Alzheimer's disease and the blood-brain barrier: Past, present and future

Aging Health

Volumn 4, Issue 1, 2008, Pages 47-57

  Bowman, Gene L ^a   Quinn, Joseph F ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Albumin; Alzheimer's disease; Amyloid; Blood brain barrier; Cerebral amyloid angiopathy; Cholesterol; Computed tomography; Homocysteine; Imaging; LRP 1; MRI; PET; RAGE

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; EDETIC ACID; GADOLINIUM; HUMAN ALBUMIN; IODINATED CONTRAST MEDIUM; LOW DENSITY LIPOPROTEIN RECEPTOR; MEGLUMINE IOTALAMATE;

ALZHEIMER DISEASE; BLOOD BRAIN BARRIER; BRAIN ATHEROSCLEROSIS; CEREBROSPINAL FLUID EXAMINATION; CEREBROVASCULAR DISEASE; CLINICAL ASSESSMENT; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; HUMAN; HYPERHOMOCYSTEINEMIA; LIPID SOLUBILITY; MOLECULAR WEIGHT; MULTIINFARCT DEMENTIA; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NEUROIMAGING; NEUROPATHOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; REVIEW; SENILE PLAQUE; VASCULAR AMYLOIDOSIS;

EID: 39349083735     PISSN: 1745509X     EISSN: 17455103     Source Type: Journal    
DOI: 10.2217/1745509X.4.1.47     Document Type: Review

References (103)

1. Goldman E: Vitalfarburg am zentralnervousystem. Berlin: Eimer (1913).
2. Ehrlich P: Das Saurerstoff-Bedrurfnis des oraganismus: eine farbenanalytische studie. Berlin: Hirschward (1885).
3. Brightman MW: The distribution within the brain of ferritin injected into cerebrospinal fluid compartments. I. Ependymal distribution. J. Cell Biol. 26, 99-123 (1965).
4. Reese TS, Karnovsky MJ: Fine structural localization of a blood-brain barrier to exogenous peroxidase. J Cell Biol. 34, 207-217 (1967).
5. Kamovsky MJ: The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J Cell Biol. 35, 213-236 (1967).
6. Francis K, van Beek J, Canova C, Neal JW, Gasque P: Innate immunity and brain inflammation: the key role of complement. Expert Rev Mol. Med. 5. 1-19 (2003).
7. Zlokovic BV: Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci. 28. 202-208 (2005).
8. Kroll RA, Neuwelt EA: Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening and other means. Neurosurgery 42, 1083-1099; discussion 1099-1100 (1998).
9. Vera JC, Rivas CI, Fischbarg J, Golde DW: Mammallian facilitative hexose transporters mediate the transport of dehydroascorbic acid. Nature 364, 79-82 (1993).
10. Deane R, Zlokovic BV: Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr. Alzheimer Res. 4. 191-197 (2007).
11. Deane R, Du Yan S. Submamaryan RK et al.: RAGE mediates amyloid-β peptide transport across the blood-brain barrier and accumulation in brain. Nat Med. 9. 907-913 (2003).
12. Begley DJ, Brightman MW: Structural and functional aspects of the blood-brain barrier. Prog. Drug Res. 61, 39-78 (2003).
13. Carmeliet P: Angiogenesis in health and disease. Nat. Med. 9, 653-660 (2003).
14. Deane R, Wu Z. Sagare A et al.: LRP/amyloid beta-peptide interaction mediates differential brain efflux of Aβ isoforms. Neuron 43, 333-344 (2004).
15. Shibata M. Yamada S, Kumar SR et al.: 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. 106, 1489-1499 (2000).
16. Frick E, Scheid-Seydel L: Exchange processes between plasma and cerebrospinal fluid examined with radio-iodine labeled albumin. Klin. Wochenschr. 36, 66-69 (1958).
17. Frick E, Scheid-Seydel L: Studies with γ globulin labeled with radioiodine on the origin of protein bodies in the cerebrospinal fluid. Klin. Worhenschr. 36, 857-863 (1958).
18. Cutler RW, Deuel RK, Barlow CF: Albumin exchange between plasma and cerebruspinal fluid. Arch. Neurol. 17, 261-270 (1967).
19. Tibbibig G, Link H, Ohman S: Principles of albumin and IgG analyses in neurological disorders. I. Establishment of reference values. Scand. J. Clin. Lab. Invest. 37, 385-390 (1977).
