Systemic vaccination with anti-oligomeric monoclonal antibodies improves cognitive function by reducing Aβ deposition and tau pathology in 3xTg-AD mice

Journal of Neurochemistry

Volumn 126, Issue 4, 2013, Pages 473-482

  Rasool, Suhail ^a   Martinez Coria, Hilda ^b   Wu, Jessica W ^a   Laferla, Frank ^b   Glabe, Charles G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

abeta oligomers; Alzheimer's disease; amyloid plaques; monoclonal antibodies; tau pathology; vaccination

Indexed keywords

AMYLOID BETA PROTEIN; ANTIBODY; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; MONOCLONAL OLIGOMER SPECIFIC ANTIBODY; OLIGOMER; OLIGOMER SPECIFIC ANTIBODY; POLYCLONAL OLIGOMER SPECIFIC ANTIBODY; TAU PROTEIN; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA-PROTEIN (1-42); MAPT PROTEIN, MOUSE; PEPTIDE FRAGMENT; PRESENILIN 1; PRESENILIN 1, MOUSE;

3XTG AD MOUSE; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; COGNITION; CONTROLLED STUDY; DRUG MECHANISM; FEMALE; IMMUNOTHERAPY; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TAUOPATHY; VACCINATION; 129 MOUSE; ABETA OLIGOMERS; AMYLOID PLAQUE; ANIMAL; AVOIDANCE BEHAVIOR; C57BL MOUSE; COGNITIVE DEFECT; DISEASE MODEL; GENE TARGETING; GENETICS; IMMUNOLOGY; MAZE TEST; METABOLISM; METHODOLOGY; MICROGLIA; MONOCLONAL ANTIBODIES; PATHOLOGY; TAU PATHOLOGY; TRANSGENIC MOUSE;

ANIMALIA; MUS;

ABETA OLIGOMERS; ALZHEIMER'S DISEASE; AMYLOID PLAQUES; MONOCLONAL ANTIBODIES; TAU PATHOLOGY; VACCINATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTIBODIES, MONOCLONAL; AVOIDANCE LEARNING; COGNITION; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; FEMALE; GENE KNOCK-IN TECHNIQUES; MAZE LEARNING; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; PEPTIDE FRAGMENTS; PRESENILIN-1; TAU PROTEINS; TAUOPATHIES; VACCINATION;

EID: 84885961431     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12305     Document Type: Article

References (61)

