr A. L. and Randall R. J. (1951) Protein measurement with the Folin reagent. J. Biol. Chem. 193, 265-275.
30. Mardones P., Strobel P., Miranda S., Leighton F., Quinones V., Amigo L., Rozowski J., Krieger M. and Rigotti A. (2002) Alpha-tocopherol metabolism is abnormal in scavenger receptor class B type I (SR-BI)-deficient mice. J. Nutr 132, 443-449.
31. Marmorstein A. D., Zurzolo C., Le Bivic A. and Rodriguez-Boulan E. (1998) Cell surface biotinylation techniques and determination of cell polarity. In: Cell Biology (Celis J. E., ed.), pp. 341-350. Academic Press, New York.
32. Matveev S., van der Westhuyzen D. R. and Smart E. J. (1999) Co-expression of scavenger receptor-BI and caveolin-1 is associated with enhanced selective cholesteryl ester uptake in THP-1 macrophages. J. Lipid Res. 40, 1647-1654.
33. Matveev S., Li X., Everson W. and Smart E. J. (2001) The role of caveolae and caveolin in vesicle-dependent and vesicle-independent trafficking. Adv. Drug Deliv. Rev. 49, 237-250.
34. Merched A., Xia Y., Visvikis S., Serot J. M. and Siest G. (2000) Decreased high-density lipoprotein cholesterol and serum apolipoprotein Al concentrations are highly correlated with the severity of Alzheimer's disease. Neurobiol. Aging 21, 27-30.
35. Mizuno T., Haass C., Michikawa M. and Yanagisawa K. (1998) Cholesterol-dependent generation of a unique amyloid β-protein from apically missorted amyloid precursor protein in MDCK cells. Biochim. Biophys. Acta 1373, 119-130.
36. Möckel B., Zinke H., Flach R., Weiß B., Weiler-Güttler, H. and Gassen H. G. (1994) Expression of apolipoprotein A-I in porcine brain endothelium in vitro. J. Neurochem. 62, 788-798.
37. Murao K., Terpstra V., Green S. R., Kondratenko, N., Steinberg D. and Quehenberger O. (1997) Characterization of CLA-1, a human homologue of rodent scavenger receptor BI, as a receptor for high density lipoprotein and apoptotic thymocytes. J. Biol. Chem. 272, 17551-17557.
38. Ness G. C. and Zhao Z. (1994) Thyroid hormone rapidly induces hepatic LDL receptor mRNA levels in hypophysectomized rats. Arch. Biochem. Biophys. 315, 199-202.
39. Oka N., Yamamoto M., Schwencke C., Kawabe J., Ebina T., Ohno S., Couet J., Lisanti M. P. and Ishikawa Y. (1997) Caveolin interaction with protein kinase C. Isoenzyme-dependent regulation of kinase activity by the caveolin scaffolding domain peptide. J. Biol. Chem. 272, 33416-33421.
40. Oram J. F. (2002) ATP-binding cassette transporter A1 and cholesterol trafficking. Curr. Opin. Lipidol. 13, 373-381.
41. Oram J. F. and Lawn R. M. (2001) ABCA1. The gatekeeper for eliminating excess tissue cholesterol. J. Lipid Res. 42, 1173-1179.
42. Oram J. F., Vaughan A. M. and Stocker R. (2001) ATP-binding cassette transporter Al mediates cellular secretion of alpha-tocopherol. J. Biol. Chem. 276, 39898-39902.
43. Orso E., Broccardo C., Kaminski W. E. et al. (2000) Transport of lipids from Golgi to plasma membrane is defective in Tangier disease patients and ABC1-deficient mice. Nat. Genet. 24, 192-196.
44. Ouahchi K., Arita M., Kayden H., Hentati F., Ben Hamida M., Sokol R., Arai H., Inoue K., Mandell J. L. and Koenig M. (1995) Ataxia with isolated vitamin E deficiency is caused by mutations in the α-tocopherol transfer protein. Nat. Genet. 9, 141-145.
45. Panzenbock U., Kritharides L., Raftery M., Rye K. A. and Stocker R. (2000) Oxidation of methionine residues to methionine sulfoxides does not decrease potential antiatherogenic properties of apolipoprotein A-I. J. Biol. Chem. 275, 19536-19544.