20. Link H, Tibbling G: Principles of albumin and IgG analyses in neurological disorders. II. Relation of the concentration of the proteins in serum and cerebrospinal fluid. Scand. J. Clin. Lab. Invest. 37, 391-396 (1977).
21. Kessler RM. Goble JC, Bird JH et al.: Measurement of blood-brain barrier permeability with positron emission tomography and (68 Ga) EDTA. J. Cereb. Blood Flow Metab. 4, 323-328 (1984).
22. Groothuis DR, Vriesendorp FJ, Kupfer B et al.: Quantitative measurements of capillary transport in human brain tumors by computed tomography. Ann. Neurol. 30, 581-588 (1991).
23. Groothuis DR, Lapin GD, Vriesendorp FJ, Mikhael MA, Patlak CS. A method to quantitatively measure transcapillary transport of iodinated compounds in canine brain tumors with computed tomography. J. Cereb.Blood Flow Metab. 11. 939-948 (1991).
24. Ludemann L, Hamm B, Zimmer C: Pharmacokinetic analysis of glioma compartments with dynamic Gd-DTPA-enhanced magnetic resonance imaging. Magn. Reson. Imaging l8, 1201-1214 (2000).
25. Johnson G, Wetzel SG, Cha S, Babb J, Tofts PS: Measuring blood volume and vascular transfer constant from dynamic, T(2)*-weighted contrast-enhanced MRI. Magn. Reson. Med. 51, 961-968 (2004).
26. Alzheimer A: Uber eine eigenartige, Erkrankung der Himrinde. Alig. Z Psychiatrie 64, 146-148 (1907).
27. Glenner GG, Wong CW: Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120, 885-890 (1984).
28. Goldgaber D, Lerman MI, McBride OW, Saffiotti U, Gajdusek DC: Characterization and chromosomal localization of a cDNA encoding brain amyloid of Alzheimer's disease. Science 235, 877-880 (1987).
29. Kang J, Lemaire HG, Unter beck A et al.: The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325, 733-736 (1987).
30. Robakis NK, Ramakrishna N, Wolfe G, Wisniewski HM: Molecular cloning and characterization of a cDNA encoding the cerebrovascular and the neuritic plaque amyloid peptides. Proc. Natl. Acad. Sci. USA 84, 4190-4194 (1987).
31. Tanzi RE, Gusella JF, Watkins PC et al.: Amyloid β protein gene: cDNA, mRNA distribution, and-genetic linkage near the Alzheimer locus. Science 235, 880-884 (1987).
32. Selkoe DJ: Toward a comprehensive theory for Alzheimer's disease. Hypothesis: Alzheimer's disease is caused by the cerebral accumulation and cytotoxicity of amyloid beta-protein. Ann. NY Acad. Sci. 924, 17-25 (2000).
33. Terry RD, Masliah E. Salmon DP et al.: Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580 (1991).
34. Lue LF, Kuo YM, Roher AE et al.: Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155, 853-862 (1999).
35. McLean CA, Cherny RA, Fraser FW et al.: Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 46, 860-866 (1999).
36. Naslund J, Haroutunian V, Mohs R et al.: Correlation between elevated levels of amyloid β-peptide in the brain and cognitive decline. JAMA 283, 1571-1577 (2000).
37. Hardy J. Selkoe DJ: The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356 (2002).
38. Silverberg GD, Mayo M, Saul T, Rubenstein E, McGuire D: Alzheimer's disease, normal-pressure hydrocephalus, and senescent changes in CSF circulatory physiology: a hypothesis. Lancet Neurol. 2. 506-511 (2003).
39. Tanzi RE, Moir RD, Wagner SL: Clearance of Alzheimer's Aβ peptide: the many roads to perdition. Neuron 43, 605-608 (2004).
40. Zlokovic BV: Clearing amyloid through the blood-brain barrier. J. Neurochem. 89, 807-811 (2004).
41. Alonzo NC, Hyman BT, Rebeck GW, Greenberg SM: Progression of cerebral amyloid angiopathy: accumulation of amyloid-β40 in affected vessels. J. Neuropathol. Exp. Neurol. 57, 353-359 (1998).
42. Greenberg SM, Gurol ME. Rosand J, Smith EE: Amyloid angiopathy-related vascular cognitive impairment. Stroke 35, 2616-2619 (2004).
43. Grammas P, Yamada M, Zlokovic B: The cerebromicrovasculature: a key player in the pathogenesis of Altzheimer's disease. J. Alzheimer's Dis. 4, 217-223 (2002).
