Human blood-brain barrier receptors for Alzheimer's amyloid-β 1-40. Asymmetrical binding, endocytosis, and transcytosis at the apical side of brain microvascular endothelial cell monolayer

Journal of Clinical Investigation

Volumn 102, Issue 4, 1998, Pages 734-743

  Mackic, Jasmina B ^a   Stins, Monique ^a   McComb, J Gordon ^a   Calero, Miguel ^b   Ghiso, Jorge ^b   Kim, Kwang Sik ^a   Yan, Shi Du ^c   Stern, David ^c   Schmidt, Ann Marie ^c   Frangione, Blas ^b   Zlokovic, Berislav V ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^c Columbia University ^*  (United States)

Author keywords

Amyloidosis; A peptide; Central nervous system; Cerebrovascular; Transporter

Indexed keywords

AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; AMYLOIDOSIS; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; NEUROPATHOLOGY; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY;

EID: 0032529151     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI2029     Document Type: Article

References (51)

1. Wisniewski, T., J. Ghiso, and B. Frangione. 1997. Biology of Aβ amyloid in Alzheimer's Disease. Neurobiol. Dis. 4:311-328.
2. Dickson, D.W. 1997. The pathogenesis of senile plaques. J. Neuropathol. Exp. Neurol. 56:321-339.
3. Mattson, M.P., and R.E. Rydel. 1996. Amyloid ox-tox transducers. Nature. 382:674-675.
4. Yan, S.D., X. Chen, J. Fu, M. Chen, H. Zhu, A. Roher, T. Slattery, L. Zhao, M. Nagashima, J. Morser, A. Migheli, et al. 1996. RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature. 382:685-691.
5. El Khoury, J., S.E. Hickman, C.A. Thomas, L. Cao, S.C. Silverstein, and J.D. Loike. 1996. Scavenger receptor-mediated adhesion of microglia to β-amyloid fibrils. Nature. 382:716-719.
6. Citron, M., T.S. Diehl, G. Gordon, A.L. Biere, P. Seubert, and D.J. Selkoe. 1996. Evidence that the 42-and 40-amino acid forms of amyloid β protein are generated from the β-amyloid precursor protein by different protease activities. Proc. Natl. Acad. Sci. USA. 93:13170-13175.
7. Seubert, P., C. Vigo-Pelfrey, F. Esch, M. Lee, H. Dovey, D. Davis, S. Sinha, M. Schlossmacher, J. Whaley, C. Swindlehurst, et al. 1992. Isolation and quantification of soluble Alzheimer's β-peptide from biological fluids. Nature. 359:325-327.
8. Shoji, M., T. Golde, J. Ghiso, T. Cheung, S. Estus, L. Shaffer, X.D. Cai, D. McKay, R. Tintner, B. Frangione, and S. Younkin. 1992. Production of the Alzheimer amyloid β protein by normal proteolytic processing. Science. 258: 126-129.
9. Tabaton, M., M.G. Nunzi, R. Xue, M. Usiak, L. Autilio-Gambetti, and P. Gambetti. 1994. Soluble amyloid beta-protein is a marker of Alzheimer amyloid in brain but not in cerebrospinal fluid. Biochem. Biophys. Rev. Commun. 200:1598-1603.
10. Suzuki, N., T. Iwatsubo, A. Odaka, Y. Ishibashi, C. Kitada, and Y. Ihara. 1994. High tissue content of soluble beta 1-40 is linked to cerebral amyloid angiopathy. Am. J. Pathol. 145:452-460.
11. Castaño, E.M., F. Prelli, C. Soto, R. Beavis, E. Matsubara, M. Shoji, and B. Frangione. 1996. The length of amyloid-beta in hereditary cerebral hemorrhage with amyloidosis. Dutch type. Implications for the role of amyloid-β 1-42 in Alzheimer's disease. J. Biol. Chem. 271:32185-32191.
12. Masters, C.L., G. Simms, N.A. Weinman, G. Multhaup, B.L. McDonald, and K. Beyreuther. 1985. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. USA. 82:4245-4249.
13. Prior, R., D. Durso, R. Frank, I. Prikulis, S. Cleven, R. Ihl, and G. Pavlakovic. 1996. Selective binding of soluble Aβ1-40 and Aβ1-42 to a subset of senile plaques. Am. J. Pathol. 148:1749-1756.
14. Zlokovic, B.V. 1997. Can blood-brain barrier play a role in the development of cerebral amyloidosis and Alzheimer's disease pathology? Neurobiol. Dis. 4:23-26.
