Anti-amyloid beta protein antibody passage across the blood-brain barrier in the SAMP8 mouse model of Alzheimer's disease: An age-related selective uptake with reversal of learning impairment

Experimental Neurology

Volumn 206, Issue 2, 2007, Pages 248-256

  Banks, William A ^a,b   Farr, Susan A ^a,b   Morley, John E ^a,b   Wolf, Kathy M ^a,b   Geylis, Valeria ^c   Steinitz, Michael ^c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Alzheimer's disease; Amyloid beta protein; Blood brain barrier; Cognition; IgM; Monoclonal antibody; Passive immunization; Therapeutics

Indexed keywords

ALBUMIN; AMYLOID BETA PROTEIN ANTIBODY; IMMUNOGLOBULIN M; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY HYL5; MONOCLONAL ANTIBODY L11.3; UNCLASSIFIED DRUG;

AGE DISTRIBUTION; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BLOOD BRAIN BARRIER; COGNITIVE DEFECT; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG UPTAKE; EXPERIMENTAL MODEL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; MEMORY DISORDER; MOUSE; MOUSE STRAIN; NONHUMAN; PASSIVE IMMUNIZATION; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPONTANEOUS MUTATION; STRAIN DIFFERENCE;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; ANTIBODIES, MONOCLONAL; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE, TRANSFORMED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNOGLOBULIN M; IMMUNOGLOBULINS, INTRAVENOUS; INJECTIONS, INTRAVENOUS; LEARNING DISORDERS; MICE; MICE, NEUROLOGIC MUTANTS; MUTATION; TREATMENT OUTCOME;

EID: 34447622675     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2007.05.005     Document Type: Article

References (52)