44. Snowdon DA, Greiner LH, Mortimer JA, Riley KP, Greiner PA, Markesbery WR: Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA 277, 813-817 (1997).
45. Vermeer SE, Prins ND, den Heijer T, Hofman A, Koudstaal PJ, Breteler MM: Silent brain Infarcts and the risk of dementia and cognitive decline. N. Engl. J. Med. 348, 1215-1222 (2003).
46. Pluta R: Role of ischemic blood-brain barrier on amyloid plaques development in Alzheimer's disease brain. Curr. Neurovasc. Res. 4, 121-129 (2007).
47. Pluta R: Pathological opening of the blood-brain barrier to horseradish peroxidase and amyloid precursor protein following ischemia-reperfusion brain injury. Chemotharapy 51, 223-226 (2005).
48. Badan I, Dinca I, Buchhold B et al.: Accelerated accumulation of N- and C-terminal β APP fragments and delayed recovery of microtubule-associated protein 1B expression following stroke in aged rats. Eur. J. Neurosci. 19, 2270-2280 (2004).
49. Gartshore G, Patterson J, Macrae IM: Influence of ischemia and reperfusion on the course of brain tissue swelling and blood-brain barrier permeability in a rodent model of transient focal cerebral ischemia. Exp. Neurol. 147. 353-360 (1997).
50. Petito CK. Pulsinelli WA, Jacobson G, Plum F: Edema and vascular permeability in cerebral ischemia: comparison between ischemic neuronal damage and infarction. J. Neuropathol Exp. Neurol. 41, 423-436 (1982).
51. Ueno M, Tomimoto H, Akiguchi I, Wakita H, Sakamoto H: blood-brain barrier disruption in white matter lesions in a rat model of chronic cerebral hypoperfusion. J. Cereb. Blood Flow Metab. 22, 97-104 (2002).
52. Wisniewski HM, Wegiel J: Alzheimer's disease neuropathology. Current status of interpretation of lesion development. Ann. NY Acad. Sci. 673, 270-284 (1992).
53. Eikelenboom P, Hack CE, Kamphorst W, Rozemuller JM: Distribution pattern and functional state of complement proteins and α1-antichymotrypsin in cerebral β/A4 deposits in Alzheimer's disease. Res. Immunol. 143, 617-620 (1992).
54. Wisniewski HM. Vorbrodt AW. Wegiel J: Amyloid angiopathy and blood-brain barrier changes in Alzheimer's disease. Ann. NY Acad. Sci. 826, 161-172 (1997).
55. Mann DM, Davies JS, Hawkes J, Yates PO: Immumohistochemical staining of senile plaques. Neuropathol. Appl. Neurobiol. 8, 55-61 (1982).
56. Kalaria RN, Golde TE, Cohen ML. Younkin SG: Serum amyloid P in Alzheimer's disease. Implications for dysfunction of the blood-brain barrier. Ann. NY Acad. Sci. 640, 145-148 (1991).
57. Claudio L: Ultrastructural features of the blood-brain barrier in biopsy tissue from Alzheimer's disease patients. Acta Neuropathol. (Berl.) 91, 6-14 (1996).
58. Stewart PA, Hayakawa K. Akers MA, Vinters HV: A morphometric study of the blood-brain barrier in Alzheimer's disease. Lab. Invest. 67, 734-742 (1992).
59. Alafuzoff I, Adolfsson R, Bucht G, Winblad B: Albumin and immunoglobulin in plasma and cerebrospinal fluid and blood-cerebrospinal fluid barrier function in patients with dementia of Alzheimer type and multi-infarct dementia. J. Neurol. Sci. 60, 465-472 (1983).
60. Algotsson A, Winblad B: The integrity of the blood-brain barrier in Alzheimer's disease. Acta Neurol. Scand. 115, 403-408 (2007).
61. Blennow K, Wallin A, Chong JK: Cerebrospinal fluid neuronal thread protein comes from serum by passage over the blood - brain barrier. Neurodegeration 4, 187-193 (1995).
62. Blennow K, Wallin A, Uhlemann C. Gottfries CG: White-matter lesions on CT in Alzheimer patients: relation to clinical symptomatology and vascular factors. Acta Neurol. Scand. 83, 187-193 (1991).
