Mixed oligomers and monomeric amyloid-β disrupts endothelial cells integrity and reduces monomeric amyloid-β transport across hCMEC/D3 cell line as an in vitro blood-brain barrier model

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 9, 2014, Pages 1806-1815

  Qosa, Hisham ^a   LeVine, Harry ^b   Keller, Jeffrey N ^c   Kaddoumi, Amal ^a  

^a UNIVERSITY OF LOUISIANA AT MONROE   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Alzheimer's disease; Amyloid ; Blood brain barrier; Clearance

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; MEMBRANE PROTEIN; MONOMER; OLIGOMER;

AMYLOID PLAQUE; ARTICLE; BLOOD BRAIN BARRIER; CELL CULTURE; CELL LINE; CELL MEMBRANE PERMEABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN TRANSPORT; SPECIES; UPREGULATION; CELL VIABILITY; CYTOTOXICITY; PROTEIN EXPRESSION;

ALZHEIMER'S DISEASE; AMYLOID-Β; BLOOD-BRAIN BARRIER; CLEARANCE;

AMYLOID BETA-PEPTIDES; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; CELLS, CULTURED; DIMERIZATION; ENDOTHELIUM, VASCULAR; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MICROVESSELS; P-GLYCOPROTEINS; PLAQUE, AMYLOID; RECEPTORS, IMMUNOLOGIC;

EID: 84904480402     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.06.029     Document Type: Article

References (48)

