Early-onset formation of parenchymal plaque amyloid abrogates cerebral microvascular amyloid accumulation in transgenic mice

Journal of Biological Chemistry

Volumn 289, Issue 25, 2014, Pages 17895-17908

  Xu, Feng ^a   Kotarba, Ann Marie E ^a   Ou Yang, Ming Hsuan ^a   Fu, Ziao ^a   Davis, Judianne ^a   Smith, Steven O ^a   Van Nostrand, William E ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; MAMMALS; PATHOLOGY; PEPTIDES;

ALZHEIMER DISEASE; AMYLOID DEPOSITS; CEREBRAL AMYLOID ANGIOPATHY; CEREBRAL MICROVESSELS; CORTICAL NEURONS; FIBRIL FORMATION; TRANSGENIC LINES; TRANSGENIC MICE;

GLYCOPROTEINS;

AMYLOID;

AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN CELL; BRAIN LEVEL; BRAIN PARENCHYMA; CELL ACTIVATION; CELL LOSS; CONTROLLED STUDY; DISEASE COURSE; IN VITRO STUDY; MICROGLIA; MOUSE; NEUROPATHOLOGY; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; VASCULAR AMYLOIDOSIS;

ALZHEIMER DISEASE; AMYLOID; CEREBRAL VASCULAR; PATHOLOGY; PLAQUE; PROTEIN MISFOLDING; TRANSGENIC MICE;

AMYLOID BETA-PEPTIDES; ANIMALS; CEREBRAL AMYLOID ANGIOPATHY; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; HUMANS; MICE; MICE, TRANSGENIC; MUTATION; PLAQUE, AMYLOID;

EID: 84903442012     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.536565     Document Type: Article

References (75)