63. Elovaara I, Palo J, Erkinjuntti T, Sulkava R: Serum and cerebrospinal fluid proteins and the blood-brain barrier in Alzheimer's disease and multi-infarct dementia. Eur. Neurol. 26. 229-234 (1987).
64. Skoog I. Wallin A, Fredman P et al.: A population study on blood-brain barrier function in 85-year-olds: relation to Alzheimer's disease and vascular dementia. Neurology 50, 966-971 (1998).
65. Wada H: Blood-brain barrier permeability of the demented elderly as studied by cerebrospinal fluid-serum albumin ratio. Intern. Med. 37, 509-513 (1998).
66. Frolich L, Kornhuber J, Ihi R, Fritze J, Maurer K, Riederer P: Integrity of the blood-CSF barrier in dementia of Alzheimer type: CSF/serum ratios of albumin and IgG. Eur. Arch. Psychiatry Clin. Neurosci. 240, 363-366 (1991).
67. Kay AD, May C, Papadopoulos NM et al.: CSF and serum concentrations of albumin and IgG in Alzheimer's disease. Neurobiol. Aging 8, 21-25 (1987).
68. Mecocci P, Parnettl L, Reboldi GP et al.: Blood-brain barrier in a geriatric population: barrier function in degenerative and vascular dementias. Acta Neurol. Scand. 84, 210-213 (1991).
69. Sun YX, Minthon L, Wallmark A, Warkentin S, Blennow K. Janclauskiene S: Inflammatory markers in matched plasma and cerebrospinal fluid from patients with Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 16, 136-144 (2003).
70. Blennow K, Wallin A. Fredman P. Gottfries CG, Karlsson I, Svennerholm L: Intrathecal synthesis of Immunoglobulins in patients with Alzheimer's disease. Eur. Neuropsychopharmacol. 1. 79-81 (1990).
71. Bowman GL, Kaye JA, Moore M, Walchunas D, Carlson NE, Quinn JF: Blood-brain barrier impairment in Atzheimer disease: stability and functional significance. Neurology 68, 1809-1814 (2007).
72. Caserta MT, Caccioppo D, Lapin GD, Ragin A, Groothuis DR: Blood-brain barrier integrity in Alzheimer's disease patients and elderly control subjects. J. Neuropsychiatry Clin. Neurosci. 10, 78-84 (1998).
73. Dysken MW, Nelson MJ, Hoover KM, Kuskowski M, McGeachie R: Rapid dynamic CT scanning in primary degenerative dementia and age-matched controls. Biol. Psychiatry 28, 425-434 (1990).
74. Schlageter NL, Carson RE, Rapoport SI: Examination of blood-brain barrier permeability in dementia of the Alzheimer type with [68Ga]EDTA and positron emission tomography. J. Cereb. Blood Flow Metab. 7, 1-8 (1987).
75. Wang H, Golob EJ, Su MY: Vascular volume and blood-brain barrier permeability measured by dynamic contrast enhanced MRI in hippocampus and cerebellum of patients with MCI and normal controls. J. Magn. Reson. Imaging 24. 695-700 (2006).
76. Starr JM, Wardlaw J, Ferguson K. MacLullich A, Deary IJ, Marshall I: Increased blood-brain barrier permeability in Type II diabetes demonstrated by gadolinium magnetic resonance imaging. J. Neurol. Neurosurg. Psychiatry 74, 70-76 (2003).
77. Bronge L, Wahlund LO: White matter lesions in dementia: an MRI study on blood-brain barrier dysfunction. Dement. Geriatr. Cogn. Disord. 11, 263-267 (2000).
78. Hanyu H, Asano T, Tanaka Y, Iwamoto T, Takasaki M, Abe K: Increased blood-brain barrier permeability in white matter lesions of Binswanger's disease evaluated by contrast-enhanced MRI. Dement. Geriatr. Cogn. Disord. 14: 1-6 (2002).
79. Zlokovic BV, Martel CL, Matsubara E et al.: Glycoprotein 330/ megalin: probable role in receptor-mediated transport of apolipoproteln J alone and in a complex with Alzheimer disease amyloid β at the blood-brain and blood-cerebrospinal fluid barriers. Proc. Natl Acad. Sci. USA 93, 4229-4234 (1996).
80. Selkoe DJ: Clearing the brain's amyloid cobwebs. Neuron 32, 177-180 (2001).
81. Martel CL, Mackic JB, Matsubara E et al.: Isoform-specific effects of apolipoproteins E2, E3, and E4 on cerebral capillary sequestration and blood-brain barrier transport of circulating Alzheimer's amyloid β. J. Neurochem. 69, 1995-2004 (1997).