15. Pardridge, W.M. 1986. Receptor-mediated peptide transport through the blood-brain barrier. Endocr. Rev. 7:314-330.
16. Takakura, Y., K.L. Audus, and R.T. Borchardt. 1991. Blood-brain barrier: transport studies in isolated brain capillaries and in cultured brain endothelial cells. In Advances in Pharmacology, Volume 22. Academic Press, New York. 137-164.
17. Banks, W.A., A.J. Kastin, and C.M. Barrera. 1991. Delivering peptides to the central nervous system: dilemmas and strategies. Pharmacol. Res. 8: 1345-1350.
18. Banks, W.A., A.J. Horvath, and E.A. Michals. 1987. Carrier-mediated transport of vasopressin across the blood-brain barrier of the mouse. J. Neurosci. Res. 18:326-332.
19. Zlokovic, B.V. 1995. Cerebrovascular permeability to peptides: manipulations of transport systems at the blood-brain barrier. Pharmacol. Res. 12: 1395-1406.
20. Zlokovic, B.V., J. Ghiso, J.B. Mackic, J.G. McComb, M.H. Weiss, and B. Frangione. 1993. Blood-brain barrier transport of circulating Alzheimer's amyloid β. Biochem. Biophys. Res. Commun. 197:1034-1040.
21. Poduslo, J.F., G.L. Curran, J.J. Haggard, A.L. Biere, and D.J. Selkoe. 1997. Permeability and residual plasma volume of human, Dutch variant, and rat amyloid β-protein 1-40 at the blood-brain barrier. Neurobiol. Dis. 4:27-34.
22. Mackic, J.B., M.H. Weiss, W. Miao, J. Ghiso, M. Calero, J. Bading, B. Frangione, and B.V. Zlokovic. 1998. Cerebrovascular accumulation and increased blood-brain barrier permeability to circulating Alzheimer's amyloid β-peptide in aged squirrel monkey with cerebral amyloid angiopathy. J. Neurochem. 70:210-215.
23. 1-40 labels amyloid deposits in the aged primate brain in vivo. Neuroreport. 7:2607-2611.
24. Stins, M.F., F. Gilles, and K.S. Kim. 1997. Selective expression of adhesion molecules on human brain microvascular endothelial cells. J. Neuroimmunol. 76:81-90.
25. Persidsky, Y., M. Stins, D. Way, M.H. Witte, M. Weinand, K.S. Kim, P. Bock, H.E. Gendelman, and M. Fiala. 1997. A model for monocyte migration through the blood-brain barrier during HIV-1 encephalitis. J. Immunol. 158: 3499-3510.
26. Fiala, M., M.F. Stins, D.J. Looney, P. Shapshank, A. Diagne, M.C. Graves, D.L. Way, O. Martinez, M.H. Witte, M. Weinard, and K.S. Kim. 1997. Penetration of HIV-1 across a blood-brain barrier model is enhanced by tumor necrosis factor α. Mol. Med. 3:553-564.
27. 125I-insulin in adipocytes and IM-9 lymphocytes. J. Biol. Chem. 257: 8667-8673.
28. Gibson, A.E., R.J. Noel, J.T. Herlihy, and W.F. Ward. 1989. Phenylarsine oxide inhibition of endocytosis: effects of asialofetuin internalization. Am. J. Physiol. 257:C182-C184.
29. Moss, A.L., and W.F. Ward. 1991. Multiple pathways for ligand internalization in rat hepatocytes I: effects of anoxia, phenylarsine oxide and monensin. J. Cell. Physiol. 149:313-318.
30. Miller, D.W., B.T. Keller, and R.T. Borchardt. 1994. Identification and distribution of insulin receptors on cultured bovine brain microvessel endothelial cells: possible function in insulin processing in the blood-brain barrier. J. Cell. Phys. 161:333-341.
31. Terasaki, T., K. Hirai, H. Sato, Y.S. Kang, and A. Tsuji. 1989. Absorptive-mediated endocytosis of a dynorphin-like analgesic peptide, E-2078 into the blood-brain barrier. J. Exp. Pharmacol. Ther. 251:352-357.
32. Martel, C.L., J.B. Mackic, E. Matsubara, S. Governale, C. Miguel, W. Miao, J.G. McComb, B. Frangione, J. Ghiso, and B.V. Zlokovic. 1997. Isoform-specific effects of apolipoproteins E2, E3, E4 on cerebral capillary sequestration and blood-brain barrier transport of circulating Alzheimer's amyloid β. J. Neurochem. 69:1995-2004.
33. Lowry, O.H., N.J. Rosebrough, A.L. Farr, and R.J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