1. Polymenidou, M., and Cleveland, D. W. (2012) Prion-like spread of protein aggregates in neurodegeneration. J. Exp. Med. 209, 889-893
2. Eisenberg, D., and Jucker, M. (2012) The amyloid state of proteins in human disease. Cell 148, 1188-1203
3. Hardy, J., and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356 (Pubitemid 34790756)
4. Tanzi, R. E., and Bertram, L. (2005) Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 120, 545-555 (Pubitemid 40269768)
5. Masters, C. L., Simms, G., Weinman, N. A., Multhaup, G., McDonald, B. L., and Beyreuther, K. (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. U.S.A. 82, 4245-4269
6. De Felice, F. G., Vieira, M. N., Saraiva, L. M., Figueroa-Villar, J. D., Garcia-Abreu, J., Liu, R., Chang, L., Klein, W. L., and Ferreira, S. T. (2004) Targeting the neurotoxic species in Alzheimer's disease: inhibitors of Aβ oligomerization. FASEB J. 18, 1366-1372 (Pubitemid 39150351)
7. Goldgaber, D., Lerman, M. I., McBride, O. W., Saffiotti, U., and Gajdusek, D. C. (1987) Characterization and chromosomal localization of a cDNA encoding brain amyloid of Alzheimer's disease. Science 235, 877-880 (Pubitemid 17019124)
8. Kang, J., Lemaire, H. G., Unterbeck, A., Salbaum, J. M., Masters, C. L., Grzeschik, K. H., Multhaup, G., Beyreuther, K., and Müller-Hill, B. (1987) The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325, 733-736 (Pubitemid 17054046)
9. Tanzi, R. E., Gusella, J. F., Watkins, P. C., Bruns, G. A., St George-Hyslop, P., Van Keuren, M. L., Patterson, D., Pagan, S., Kurnit, D. M., and Neve, R. L. (1987) Amyloid β protein gene: cDNA, mRNA distribution, and genetic linkage near the Alzheimer's locus. Science 235, 880-884 (Pubitemid 17019125)
10. Sinha, S., Anderson, J. P., Barbour, R., Basi, G. S., Caccavello, R., Davis, D., Doan, M., Dovey, H. F., Frigon, N., Hong, J., Jacobson-Croak, K., Jewett, N., Keim, P., Knops, J., Lieberburg, I., Power, M., Tan, H., Tatsuno, G., Tung, J., Schenk, D., Seubert, P., Suomensaari, S. M., Wang, S., Walker, D., Zhao, J., McConlogue, L., and John, V. (1999) Purification and cloning of amyloid precursor protein β-secretase from human brain. Nature 402, 537-540
11. Vassar, R., Bennett, B. D., Babu-Khan, S., Kahn, S., Mendiaz, E. A., Denis, P., Teplow, D. B., Ross, S., Amarante, P., Loeloff, R., Luo, Y., Fisher, S., Fuller, J., Edenson, S., Lile, J., Jarosinski, M. A., Biere, A. L., Curran, E., Burgess, T., Louis, J. C., Collins, F., Treanor, J., Rogers, G., and Citron, M. (1999) β-secretase cleavage of the Alzheimer's precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741
12. De Strooper, B., Saftig, P., Craessaerts, K., Vanderstichele, H., Guhde, G., Annaert, W., Von Figura, K., and Van Leuven, F. (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391, 387-390 (Pubitemid 28093512)
13. Wolfe, M. S., Xia, W., Ostaszewski, B. L., Diehl, T. S., Kimberly, W. T., and Selkoe, D. J. (1999) Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and γ-secretase activity. Nature 398, 513-517
14. Jellinger, K. A. (2002) Alzheimer's disease and cerebrovascular pathology: an update. J. Neural Transm. 109, 813-836
15. Rensink, A. A., de Waal, R. M., Kremer, B., and Verbeek, M. M. (2003) Pathogenesis of cerebral amyloid angiopathy. Brain Res. Brain Res. Rev. 43, 207-223 (Pubitemid 37315654)
16. Thal, D. R., Ghebremedhin, E., Rüb, U., Yamaguchi, H., Del Tredici, K., and Braak, H. (2002) Two types of sporadic cerebral amyloid angiopathy. J. Neuropathol. Exp. Neurol. 61, 282-293 (Pubitemid 34212603)