82. Leissring MA, Farris W, Chang AY et al.: Enhanced proteolysis of β-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 40, 1087-1093 (2003).
83. Kayed R, Head E, Thompson JL et al.: Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003).
84. Iwata N, Higuchi M, Saido TC: Metabolism of amyloid-β peptide and Alzheimer's disease. Pharmacol. Ther. 108, 129-148 (2005).
85. Ghiso J, Frangione B: Amyloidosis and Alzheimer's disease. Adv. Drug Deliv. Rev. 54, 1539-1551 (2002).
86. Kang DE, Saitoh T, Chen X et al.: Genetic association of the low-density lipoprotein receptor-related protein gene (LRP), an apolipoprotein E receptor, with late-onset Alzheimer's disease. Neurology 49, 56-61 (1997).
87. Hendriks L, van Duljn CM, Cras P et al.: Presenile dementia and cerebral haemorrhage linked to a mutation at codon 692 of the β-amyloid precursor protein gene. Nat. Genet. 1, 218-221 (1992).
88. Donahue JE, Flaherty SL, Johanson CE et al.: RAGE, LRP-1, and amyloid-β protein in Alzheimer's disease. Acta Neuropathol. 112, 405-415 (2006).
89. Kislinger T, Fu C, Huber B et al.: N(ε)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J. Biol. Chem. 274, 31740-31749 (1999).
90. Hori O, Brett J, Slattery T et al.: The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system. J. Biol. Chem. 270, 25752-25761 (1995).
91. Hofmann MA, Drury S, Fu C et al.: RAGE mediates a novel proinflammatory axis: a central cell surfare receptor for S100/ calgranulin polypeptides. Cell 97, 889-901 (1999).
92. Yan SD, Chen X, Fu J et al.: RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature 382, 685-691 (1996).
93. Dickstein DL, Biron KE, Ujiie M, Pfeifer CG, Jeffries AR, Jefferies WA: Aβ peptide immunization restores blood-brain barrier integrity in Alzheimer disease. FASEB J. 20, 426-433 (2006).
94. Clarke R, Smith AD, Jobst KA, Refsum H, Sutton L, Ueland PM: Folate, vitamin B12, and serum total homocysteine levels in confirmed Alzheimer disease. Arch. Neurol. 55, 1449-1455 (1998).
95. Ravaglia G, Forti P, Maioli F et al.: Homocysteine and folate as risk factors for dementia and Alzheimer disease. Am. J. Clin. Nutr. 82, 636-643 (2005).
96. Seshadri S, Beiser A, Selhub J et al.: Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N. Engl. J. Med. 346, 476-483 (2002).
97. Bostom AG. Silbershatz H, Rosenberg IH et al.: Nonfasting plasma total homocysteine levels and all-cause and cardiovascular disease mortality in elderly Framingham men and women. Arch. Intern. Med. 159, 1077-1080 (1999).
98. Bots ML, Launer LJ, Lindemans J, Hofman A, Grobbee DE: Homocysteine, atherosclerosis and prevalent cardiovascular disease in the elderly: The Rotterdam Study. J. Intern. Med. 242, 339-347 (1997).
99. Malinow MR, Nieto FJ, Szkio M, Chambless LE, Bond G: Carotid artery intimal-medial wall thickening and plasma homocyst(e)ine in asymptomatic adults. The Atherosclerosis Risk in Communities Study. Circulation 87, 1107-1113 (1993).
100. Matsui T, Arai H, Yuzuriha T et al.: Elevated plasma homocysteine levels and risk of silent brain infarction in elderly people. Stroke 32, 1116-1119 (2001).
101. Perry IJ, Refsum H, Morris RW, Ebrahim SB, Ueland PM. Shaper AG: Prospective study of serum total homocysteine concentration and risk of stroke in middle-aged British men. Lancet 346, 1395-1398 (1995).
102. Selhub J, Jacques PF, Bostom AG et al.: Association between plasma homocysteine concentrations and extracranial carotid-artery stenosis. N. Engl. J. Med. 332, 286-291 (1995).
103. Lehmann M, Regland B, Blennow K, Gottfries CG: Vitamin B12-B6-folate treatment improves blood-brain barrier function in patients with hyperhomocysteinaemia and mild cognitive impairment. Dement. Geriatr. Cogn. Disord. 16, 145-150 (2003)