1. Attems J., and Jellinger K.A. Olfactory tau pathology in Alzheimer's disease and mild cognitive impairment. Clin. Neuropathol. 25 (2006) 265-271
2. Banks W.A. Are the extracellular pathways a conduit for the delivery of therapeutics to the brain?. Curr. Pharm. Des. 10 (2004) 1365-1370
3. Banks W.A., and Kastin A.J. Exchange of peptides between the circulation and the nervous system: role of the blood-brain barrier. In: Porter J.C., and Jezova D. (Eds) (1990), Plenum Press, New York 59-69
4. Banks W.A., Farr S.A., and Morley J.E. Permeability of the blood-brain barrier to albumin and insulin in the young and aged SAMP8 mouse. J. Gerontol., Biol. Sci. 55A (2000) B601-B606
5. Banks W.A., Farr S.A., Butt W., Kumar V.B., Franko M.W., and Morley J.E. Delivery across the blood-brain barrier of antisense directed against amyloid β: reversal of learning and memory deficits in mice overexpressing amyloid precursor protein. J. Pharmacol. Exp. Ther. 297 (2001) 1113-1121
6. Banks W.A., Farr S.A., La Scola M.E., and Morley J.E. Intravenous human interleukin-1α impairs memory processing in mice: dependence on blood-brain barrier transport into posterior division of the septum. J. Pharmacol. Exp. Ther. 299 (2001) 536-541
7. Banks W.A., Terrell B., Farr S.A., Robinson S.M., Nonaka N., and Morley J.E. Transport of amyloid β protein antibody across the blood-brain barrier in an animal model of Alzheimer's disease. Peptides 23 (2002) 2223-2226
8. Banks W.A., Pagliari P., Nakaoke R., and Morley J.E. Effects of a behaviorally active antibody on the brain uptake and clearance of amyloid beta proteins. Peptides 26 (2005) 287-294
9. Bard F., Cannon C., Barbour R., Burke R.L., Games D., Grajeda H., Guido T., Hu K., Huang J., Johnson-Wood K., Khan K., Kholodenko D., Lee M., Lieberburg I., Motter R., Nguyen M., Soriano F., Vasquez N., Weiss K., Welch B., Seubert P., Schenk D., and Yednock T. Peripherally administered antibodies against amyloid β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer's disease. Nat. Med. 6 (2000) 916-919
10. Blasberg R.G., Fenstermacher J.D., and Patlak C.S. Transport of α-aminoisobutyric acid across brain capillary and cellular membranes. J. Cereb. Blood Flow Metab. 3 (1983) 8-32
11. Boules M., Williams K., Gollatz E., Fauq A., and Richelson E. Down-regulation of amyloid precursor protein by peptide nucleic acid in vivo. J. Mol. Neurosci. 24 (2004) 123-128
12. Broadwell, R.D., Bakder, B.J., Banks, W.A., Friden, P.M., Moran, M., Oliver, C., Villegas, J.C., 1994. Ferrotransferrin and antibody against the transferrin receptor as potential vehicles for drug delivery across the mammalian blood-brain barrier into the central nervous system. Flanagan, T.R., Emerich, D.F., Winn, S.R. [21], 93-117. Methods in Neuroscience. Ref Type: Serial (Book, Monograph).
13. Butterfield D.A. Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review. Free Radic. Res. 36 (2002) 1307-1313
14. Chekhonin V.P., Kabanov A.V., Zhirkov Y.A., and Morozov G.V. Fatty acid acylated Fab-fragments of antibodies to neurospecific proteins as carriers for neuroleptic targeted delivery in brain. FEBS Lett. 287 (1991) 149-152
15. Chen G., Chen K.S., Knox J., Inglis J., Bernard A., Martin S.J., Justice A., McConlogue L., Games D., Freedman S.B., and Morris R.G.M. A learning deficit related to age and β-amyloid plaques in a mouse model of Alzheimer's disease. Nature 408 (2000) 975-979
16. Christen-Zaech S., Kraftsik R., Pillevuit O., Kiraly M., Martins R., Khalili K., and Miklossy J. Early olfactory involvement in Alzheimer's disease. Can. J. Neurol. Sci. 30 (2003) 20-25
17. DeMattos R.B., Bales K.R., Cummins D.J., Paul S.M., and Holtzman D.M. Brain to plasma amyloid-β efflux: a measure of brain amyloid burden in a mouse model of Alzheimer's disease. Science 295 (2002) 2264
18. Elder G.A., De Gasperi R., and Gama Sosa M.A. Research update: neurogenesis in adult brain and neuropsychiatric disorders. Mt. Sinai J. Med. 73 (2006) 931-940
19. Farr S.A., Poon H.F., Dogrukol-Ak D., Drake J., Banks W.A., Eyerman E., Butterfield D.A., and Morley J.E. The antioxidants alpha-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice. J. Neurochem. 84 (2003) 1173-1183
20. Flood J.F., and Morley J.E. Learning and memory in the SAMP8 mouse. Neurosci. Biobehav. Rev. 22 (1998) 1-20
21. Flood J.F., Morley J.E., and La Reginna M. Age-related changes in the pharmacological improvement of retention in senescence accelerated mouse (SAM). Neurobiol. Aging 14 (1993) 159-166
22. Frautschy S.A., Yang F., Irrizarry M., Hyman B., Saido T.C., Hsiao K., and Cole G.M. Microglial response to amyloid plaques in APPsw transgenic mice. Am. J. Pathol. 152 (1998) 307-317
23. Geylis V., Kourilov B., Meiner Z., Nennesmo I., Bogdanovic N., and Steinitz M. Human monoclonal antibody against amyloid-beta engendered by EBV-immortalized lymphocytes from healthy adults. Neurobiol. Aging 26 (2005) 597-606
24. Glenner G.G., and Wong C.W. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120 (1984) 885-890
25. Gutierrez E.G., Banks W.A., and Kastin A.J. Murine tumor necrosis factor alpha is transported from blood to brain in the mouse. J. Neuroimmunol. 47 (1993) 169-176
26. Hallam K.T., Horgan J.E., McGrath C., and Norman T.R. An investigation of the effect of tacrine and physostigmine on spatial working memory deficits in the olfactory bulbectomized rat. Behav. Brain Res. 153 (2004) 481-486