17. Thal, D. R., Griffin, W. S., de Vos, R. A., and Ghebremedhin, E. (2008) Cerebral amyloid angiopathy and its relationship to Alzheimer's disease. Acta Neuropathol. 115, 599-609
18. Attems, J., Jellinger, K., Thal, D. R., and Van Nostrand, W. (2011) Sporadic cerebral amyloid angiopathy. Neuropathol. Appl. Neurobiol. 37, 75-93
19. Kawai, M., Kalaria, R. N., Cras, P., Siedlak, S. L., Velasco, M. E., Shelton, E. R., Chan, H. W., Greenberg, B. D., and Perry, G. (1993) Degeneration of vascular muscle cells in cerebral amyloid angiopathy of Alzheimer disease. Brain Res. 623, 142-146 (Pubitemid 23267401)
20. Rozemuller, A. J., van Gool, W. A., and Eikelenboom, P. (2005) The neuroinflammatory response in plaques and amyloid angiopathy in Alzheimer's disease: therapeutic implications. Curr. Drug Targets CNS Neurol. Disord. 4, 223-233 (Pubitemid 40754159)
21. Allen, N., Robinson, A. C., Snowden, J., Davidson, Y. S., and Mann, D. M. (2014) Patterns of cerebral amyloid angiopathy define histopathological phenotypes in Alzheimer's disease. Neuropathol. Appl. Neurobiol. 40, 136-148
22. Oshima, K., Uchikado, H., and Dickson, D. W. (2008) Perivascular neuritic dystrophy associated with cerebral amyloid angiopathy in Alzheimer's disease. Int. J. Clin. Exp. Pathol. 1, 403-408
23. Richard, E., Carrano, A., Hoozemans, J. J., van Horssen, J., van Haastert, E. S., Eurelings, L. S., de Vries, H. E., Thal, D. R., Eikelenboom, P., van Gool, W. A., and Rozemuller, A. J. (2010) Characteristics of dyshoric capillary cerebral amyloid angiopathy. J. Neuropathol. Exp. Neurol. 69, 1158-1167
24. Thal, D. R., Ghebremedhin, E., Orantes, M., and Wiestler, O. D. (2003) Vascular pathology in Alzheimer's disease: correlation of cerebral amyloid angiopathy and arteriosclerosis/lipohyalinosis with cognitive decline. J. Neuropath. Exp. Neurol. 62, 1287-1301 (Pubitemid 37494197)
25. Harkness, K. A., Coles, A., Pohl, U., Xuereb, J. H., Baron, J. C., and Lennox, G. G. (2004) Rapidly reversible dementia in cerebral amyloid inflammatory vasculopathy. Eur. J. Neurol. 11, 59-62 (Pubitemid 38174924)
26. Attems, J., and Jellinger, K. A. (2004) Only cerebral capillary amyloid angiopathy correlates with Alzheimer pathology: a pilot study. Acta Neuropathol. 107, 83-90 (Pubitemid 38159295)
27. Bailey, T. L., Rivara, C. B., Rocher, A. B., and Hof, P. R. (2004) The nature and effects of cortical microvascular pathology in aging and Alzheimer's disease. Neurol. Res. 26, 573-578 (Pubitemid 38879242)
28. Xu, W., Xu, F., Anderson, M. E., Kotarba, A. E., Davis, J., Robinson, J. K., and Van Nostrand, W. E. (2014) Cerebral microvascular rather than parenchymal amyloid β-protein pathology promotes early cognitive impairment in transgenic mice. J. Alzheimers Dis. 38, 621-632
29. Levy, E., Carman, M. D., Fernandez-Madrid, I. J., Power, M. D., Lieberburg, I., van Duinen, S. G., Bots, G. T., Luyendijk, W., and Frangione, B. (1990) Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. Science 248, 1124-1126
30. Van Broeckhoven, C., Haan, J., Bakker, E., Hardy, J. A., Van Hul, W., Wehnert, A., Vegter-Van der Vlis, M., and Roos, R. A. (1990) Amyloid β protein precursor gene and hereditary cerebral hemorrhage with amyloidosis (Dutch). Science 248, 1120-1122 (Pubitemid 20189867)
31. Hendriks, L., van Duijn, C. M., Cras, P., Cruts, M., Van Hul, W., van Harskamp, F., Warren, A., McInnis, M. G., Antonarakis, S. E., and Martin, J. J. (1992) Presenile dementia and cerebral haemorrhage linked to a mutation at codon 692 of the β-amyloid precursor protein gene. Nat. Genet. 1, 218-221
32. Tagliavini, F., Rossi, G., Padovani, A., Magoni, M., Andora, G., Sgarzi, M., Bizzi, A., Savioardo, M., Carella, F., Morbin, M., Giaccone, G., and Bugiani, O. (1999) A new βPP mutation related to hereditary cerebral haemorrhage. Alz. Rep. 2, S28