1. Citron M. Alzheimer's disease: strategies for disease modification. Nat. Rev. Drug Discov. 2010, 9:387-398.
2. Huang Y., Mucke L. Alzheimer mechanisms and therapeutic strategies. Cell 2012, 148:1204-1222.
3. Ubhi K., Masliah E. Alzheimer's disease: recent advances and future perspectives. J. Alzheimers Dis. 2013, 33(Suppl. 1):S185-S194.
4. Selkoe D.J. Physiological production of the beta-amyloid protein and the mechanism of Alzheimer's disease. Trends Neurosci. 1993, 16:403-409.
5. Benilova I., Karran E., De Strooper B. The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nat. Neurosci. 2012, 15:349-357.
6. Finder V.H., Glockshuber R. Amyloid-beta aggregation. Neurodegener. Dis. 2007, 4:13-27.
7. Jan A., Hartley D.M., Lashuel H.A. Preparation and characterization of toxic Abeta aggregates for structural and functional studies in Alzheimer's disease research. Nat. Protoc. 2010, 5:1186-1209.
8. McLean C.A., Cherny R.A., Fraser F.W., Fuller S.J., Smith M.J., Beyreuther K., Bush A.I., Masters C.L. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 1999, 46:860-866.
9. Li S., Hong S., Shepardson N.E., Walsh D.M., Shankar G.M., Selkoe D. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009, 62:788-801.
10. Irizarry M.C., Soriano F., McNamara M., Page K.J., Schenk D., Games D., Hyman B.T. Abeta deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein V717F (PDAPP) transgenic mouse. J. Neurosci. 1997, 17:7053-7059.
11. Wang J., Dickson D.W., Trojanowski J.Q., Lee V.M. The levels of soluble versus insoluble brain Abeta distinguish Alzheimer's disease from normal and pathologic aging. Exp. Neurol. 1999, 158:328-337.
12. Irie K., Murakami K., Masuda Y., Morimoto A., Ohigashi H., Ohashi R., Takegoshi K., Nagao M., Shimizu T., Shirasawa T. Structure of beta-amyloid fibrils and its relevance to their neurotoxicity: implications for the pathogenesis of Alzheimer's disease. J. Biosci. Bioeng. 2005, 99:437-447.
13. Bell R.D., Zlokovic B.V. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol. 2009, 118:103-113.
14. Cirrito J.R., Deane R., Fagan A.M., Spinner M.L., Parsadanian M., Finn M.B., Jiang H., Prior J.L., Sagare A., Bales K.R., Paul S.M., Zlokovic B.V., Piwnica-Worms D., Holtzman D.M. P-glycoprotein deficiency at the blood-brain barrier increases amyloid-beta deposition in an Alzheimer disease mouse model. J. Clin. Invest. 2005, 115:3285-3290.
15. Deane R., Sagare A., Zlokovic B.V. The role of the cell surface LRP and soluble LRP in blood-brain barrier Abeta clearance in Alzheimer's disease. Curr. Pharm. Des. 2008, 14:1601-1605.
16. Qosa H., Abuznait A.H., Hill R.A., Kaddoumi A. Enhanced brain amyloid-beta clearance by rifampicin and caffeine as a possible protective mechanism against Alzheimer's disease. J. Alzheimers Dis. 2012, 31:151-165.
17. Deane R., Du Yan S., Submamaryan R.K., LaRue B., Jovanovic S., Hogg E., Welch D., Manness L., Lin C., Yu J., Zhu H., Ghiso J., Frangione B., Stern A., Schmidt A.M., Armstrong D.L., Arnold B., Liliensiek B., Nawroth P., Hofman F., Kindy M., Stern D., Zlokovic B. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat. Med. 2003, 9:907-913.
18. Gao W., Eisenhauer P.B., Conn K., Lynch J.A., Wells J.M., Ullman M.D., McKee A., Thatte H.S., Fine R.E. Insulin degrading enzyme is expressed in the human cerebrovascular endothelium and in cultured human cerebrovascular endothelial cells. Neurosci. Lett. 2004, 371:6-11.
19. Lynch J.A., George A.M., Eisenhauer P.B., Conn K., Gao W., Carreras I., Wells J.M., McKee A., Ullman M.D., Fine R.E. Insulin degrading enzyme is localized predominantly at the cell surface of polarized and unpolarized human cerebrovascular endothelial cell cultures. J. Neurosci. Res. 2006, 83:1262-1270.
20. Iwata N., Tsubuki S., Takaki Y., Watanabe K., Sekiguchi M., Hosoki E., Kawashima-Morishima M., Lee H.J., Hama E., Sekine-Aizawa Y., Saido T.C. Identification of the major Abeta1-42-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition. Nat. Med. 2000, 6:143-150.
21. Qosa H., Abuasal B.S., Romero I.A., Weksler B., Couraud P.O., Keller J.N., Kaddoumi A. Differences in amyloid-beta clearance across mouse and human blood-brain barrier models: kinetic analysis and mechanistic modeling. Neuropharmacology 2014, 79C:668-678.
22. Chen K.L., Wang S.S., Yang Y.Y., Yuan R.Y., Chen R.M., Hu C.J. The epigenetic effects of amyloid-beta(1-40) on global DNA and neprilysin genes in murine cerebral endothelial cells. Biochem. Biophys. Res. Commun. 2009, 378:57-61.
23. Kania K.D., Wijesuriya H.C., Hladky S.B., Barrand M.A. Beta amyloid effects on expression of multidrug efflux transporters in brain endothelial cells. Brain Res. 2011, 1418:1-11.
24. Carrano A., Hoozemans J.J., van der Vies S.M., Rozemuller A.J., van Horssen J., de Vries H.E. Amyloid Beta induces oxidative stress-mediated blood-brain barrier changes in capillary amyloid angiopathy. Antioxid. Redox Signal. 2011, 15:1167-1178.
25. Brenn A., Grube M., Peters M., Fischer A., Jedlitschky G., Kroemer H.K., Warzok R.W., Vogelgesang S. Beta-amyloid downregulates MDR1-P-glycoprotein (Abcb1) expression at the blood-brain barrier in mice. Int. J. Alzheimers Dis. 2011, 2011:690121.