34. Feldman, H.A. 1972. Mathematical theory of complex ligand-binding systems of equilibrium: some methods for parameter fitting. Anal. Biochem. 48: 317-338.
35. Yan, S.D., J. Fu, C. Soto, X. Chen, H. Zhu, F. Al-Mohanna, K. Collison, A. Zhu, E. Stern, T. Saido, et al. 1997. ERAB: a novel intracellular amyloid-beta peptide binding protein which mediates neurotoxicity in Alzheimer's disease. Nature. 381:689-695.
36. Hsu, H.-Y., D. Hajjar, K. Khan, and D. Falcone. 1998. Ligand binding to macrophage scavenger receptor A induces urokinase-type plasminogen activator expression by a protein kinase-dependent signaling pathway. J. Biol. 273: 1240-1246.
37. Klotz, I., and D. Hunston. 1984. Mathematical models for ligand receptor binding. J. Biol. Chem. 258:11442-11445.
38. Zlokovic, B.V., C.L. Martel, E. Matsubara, J.G. McComb, G. Zheng, R.T. McClusky, B. Frangione, and J. Ghiso. 1996. Glycoprotein 330/megalin: probable role in receptor-mediated transport of apolipoproetin J alone and in complex with Alzheimer's disease amyloid β at the blood-brain and blood-cerebrospinal fluid barriers. Proc. Natl. Acad. Sci. USA. 93:4229-4236.
39. Lucarelli, M., M. Gennarelli, R. Cardeli, G. Novelli, S. Scarpa, B. Dallapiccola, and R. Storm. 1997. Expression of receptors for native and chemically modified low-density lipoproteins in brain microvessels. FEBS Lett. 401:53-58.
40. Dehouck, B., L. Fenart, M.P. Dehouck, A. Pierce, G. Torpier, and R. Cecchelli. 1997. A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier. J. Cell Biol. 138:877-889.
41. Golden, P.L., T.J. Maccagnan, and W.M. Pardridge. 1997. Human blood-brain barrier leptin receptor: binding and endocytosis in isolated human brain microvessels. J. Clin. Invest. 99:14-18.
42. Goldstein, G.W., A.L. Betz, and P.D. Dowman. 1984. Use of isolated brain capillaries and cultured endothelial cells to study the blood-brain barrier. Fed. Proc. 43:191-195.
43. Ghersi-Egea, J.F., P.D. Gorevic, J. Ghiso, B.F. Frangione, C.S. Patlak, and J.D. Fenstermacher. 1996. Fate of cerebrospinal fluid-borne amyloid β-peptide: rapid clearance into blood and appreciable accumulation by cerebral arteries. J. Neurochem. 67:880-883.
44. Maness, L.M., W.A. Banks, M.B. Podlisny, D.J. Selkoe, and A.J. Kastin. 1994. Passage of human amyloid-β protein 1-40 across the murine blood-brain barrier. Life Sci. 55:1643-1650.
45. Gajdusek, D.C. 1988. Transmissible and non-transmissible amyloidoses: autocatalytic post-translational conversion of host precursor proteins to β-pleated configurations. J. Neuroimmunol. 20:95-110.
46. Jarrett, J.T., and P.T. Lansbury, Jr. 1993. Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell. 73:1055-1058.
47. Soto, C., and B. Frangione. 1995. Two conformational states of amyloid β-peptide: implications for the pathogenesis of Alzheimer's disease. Neurosci. Lett. 186:115-118.
48. Thomas, T., G. Thomas, C. McLendon, T. Sutton, and M. Mullan. 1996. β-Amyloid-mediated vasoactivity and vascular endothelial damage. Nature. 380:168-171.
49. Thomas, T., E.T. Sutton, M.W. Bryant, and J.A.G. Rhodin. 1997. In vivo vascular damage, leukocyte activation and inflammatory response induced by β-amyloid. J. Submicrosc. Cytol. Pathol. 29:293-304.
50. Shayo, M., R.N. McLay, A.J. Kastin, and W.A. Banks. 1997. The putative blood-brain barrier transporter for the β-amyloid binding protein apolipoprotein J is saturated at physiological concentrations. Life Sci. 60:115-118.
51. Schmidt, A.M., M. Hasu, D. Popov, J.H. Zhang, J. Chen, S.D. Yan, J. Brett, R. Cao, K. Kuwabara, G. Gostache, et al. 1994. Receptor for advanced glycation end products (AGE) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. Proc. Natl. Acad. Sci. USA. 91:8807-8811.