33. Grabowski, T. J., Cho, H. S., Vonsattel, J. P., Rebeck, G. W., and Greenberg, S. M. (2001) Novel amyloid precursor protein mutation in an Iowa family with dementia and severe cerebral amyloid angiopathy. Ann. Neurol. 49, 697-705 (Pubitemid 32530235)
34. van Duinen, S. G., Castaño, E. M., Prelli, F., Bots, G. T., Luyendijk, W., and Frangione, B. (1987) Hereditary cerebral hemorrhage with amyloidosis in patients of Dutch origin is related to Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 84, 5991-5994 (Pubitemid 17130424)
35. Rozemuller, A. J., Roos, R. A., Bots, G. T., Kamphorst, W., Eikelenboom, P., and Van Nostrand, W. E. (1993) Distribution of β/A4 and amyloid precursor protein in hereditary cerebral hemorrhage with amyloidosis-Dutch type and Alzheimer's disease. Am. J. Pathol. 142, 1449-1457 (Pubitemid 24058132)
36. Wattendorff, A. R., Frangione, B., Luyendijk, W., and Bots, G. T. A. M. (1995) Hereditary cerebral haemorrhage with amyloidosis, Dutch type (HCHWA-D): clinicopathological studies. J. Neurol. Neurosurg. Psychiatry 59, 699-705
37. Melchor, J. P., McVoy, L., and Van Nostrand, W. E. (2000) Charge alterations of E22 in the amyloid β-protein enhance its pathogenic properties. J. Neurochem. 74, 2209-2212 (Pubitemid 30217679)
38. Miravalle, L., Tokuda, T., Chiarle, R., Giaccone, G., Bugiani, O., Tagliavini, F., Frangione, B., and Ghiso, J. (2000) Substitutions at codon 22 of Alzheimer's Aβ peptide induce diverse conformational changes and apoptotic effects in human cerebral endothelial cells. J. Biol. Chem. 275, 27110-27116
39. Van Nostrand, W. E., Melchor, J. P., Cho, H. S., Greenberg, S. M., and Rebeck, G. W. (2001) Pathogenic effects of D23N "Iowa" amyloid β-protein. J. Biol. Chem. 276, 32860-32866
40. Davis, J., Xu, F., Deane, R., Romanov, G., Previti, M. L., Zeigler, K., Zlokovic, B. V., and Van Nostrand, W. E. (2004) Early-onset and robust cerebral microvascular accumulation of amyloid β-protein in transgenic mice expressing low levels of a vasculotropic Dutch/Iowa mutant form of amyloid β-protein precursor. J. Biol. Chem. 279, 20296-20306 (Pubitemid 38623475)
41. Miao, J., Xu, F., Davis, J., Otte-Höller, I., Verbeek, M. M., and Van Nostrand, W. E. (2005) Cerebral microvascular amyloid β-protein deposition induces vascular degeneration and neuroinflammation in transgenic mice expressing human vasculotropic mutant amyloid β-protein precursor. Am. J. Pathol. 167, 505-515 (Pubitemid 43026105)
42. Fan, R., Xu, F., Previti, M. L., Davis, J., Grande, A. M., Robinson, J. K., and Van Nostrand, W. E. (2007) Minocycline reduces microglial activation and improves behavioral deficits in a transgenic model of cerebral microvascular amyloid. J. Neurosci. 27, 3057-3063 (Pubitemid 46474134)
43. Xu, F., Grande, A. M., Robinson, J. K., Previti, M. L., Vasek, M., Davis, J., and Van Nostrand, W. E. (2007) Early-onset subicular microvascular amyloid and neuroinflammation correlate with behavioral deficits in vasculotropic mutant amyloid β-protein precursor transgenic mice. Neuroscience 146, 98-107 (Pubitemid 46654629)
44. Oakley, H., Cole, S. L., Logan, S., Maus, E., Shao, P., Craft, J., Guillozet-Bongaarts, A., Ohno, M., Disterhoft, J., Van Eldik, L., Berry, R., and Vassar, R. (2006) Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 26, 10129-10140 (Pubitemid 44527407)