26. Zlokovic B.V. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 2011, 12:723-738.
27. Forster C. Tight junctions and the modulation of barrier function in disease. Histochem. Cell Biol. 2008, 130:55-70.
28. Hartz A.M., Bauer B., Soldner E.L., Wolf A., Boy S., Backhaus R., Mihaljevic I., Bogdahn U., Klunemann H.H., Schuierer G., Schlachetzki F. Amyloid-beta contributes to blood-brain barrier leakage in transgenic human amyloid precursor protein mice and in humans with cerebral amyloid angiopathy. Stroke 2012, 43:514-523.
29. Gonzalez-Velasquez F.J., Kotarek J.A., Moss M.A. Soluble aggregates of the amyloid-beta protein selectively stimulate permeability in human brain microvascular endothelial monolayers. J. Neurochem. 2008, 107:466-477.
30. Tai L.M., Holloway K.A., Male D.K., Loughlin A.J., Romero I.A. Amyloid-beta-induced occludin down-regulation and increased permeability in human brain endothelial cells is mediated by MAPK activation. J. Cell. Mol. Med. 2010, 14:1101-1112.
31. Rensink A.A., de Waal R.M., Kremer B., Verbeek M.M. Pathogenesis of cerebral amyloid angiopathy. Brain Res. Brain Res. Rev. 2003, 43:207-223.
32. Klein W.L. Abeta toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem. Int. 2002, 41:345-352.
33. LeVine H. Alzheimer's beta-peptide oligomer formation at physiologic concentrations. Anal. Biochem. 2004, 335:81-90.
34. Cooray H.C., Shahi S., Cahn A.P., van Veen H.W., Hladky S.B., Barrand M.A. Modulation of p-glycoprotein and breast cancer resistance protein by some prescribed corticosteroids. Eur. J. Pharmacol. 2006, 531:25-33.
35. Weksler B.B., Subileau E.A., Perriere N., Charneau P., Holloway K., Leveque M., Tricoire-Leignel H., Nicotra A., Bourdoulous S., Turowski P., Male D.K., Roux F., Greenwood J., Romero I.A., Couraud P.O. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 2005, 19:1872-1874.
36. Omidi Y., Campbell L., Barar J., Connell D., Akhtar S., Gumbleton M. Evaluation of the immortalised mouse brain capillary endothelial cell line, b.End3, as an in vitro blood-brain barrier model for drug uptake and transport studies. Brain Res. 2003, 990:95-112.
37. Nazer B., Hong S., Selkoe D.J. LRP promotes endocytosis and degradation, but not transcytosis, of the amyloid-beta peptide in a blood-brain barrier in vitro model. Neurobiol. Dis. 2008, 30:94-102.
38. Shibata M., Yamada S., Kumar S.R., Calero M., Bading J., Frangione B., Holtzman D.M., Miller C.A., Strickland D.K., Ghiso J., Zlokovic B.V. Clearance of Alzheimer's amyloid-ss(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J. Clin. Invest. 2000, 106:1489-1499.
39. Hardy J. The amyloid hypothesis for Alzheimer's disease: a critical reappraisal. J. Neurochem. 2009, 110:1129-1134.
40. Hepler R.W., Grimm K.M., Nahas D.D., Breese R., Dodson E.C., Acton P., Keller P.M., Yeager M., Wang H., Shughrue P., Kinney G., Joyce J.G. Solution state characterization of amyloid beta-derived diffusible ligands. Biochemistry 2006, 45:15157-15167.
41. Shankar G.M., Leissring M.A., Adame A., Sun X., Spooner E., Masliah E., Selkoe D.J., Lemere C.A., Walsh D.M. Biochemical and immunohistochemical analysis of an Alzheimer's disease mouse model reveals the presence of multiple cerebral Abeta assembly forms throughout life. Neurobiol. Dis. 2009, 36:293-302.
42. Steinerman J.R., Irizarry M., Scarmeas N., Raju S., Brandt J., Albert M., Blacker D., Hyman B., Stern Y. Distinct pools of beta-amyloid in Alzheimer disease-affected brain: a clinicopathologic study. Arch. Neurol. 2008, 65:906-912.
43. Kawarabayashi T., Younkin L.H., Saido T.C., Shoji M., Ashe K.H., Younkin S.G. Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J. Neurosci. 2001, 21:372-381.
44. Cecchelli R., Berezowski V., Lundquist S., Culot M., Renftel M., Dehouck M.P., Fenart L. Modelling of the blood-brain barrier in drug discovery and development. Nat. Rev. Drug Discov. 2007, 6:650-661.
45. Poller B., Gutmann H., Krahenbuhl S., Weksler B., Romero I., Couraud P.O., Tuffin G., Drewe J., Huwyler J. The human brain endothelial cell line hCMEC/D3 as a human blood-brain barrier model for drug transport studies. J. Neurochem. 2008, 107:1358-1368.
46. Gravina S.A., Ho L., Eckman C.B., Long K.E., Otvos L., Younkin L.H., Suzuki N., Younkin S.G. Amyloid beta protein (A beta) in Alzheimer's disease brain. Biochemical and immunocytochemical analysis with antibodies specific for forms ending at A beta 40 or A beta 42(43). J. Biol. Chem. 1995, 270:7013-7016.
47. Marco S., Skaper S.D. Amyloid beta-peptide1-42 alters tight junction protein distribution and expression in brain microvessel endothelial cells. Neurosci. Lett. 2006, 401:219-224.
48. Villain N., Chetelat G., Grassiot B., Bourgeat P., Jones G., Ellis K.A., Ames D., Martins R.N., Eustache F., Salvado O., Masters C.L., Rowe C.C., Villemagne V.L. Regional dynamics of amyloid-beta deposition in healthy elderly, mild cognitive impairment and Alzheimer's disease: a voxelwise PiB-PET longitudinal study. Brain 2012, 135:2126-2139.