27. Hardy J., and Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297 (2002) 353-356
28. Hock C., Konietzko U., Streffer J.R., Tracy J., Signorell A., Muller-Tillmanns B., Lemke U., Henke K., Moritz E., Garcia E., Wollmer M.A., Umbricht D., de Quervain D.J., Hofmann M., Maddalena A., Papassotiropoulos A., and Nitsch R.M. Antibodies against beta-amyloid slow cognitive decline in Alzheimer's disease. Neuron 38 (2003) 547-554
29. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., and Cole G. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274 (1996) 99-102
30. Janus C., Pearson J., McLaurin J., Mathews P.M., Jiang Y., Schmidt S.D., Chishti M.A., Horne P., Heslin D., French J., Mount H.T.J., Nixon R.A., Mercken M., Bergeron C., Fraser P.E., George-Hyslop P., and Westaway D. Aβ peptide immunization reduces behavioral impairment and plaques in a model of Alzheimer's disease. Nature 408 (2000) 979-982
31. Kozlowski G.P., Sterzl I., and Nilaver G. Localization patterns for immunoglobulins and albumins in the brain suggest diverse mechanisms for their transport across the blood-brain barrier (BBB). In: Ermisch A., Landgraf R., and Rühle H.J. (Eds) (1992), Elsevier, Amsterdam 149-154
32. Kumar V.B., Farr S.A., Flood J.F., Kamlesh V., Franko M., Banks W.A., and Morley J.E. Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice. Peptides 21 (2000) 1769-1775
33. Morgan D., Diamond D.M., Gottschall P.E., Ugen K.E., Dickey C., Hardy J., Duff K., Jantzen P., DiCarlo G., Wilcock D., Connor K., Hatcher J., Hope C., Gordon M., and Arendash G.W. Aβ peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408 (2000) 982-985
34. Morley J.E. The SAMP8 mouse: a model of Alzheimer's disease?. Biogerontology 31 (2002) 57-60
35. Morley J.E., Kumar V.B., Bernardo A.F., Farr S.A., Uezu K., Tumosa N., and Flood J.F. β-Amyloid precursor polypeptide in SAMP8 mice affects learning and memory. Peptides 21 (2000) 1761-1767
36. Morley J.E., Farr S.A., and Flood J.F. Antibody to amyloid beta protein alleviates impaired acquisition, retention, and memory processing in SAMP8 mice. Neurobiol. Learn. Mem. 78 (2002) 125-138
37. Morley J.E., Farr S.A., Kumar V.B., and Banks W.A. Alzheimer's disease through the eye of a mouse: acceptance lecture for the 2001 Gayle A. Olson and Richard D. Olson prize. Peptides 23 (2002) 589-599
38. Pan W., Solomon B., Maness L.M., and Kastin A.J. Antibodies to β-amyloid decrease the blood-to-brain transfer of β-amyloid peptide. Exp. Biol. Med. 227 (2002) 609-615
39. Patlak C.S., Blasberg R.G., and Fenstermacher J.D. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J. Cereb. Blood Flow Metab. 3 (1983) 1-7
40. Permanne B., Adessi C., Saborio G.P., Fraga S., Frossard M.J., Van Dorpe J., Dewachter I., Banks W.A., Van Leuven F., and Soto C. Reduction of amyloid load and cerebral damage in a transgenic mouse model of Alzheimer's disease by treatment with a beta-sheet breaker peptide. FASEB J. 16 (2002) 860-862
41. Poduslo J.F., Curran G.L., and Berg C.T. Macromolecular permeability across the blood-nerve and blood-brain barrier. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 5705-5709
42. Poon H.F., Castegna A., Farr S.A., Thongboonkerd V., Lynn B.C., Banks W.A., Morley J.E., Klein J.B., and Butterfield D.A. Quantitative proteomics analysis of specific protein expression and oxidative modification in aged senescence-accelerated-prone 8 mice brain. Neuroscience 126 (2004) 915-926
43. Schenk D., Barbour R., Dunn W., Gordon G., Grajeda H., Guido T., Hu K., Huang J., Johnson-Wood K., Khan K., Kholodenko D., Lee M., Liao A., Lieberburg I., Motter R., Mutter L., Soriano F., Shopp G., Vasquez N., Vandevert C., Walker S., Wogulis M., Yednock T., Games D., and Seubert P. Immunization with amyloid-β attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400 (1999) 173-177
44. Schlachetzki F., Zhu C., and Pardridge W.M. Expression of the neonatal Fc receptor (FcRn) at the blood-brain barrier. J. Neurochem. 81 (2002) 203-206
45. Steinitz M., Izak G., Cohen S., Ehrenfeld M., and Flechner I. Continuous production of monoclonal rheumatoid factor by in vitro EBV-transformed lymphocytes. Nature 287 (1980) 443-445
46. Townsend K.P., and Pratico D. Novel therapeutic opportunities for Alzheimer's disease: focus on nonsteroidal anti-inflammatory drugs. FASEB J. 19 (2005) 1592-1601
47. Triguero D., Buciak J., and Pardridge W.M. Capillary depletion method for quantification of blood-brain barrier transport of circulating peptides and plasma proteins. J. Neurochem. 54 (1990) 1882-1888
48. Uchida D., Arimura A., Somogyvari-Vigh A., Shioda S., and Banks W.A. Prevention of ischemia-induced death of hippocampal neurons by pituitary adenylate cyclase activating polypeptide. Brain Res. 736 (1996) 280-286
49. Ueno M., Dobrogowska D.H., and Vorbrodt A.W. Immunocytochemical evaluation of the blood-brain barrier to endogenous albumin in the olfactory bulb and pons of senescence-accelerated mice (SAM). Histochem. Cell Biol. 105 (1996) 203-212
50. Watt J.A., Pike C.J., Walencewicz-Wasserman A.J., and Cotman C.W. Ultrastructural analysis of β-amyloid-induced apoptosis in cultured hippocampal neurons. Brain Res. 661 (1994) 147-156
51. 5]enkephalin and two halogenated analogs after intravenous administration. J. Pharmacol. Exp. Ther. 259 (1991) 1109-1117
52. 5] enkephalin after intraperitoneal, intravenous, oral and subcutaneous administration. J. Pharmacol. Exp. Ther. 263 (1992) 1308-1316