45. Johnson-Wood, K., Lee, M., Motter, R., Hu, K., Gordon, G., Barbour, R., Khan, K., Gordon, M., Tan, H., Games, D., Lieberburg, I., Schenk, D., Seubert, P., and McConlogue, L. (1997) Amyloid precursor protein processing and Aβ42 deposition in a transgenic mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 94, 1550-1555
46. DeMattos, R. B., O'dell, M. A., Parsadanian, M., Taylor, J. W., Harmony, J. A., Bales, K. R., Paul, S. M., Aronow, B. J., and Holtzman, D. M. (2002) Clusterin promotes amyloid plaque formation and is critical for neuritic toxicity in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 99, 10843-10848
47. Yang, T., Hong, S., O'Malley, T., Sperling, R. A., Walsh, D. M., and Selkoe, D. J. (2013) New ELISAs with high specificity for soluble oligomers of amyloid β-protein detect natural Aβ oligomers in human brain but not in CSF. Alzheimers Dement. 9, 99-112
48. Davis-Salinas, J., Saporito-Irwin, S. M., Donovan, F. M., Cunningham, D. D., and Van Nostrand, W. E. (1994) Thrombin receptor activation induces secretion and nonamyloidogenic processing of amyloid β-protein precursor. J. Biol. Chem. 269, 22623-22627 (Pubitemid 24273369)
49. Long, J. M., Kalehua, A. N., Muth, N. J., Calhoun, M. E., Jucker, M., Hengemihle, J. M., Ingram, D. K., and Mouton, P. R. (1998) Stereological estimation of total microglia number in mouse hippocampus. J. Neurosci. Meth. 84, 101-108 (Pubitemid 28485053)
50. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., and Selkoe, D. J. (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539 (Pubitemid 34288854)
51. Glabe, C. G. (2006) Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol. Aging 27, 570-575
52. Ono, K., Condron, M. M., and Teplow, D. B. (2009) Structure-neurotoxicity relationships of amyloid β-protein oligomers. Proc. Natl. Acad. Sci. U.S.A. 106, 14745-14750
53. Kayed, R., Head, E., Sarsoza, F., Saing, T., Cotman, C. W., Necula, M., Margol, L., Wu, J., Breydo, L., Thompson, J. L., Rasool, S., Gurlo, T., Butler, P., and Glabe, C. G. (2007) Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol. Neurodegener. 2, 18
54. Jawhar, S., Trawicka, A., Jenneckens, C., Bayer, T. A., and Wirths, O. (2012) Motor deficits, neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal Aβ aggregation in the 5XFAD mouse model of Alzheimer's disease. Neurobiol. Aging 33, 196.e29-196.e40
55. Kim, K. S., Miller, D. L., Sapienza, V. J., Chen, C.-M. J., Bai, C., Gundke- Iqbal, I., Currie, J. R., and Wisniewski, H. M. (1988) Production and characterization of monoclonal antibodies reactive to synthetic cerebrovascular amyloid peptide. Neurosci. Res. Commun. 2, 121-130
56. Meyer-Luehmann, M., Coomaraswamy, J., Bolmont, T., Kaeser, S., Schaefer, C., Kilger, E., Neuenschwander, A., Abramowski, D., Frey, P., Jaton, A. L., Vigouret, J. M., Paganetti, P., Walsh, D. M., Mathews, P. M., Ghiso, J., Staufenbiel, M., Walker, L. C., and Jucker, M. (2006) Exogenous induction of cerebral β-amyloidogenesis is governed by agent and host. Science 313, 1781-1784 (Pubitemid 44454153)
57. Langer, F., Eisele, Y. S., Fritschi, S. K., Staufenbiel, M., Walker, L. C., and Jucker, M. (2011) Soluble Aβ seeds are potent inducers of cerebral β-amyloid deposition. J. Neurosci. 31, 14488-14495
58. Rosen, R. F., Fritz, J. J., Dooyema, J., Cintron, A. F., Hamaguchi, T., Lah, J. J., LeVine, H., 3rd, Jucker, M., and Walker, L. C. (2012) Exogenous seeding of cerebral β-amyloid deposition in βAPP-transgenic rats. J. Neurochem. 120, 660-666
59. Hamaguchi, T., Eisele, Y. S., Varvel, N. H., Lamb, B. T., Walker, L. C., and Jucker, M. (2012) The presence of Aβ seeds, and not age per se, is critical to the initiation of Aβ deposition in brain. Acta Neuropathol. 123, 31-37
