Traffic jam at the blood-brain barrier promotes greater accumulation of Alzheimer's disease amyloid-β proteins in the cerebral vasculature

Molecular Pharmaceutics

Volumn 10, Issue 5, 2013, Pages 1557-1565

  Agyare, Edward K ^a   Leonard, Sarah R ^b   Curran, Geoffry L ^c   Yu, Caroline C ^d   Lowe, Val J ^e   Paravastu, Anant K ^b   Poduslo, Joseph F ^c   Kandimalla, Karunya K ^a,c,f  

^a FLORIDA A AND M UNIVERSITY   (United States)

^b FAMU FSU COLLEGE OF ENGINEERING   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

^d Cell Applications Inc   (United States)

^e MAYO CLINIC   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Alzheimer's disease; amyloid beta proteins; blood brain barrier; cerebral amyloid angiopathy; transcytosis

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID BETA PROTEIN; MUTANT PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN; BRAIN BLOOD VESSEL; BRAIN CORTEX; BRAIN STEM; CAUDATE NUCLEUS; CEREBELLUM; HIPPOCAMPUS; MATHEMATICAL MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; THALAMUS; TRANSCYTOSIS; VASCULAR AMYLOIDOSIS; VASCULAR ENDOTHELIUM; ANIMAL; BIOLOGICAL MODEL; BLOOD; BOVINE; CELL CULTURE; ENDOTHELIUM CELL; GENETICS; HUMAN; METABOLISM; PROTEIN TRANSPORT;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BLOOD-BRAIN BARRIER; CATTLE; CELLS, CULTURED; CEREBRAL AMYLOID ANGIOPATHY, FAMILIAL; ENDOTHELIAL CELLS; HUMANS; MODELS, NEUROLOGICAL; MUTANT PROTEINS; PROTEIN TRANSPORT; TRANSCYTOSIS;

EID: 84877280219     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300352c     Document Type: Article

References (29)