46. Panzenboeck U., Balazs Z., Sovic A., Hrzenjak A., Levak-Frank S., Wintersperger A., Malle E. and Sattler W. (2002) ABCA1 and SR-BI are modulators of reverse sterol transport at an in vitro blood-brain barrier constituted of porcine brain capillary endothelial cells. J. Biol. Chem. 277, 42781-42789.
47. Ricciarelli R., Tasinato A., Clement S., Özer N. K., Boscoboinik D. and Azzi A. (1998) α-Tocopherol specifically inactivates cellular protein kinase Ca by changing its phosphorylation state. Biochem. J. 334, 243-249.
48. Ricciarelli R., Zingg J. M. and Azzi A. (2001) Vitamin E: protective role of a Janus molecule. FASEB J. 15, 2314-2325.
49. Rist R. J., Romero I. A., Chan M. W., Couraud P. O., Roux F. and Abbott N. J. (1997) F-actin cytoskeleton and sucrose permeability of immortalised rat brain microvascular endothelial cell monolayers: effects of cyclic AMP and astrocytic factors. Brain Res. 768, 10-18.
50. Sattler W., Mohr D. and Stocker R. (1994) Rapid isolation of lipoproteins and assessment of their peroxidation by high-performance liquid chromatography postcolumn chemiluminescence. Meth. Enzymol. 233, 469-489.
51. Silver D. L., Wang N., Xiao X. and Tall A. R. (2001) High density lipoprotein (HDL) particle uptake mediated by scavenger receptor class B type 1 results in selective sorting of HDL cholesterol from protein and polarized cholesterol secretion. J. Biol. Chem. 276, 25287-25293.
52. Sinn H. J., Schrenk H. H., Friedrich E. A., Via D. P. and Dresel H. A. (1988) Radioiodination of proteins and lipoproteins using N-bromosuccinimide as oxidizing agent. Anal. Biochem. 170, 186-192.
53. Smart E. J., Ying Y. S., Donzell W. C. and Anderson R. G. W. (1996) A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J. Biol. Chem. 271, 29427-29435.
54. Smart E. J., Graf G. A., McNiven M. A., Sessa W. C., Engelman J. A., Scherer P. E., Okamoto T. and Lisanti M. P. (1999) Caveolins, liquid-ordered domains, and signal transduction. Mol. Cell. Biol. 19, 7289-7304.
55. Song K. S., Li S., Okamoto T., Quilliam, L. A., Sargiacomo M. and Lisanti M. P. (1996) Co-purification and direct interaction of ras with caveolin, an integral membrane protein of caveolae microdomains. J. Biol. Chem. 271, 9690-9697.
56. Song H., Saito K., Seishima M., Noma A., Urakami K. and Nakashima K. (1997) Cerebrospinal fluid apo E and apo A-I concentrations in early- and late-onset Alzheimer's disease. Neurosci. Lett. 231, 175-178.
57. Tewes B., Franke H., Hellwig S., Hoheisel D., Decker S., Griesche G., Tilling T., Wegener J. and Galla H. J. (1997) Preparation of endothelial cells in primary cultures obtained from brains of 6-month old pigs. In: Drug Transport Across the Blood-Brain Barrier (BBB): in Vivo and in Vitro Techniques (de Boer A. G. and Sutano W., eds), pp. 91-97, Harwood Academic Publisher, Amsterdam.
58. Uittenbogaard A., Everson W. V., Matveev S. V. and Smart E. J. (2002) Cholesteryl ester is transported from caveolae to internal membranes as part of a caveolin-annexin II lipid-protein complex. J. Biol. Chem. 277, 4925-4931.
59. de Vries H. E., Breedveld B., Kuiper J., de Boer A. G., van Berkel T. J. C. and Breimer D. D. (1995) High-density lipoprotein and cerebral endothelaial cells in vitro. Interacts. Transport. Biochem. Pharmacol. 50, 271-273.
60. Wolozin B., Kellman W., Ruosseau P., Celesia G. G. and Siegel G. (2000) Decreased prevalence of Alzheimer's disease associated with 3-hydroxy-3-methylglutaryl Coenzyme A reductase inhibitors. Arch. Neurol. 57, 1439-1443.
61. Yokota T., Igarashi K., Uchihara T. et al. (2001) Delayed-onset ataxia in mice lacking alpha-tocopherol transfer protein: model for neuronal degeneration caused by chronic oxidative stress. Proc. Natl Acad. Sci. USA 98, 15185-15190.