60. Morales, R., Estrada, L. D., Diaz-Espinoza, R., Morales-Scheihing, D., Jara, M. C., Castilla, J., and Soto, C. (2010) Molecular cross talk between misfolded proteins in animal models of Alzheimer's and prion diseases. J. Neurosci. 30, 4528-4535
61. Herzig, M. C., Eisele, Y. S., Staufenbiel, M., and Jucker, M. (2009) E22Q mutant Aβ peptide (AßDutch) increases vascular but reduces parenchymal Aβ deposition. Am. J. Pathol. 172, 722-726
62. Bakker, E., van Broeckhoven, C., Haan, J., Voorhoeve, E., van Hul, W., Levy, E., Lieberburg, I., Carman, M. D., and van Ommen, G. J. (1991) DNA diagnosis for hereditary cerebral hemorrhage with amyloidosis (Dutch-type). Am. J. Hum. Genet. 49, 518-521 (Pubitemid 21891695)
63. Nilsson, K. P., Joshi-Barr, S., Winson, O., and Sigurdson, C. J. (2010) Prion strain interactions are highly selective. J. Neurosci. 30, 12094-12102
64. McCarter, J. F., Liebscher, S., Bachhuber, T., Abou-Ajram, C., Hübener, M., Hyman, B. T., Haass, C., and Meyer-Luehmann, M. (2013) Clustering of plaques contributes to plaque growth in a mouse model of Alzheimer's disease. Acta Neuropathol. 126, 179-188
65. Xu, F., Vitek, M. P., Colton, C. A., Previti, M. L., Davis, J., and Van Nostrand, W. E. (2012) Human apolipoprotein E2 promotes parenchymal amyloid deposition and neuronal loss in vasculotropic mutant amyloid β-protein Tg-SwDI mice. J. Alzheimers Dis. 31, 359-369
66. Zlokovic, B. V. (2004) Clearing amyloid through the blood-brain barrier. J. Neurochem. 89, 807-811
67. Deane, R., Wu, Z., Sagare, A., Davis, J., Du Yan, S., Hamm, K., Xu, F., Parisi, M., LaRue, B., Hu, H. W., Spijkers, P., Guo, H., Song, X., Lenting, P. J., Van Nostrand, W. E., and Zlokovic, B. V. (2004) LRP-amyloid β-peptide (Aβ) interaction regulates differential brain efflux of Aβ isoforms. Neuron 43, 333-344 (Pubitemid 39061126)
68. Weller, R. O., Subash, M., Preston, S. D., Mazanti, I., and Carare, R. O. (2008) Perivascular drainage of amyloid-β peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol. 18, 253-266 (Pubitemid 351430402)
69. Weller, R. O., Djuanda, E., Yow, H. Y., and Carare, R. O. (2009) Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol. 117, 1-14
70. Wisniewski, T., Ghiso, J., and Frangione, B. (1991) Peptides homologous to the amyloid protein of Alzheimer's disease containing a glutamine for glutamic acid substitution have accelerated amyloid fibril formation. Biochem. Biophys. Res. Comm. 179, 1247-1254
71. Davis, J., and Van Nostrand, W. E. (1996) Enhanced pathologic properties of Dutch-type mutant amyloid β-protein. Proc. Natl. Acad. Sci. U.S.A. 93, 2996-3000 (Pubitemid 26114352)
72. Verbeek, M. M., de Waal, R. M., Schipper, J. J., and Van Nostrand, W. E. (1997) Rapid degeneration of cultured human brain pericytes by amyloid β protein. J. Neurochem. 68, 1135-1141 (Pubitemid 27086218)
73. Yamamoto, N., Hirabayashi, Y., Amari, M., Yamaguchi, H., Romanov, G., Van Nostrand, W. E., and Yanagisawa, K. (2005) Assembly of hereditary amyloid β-protein variants in the presence of favorable gangliosides. FEBS Lett. 579, 2185-2190 (Pubitemid 40469690)
74. Yamamoto, N., Van Nostrand, W. E., and Yanagisawa, K. (2006) Further evidence of local ganglioside-dependent Aβ assembly in brain. Neuroreport 17, 1735-1737 (Pubitemid 44621574)
75. Monro, O. R., Mackic, J. B., Yamada, S., Segal, M. B., Ghiso, J., Maurer, C., Calero, M., Frangione, B., and Zlokovic, B. V. (2002) Substitution at codon 22 reduces clearance of Alzheimer's amyloid-β peptide from the cerebrospinal fluid and prevents its transport from the central nervous system into blood. Neurobiol. Aging 23, 405-412 (Pubitemid 34312024)