1. Rensink, A. A.; de Waal, R. M.; Kremer, B.; Verbeek, M. M. Pathogenesis of cerebral amyloid angiopathy Brain Res. Rev. 2003, 43 (2) 207-23
2. Hirohata, M.; Yoshita, M.; Ishida, C.; Ikeda, S. I.; Tamaoka, A.; Kuzuhara, S.; Shoji, M.; Ando, Y.; Tokuda, T.; Yamada, M. Clinical features of non-hypertensive lobar intracerebral hemorrhage related to cerebral amyloid angiopathy Eur. J. Neurol. 2010, 17 (6) 823-9
3. Jellinger, K. A. Alzheimer disease and cerebrovascular pathology: an update J. Neural Transm. 2002, 109 (5-6) 813-36
4. Rosenblum, W. I.; Haider, A. Negative correlations between parenchymal amyloid and vascular amyloid in hippocampus Am. J. Pathol. 1988, 130 (3) 532-6
5. Alonzo, N. C.; Hyman, B. T.; Rebeck, G. W.; Greenberg, S. M. Progression of cerebral amyloid angiopathy: accumulation of amyloid-beta40 in affected vessels J. Neuropathol. Exp. Neurol. 1998, 57 (4) 353-9
6. Fryer, J. D.; Simmons, K.; Parsadanian, M.; Bales, K. R.; Paul, S. M.; Sullivan, P. M.; Holtzman, D. M. Human apolipoprotein E4 alters the amyloid-beta 40:42 ratio and promotes the formation of cerebral amyloid angiopathy in an amyloid precursor protein transgenic model J. Neurosci. 2005, 25 (11) 2803-10
7. Wilcock, D. M.; Colton, C. A. Immunotherapy, vascular pathology, and microhemorrhages in transgenic mice CNS Neurol. Disord.: Drug Targets 2009, 8 (1) 50-64
8. Herzig, M. C.; Van Nostrand, W. E.; Jucker, M. Mechanism of cerebral beta-amyloid angiopathy: murine and cellular models Brain Pathol. 2006, 16 (1) 40-54
9. De Jonghe, C.; Esselens, C.; Kumar-Singh, S.; Craessaerts, K.; Serneels, S.; Checler, F.; Annaert, W.; Van Broeckhoven, C.; De Strooper, B. Pathogenic APP mutations near the gamma-secretase cleavage site differentially affect Abeta secretion and APP C-terminal fragment stability Hum. Mol. Genet. 2001, 10 (16) 1665-71
10. Suzuki, N.; Cheung, T. T.; Cai, X. D.; Odaka, A.; Otvos, L., Jr.; Eckman, C.; Golde, T. E.; Younkin, S. G. An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants Science 1994, 264 (5163) 1336-40
11. Murrell, J.; Farlow, M.; Ghetti, B.; Benson, M. D. A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease Science 1991, 254 (5028) 97-9
12. Herzig, M. C.; Winkler, D. T.; Burgermeister, P.; Pfeifer, M.; Kohler, E.; Schmidt, S. D.; Danner, S.; Abramowski, D.; Sturchler-Pierrat, C.; Burki, K.; van Duinen, S. G.; Maat-Schieman, M. L.; Staufenbiel, M.; Mathews, P. M.; Jucker, M. Abeta is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis Nat. Neurosci. 2004, 7 (9) 954-60
13. Bugiani, O.; Giaccone, G.; Rossi, G.; Mangieri, M.; Capobianco, R.; Morbin, M.; Mazzoleni, G.; Cupidi, C.; Marcon, G.; Giovagnoli, A.; Bizzi, A.; Di Fede, G.; Puoti, G.; Carella, F.; Salmaggi, A.; Romorini, A.; Patruno, G. M.; Magoni, M.; Padovani, A.; Tagliavini, F. Hereditary cerebral hemorrhage with amyloidosis associated with the E693K mutation of APP Arch. Neurol. 2010, 67 (8) 987-95
14. Pezzini, A.; Del Zotto, E.; Volonghi, I.; Giossi, A.; Costa, P.; Padovani, A. Cerebral amyloid angiopathy: a common cause of cerebral hemorrhage Curr. Med. Chem. 2009, 16 (20) 2498-513
15. Mullan, M.; Crawford, F.; Axelman, K.; Houlden, H.; Lilius, L.; Winblad, B.; Lannfelt, L. A pathogenic mutation for probable Alzheimer's disease in the APP gene at the N-terminus of beta-amyloid Nat. Genet. 1992, 1 (5) 345-7
16. Kumar-Singh, S.; Cras, P.; Wang, R.; Kros, J. M.; van Swieten, J.; Lubke, U.; Ceuterick, C.; Serneels, S.; Vennekens, K.; Timmermans, J. P.; Van Marck, E.; Martin, J. J.; van Duijn, C. M.; Van Broeckhoven, C. Dense-core senile plaques in the Flemish variant of Alzheimer's disease are vasocentric Am. J. Pathol. 2002, 161 (2) 507-20
17. Bornebroek, M.; De Jonghe, C.; Haan, J.; Kumar-Singh, S.; Younkin, S.; Roos, R.; Van Broeckhoven, C. Hereditary cerebral hemorrhage with amyloidosis Dutch type (AbetaPP 693): decreased plasma amyloid-beta 42 concentration Neurobiol. Dis. 2003, 14 (3) 619-23
18. Kandimalla, K. K.; Scott, O. G.; Fulzele, S.; Davidson, M. W.; Poduslo, J. F. Mechanism of neuronal versus endothelial cell uptake of Alzheimer's disease amyloid beta protein PLoS One 2009, 4 (2) e4627
19. Kandimalla, K. K.; Curran, G. L.; Holasek, S. S.; Gilles, E. J.; Wengenack, T. M.; Poduslo, J. F. Pharmacokinetic analysis of the blood-brain barrier transport of 125I-amyloid beta protein 40 in wild-type and Alzheimer's disease transgenic mice (APP,PS1) and its implications for amyloid plaque formation J. Pharmacol. Exp. Ther. 2005, 313 (3) 1370-8
20. McGowan, E.; Pickford, F.; Kim, J.; Onstead, L.; Eriksen, J.; Yu, C.; Skipper, L.; Murphy, M. P.; Beard, J.; Das, P.; Jansen, K.; Delucia, M.; Lin, W. L.; Dolios, G.; Wang, R.; Eckman, C. B.; Dickson, D. W.; Hutton, M.; Hardy, J.; Golde, T. Abeta42 is essential for parenchymal and vascular amyloid deposition in mice Neuron 2005, 47 (2) 191-9
21. Tanzi, R. E.; Moir, R. D.; Wagner, S. L. Clearance of Alzheimer's Abeta peptide: the many roads to perdition Neuron 2004, 43 (5) 605-8
22. Vogelgesang, S.; Warzok, R. W.; Cascorbi, I.; Kunert-Keil, C.; Schroeder, E.; Kroemer, H. K.; Siegmund, W.; Walker, L. C.; Pahnke, J. The role of P-glycoprotein in cerebral amyloid angiopathy; implications for the early pathogenesis of Alzheimer's disease Curr. Alzheimer Res. 2004, 1 (2) 121-5
23. Bading, J. R.; Yamada, S.; Mackic, J. B.; Kirkman, L.; Miller, C.; Calero, M.; Ghiso, J.; Frangione, B.; Zlokovic, B. V. Brain clearance of Alzheimer's amyloid-beta40 in the squirrel monkey: a SPECT study in a primate model of cerebral amyloid angiopathy J. Drug Targeting 2002, 10 (4) 359-68
24. Mackic, J. B.; Weiss, M. H.; Miao, W.; Kirkman, E.; Ghiso, J.; Calero, M.; Bading, J.; Frangione, B.; Zlokovic, B. V. Cerebrovascular accumulation and increased blood-brain barrier permeability to circulating Alzheimer's amyloid beta peptide in aged squirrel monkey with cerebral amyloid angiopathy J. Neurochem. 1998, 70 (1) 210-5
25. Davis, J.; Xu, F.; Miao, J.; Previti, M. L.; Romanov, G.; Ziegler, K.; Van Nostrand, W. E. Deficient cerebral clearance of vasculotropic mutant Dutch/Iowa Double A beta in human A betaPP transgenic mice Neurobiol. Aging 2006, 27 (7) 946-54
26. Tomlin, S. G. Vesicular transport across endothelial cells Biochim. Biophys. Acta 1969, 183 (3) 559-64
27. Shea, S. M.; Karnovsky, M. J.; Bossert, W. H. Vesicular transport across endothelium: Simulation of a diffusion model J. Theor. Biol. 1969, 24 (1) 30-42
28. Deane, R.; Sagare, A.; Hamm, K.; Parisi, M.; Lane, S.; Finn, M. B.; Holtzman, D. M.; Zlokovic, B. V. apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain J. Clin. Invest. 2008, 118 (12) 4002-13
29. Attems, J.; Yamaguchi, H.; Saido, T. C.; Thal, D. R. Capillary CAA and perivascular Abeta-deposition: two distinct features of Alzheimer's disease pathology J. Neurol. Sci. 2010, 299 (1-2) 155-62