1. Asuni A. A., Boutajangout A., Quartermain D., and, Sigurdsson E. M., (2007) Immunotherapy targeting pathological tau conformers in a tangle mouse model reduces brain pathology with associated functional improvements. J. Neurosci. 27, 9115-9129.
2. Avila J., Dominguez J., and, Diaz-Nido J., (1994) Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int. J. Dev. Biol. 38, 13-25.
3. Banks W. A., Terrell B., Farr S. A., Robinson S. M., Nonaka N., and, Morley J. E., (2002) Passage of amyloid beta protein antibody across the blood-brain barrier in a mouse model of Alzheimer's disease. Peptides 23, 2223-2226.
4. Bard F., Cannon C., Barbour R., et al,. (2000) Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med. 6, 916-919.
5. Billings L. M., Oddo S., Green K. N., McGaugh J. L., and, LaFerla F. M., (2005) Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45, 675-688.
6. Blennow K., de Leon M. J., and, Zetterberg H., (2006) Alzheimer's disease. Lancet 368, 387-403.
7. Boutajangout A., Quartermain D., and, Sigurdsson E. M., (2010) Immunotherapy targeting pathological tau prevents cognitive decline in a new tangle mouse model. J. Neurosci. 30, 16559-16566.
8. Brody D. L., and, Holtzman D. M., (2008) Active and passive immunotherapy for neurodegenerative disorders. Annu. Rev. Neurosci. 31, 175-193.
9. Bussiere T., Bard F., Barbour R., et al,. (2004) Morphological characterization of Thioflavin-S-positive amyloid plaques in transgenic Alzheimer mice and effect of passive Abeta immunotherapy on their clearance. Am. J. Pathol. 165, 987-995.
10. Caceres A., and, Kosik K. S., (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461-463.
11. Chen G., Chen K. S., Knox J., et al,. (2000) A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer's disease. Nature 408, 975-979.
12. Decker M. W., Gill T. M., and, McGaugh J. L., (1990) Concurrent muscarinic and beta-adrenergic blockade in rats impairs place-learning in a water maze and retention of inhibitory avoidance. Brain Res. 513, 81-85.
13. DeMattos R. B., Bales K. R., Cummins D. J., Dodart J. C., Paul S. M., and, Holtzman D. M., (2001) Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of Alzheimer's disease. Proc. Natl Acad. Sci. USA 98, 8850-8855.
14. Dodart J. C., Bales K. R., Gannon K. S., et al,. (2002) Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Nat. Neurosci. 5, 452-457.
15. Esmaeli-Azad B., McCarty J. H., and, Feinstein S. C., (1994) Sense and antisense transfection analysis of tau function: tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J. Cell Sci. 107 (Pt 4), 869-879.
16. Frazer M. E., Hughes J. E., Mastrangelo M. A., Tibbens J. L., Federoff H. J., and, Bowers W. J., (2008) Reduced pathology and improved behavioral performance in Alzheimer's disease mice vaccinated with HSV amplicons expressing amyloid-beta and interleukin-4. Mol. Ther. 16, 845-853.
17. Golde T. E., Eckman C. B., and, Younkin S. G., (2000) Biochemical detection of Abeta isoforms: implications for pathogenesis, diagnosis, and treatment of Alzheimer's disease. Biochim. Biophys. Acta 1502, 172-187.
18. Gordon M. N., Holcomb L. A., Jantzen P. T., DiCarlo G., Wilcock D., Boyett K. W., Connor K., Melachrino J., O'Callaghan J. P., and, Morgan D., (2002) Time course of the development of Alzheimer-like pathology in the doubly transgenic PS1+ APP mouse. Exp. Neurol. 173, 183-195.
19. Gotz J., Chen F., van Dorpe J., and, Nitsch R. M., (2001) Formation of neurofibrillary tangles in P301 l tau transgenic mice induced by Abeta 42 fibrils. Science 293, 1491-1495.
20. Greenberg S. G., Davies P., Schein J. D., and, Binder L. I., (1992) Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau. J. Biol. Chem. 267, 564-569.
21. Harada A., Oguchi K., Okabe S., Kuno J., Terada S., Ohshima T., Sato-Yoshitake R., Takei Y., Noda T., and, Hirokawa N., (1994) Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369, 488-491.
22. 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.
23. Iqbal K., Zaidi T., Bancher C., and, Grundke-Iqbal I., (1994) Alzheimer paired helical filaments. Restoration of the biological activity by dephosphorylation. FEBS Lett. 349, 104-108.
24. Janus C., Pearson J., McLaurin J., et al,. (2000) A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408, 979-982.
25. Jin M., Shepardson N., Yang T., Chen G., Walsh D., and, Selkoe D. J., (2011) Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc. Natl Acad. Sci. USA 108, 5819-5824.
26. Kawarabayashi T., Younkin L. H., Saido T. C., Shoji M., Ashe K. H., and, Younkin S. G., (2001) Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J. Neurosci. 21, 372-381.
27. Kayed R., Head E., Thompson J. L., McIntire T. M., Milton S. C., Cotman C. W., and, Glabe C. G., (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489.
28. Kayed R., Canto I., Breydo L., et al,. (2010) Conformation dependent monoclonal antibodies distinguish different replicating strains or conformers of prefibrillar Abeta oligomers. Mol. Neurodegener. 5, 57.
29. Lee V. M., and, Trojanowski J. Q., (1999) Neurodegenerative tauopathies: human disease and transgenic mouse models. Neuron 24, 507-510.
30. Lee H. G., Zhu X., Castellani R. J., Nunomura A., Perry G., and, Smith M. A., (2007) Amyloid-beta in Alzheimer disease: the null versus the alternate hypotheses. J. Pharmacol. Exp. Ther. 321, 823-829.
31. Lemere C. A., Spooner E. T., LaFrancois J., et al,. (2003) Evidence for peripheral clearance of cerebral Abeta protein following chronic, active Abeta immunization in PSAPP mice. Neurobiol. Dis. 14, 10-18.
32. Levites Y., Smithson L. A., Price R. W., et al,. (2006) Insights into the mechanisms of action of anti-Abeta antibodies in Alzheimer's disease mouse models. FASEB J. 20, 2576-2578.
33. Liu B., Wang K., Gao H. M., Mandavilli B., Wang J. Y., and, Hong J. S., (2001) Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J. Neurochem. 77, 182-189.
34. Lord A., Gumucio A., Englund H., et al,. (2009) An amyloid-beta protofibril-selective antibody prevents amyloid formation in a mouse model of Alzheimer's disease. Neurobiol. Dis. 36, 425-434.
35. Lovestone S., and, Reynolds C. H., (1997) The phosphorylation of tau: a critical stage in neurodevelopment and neurodegenerative processes. Neuroscience 78, 309-324.
36. Ma Q. L., Lim G. P., Harris-White M. E., Yang F., Ambegaokar S. S., Ubeda O. J., Glabe C. G., Teter B., Frautschy S. A., and, Cole G. M., (2006) Antibodies against beta-amyloid reduce Abeta oligomers, glycogen synthase kinase-3beta activation and tau phosphorylation in vivo and in vitro. J. Neurosci. Res. 83, 374-384.
37. Monsonego A., Imitola J., Zota V., Oida T., and, Weiner H. L., (2003) Microglia-mediated nitric oxide cytotoxicity of T cells following amyloid beta-peptide presentation to Th1 cells. J. Immunol. 171, 2216-2224.
38. Morgan D., Diamond D. M., Gottschall P. E., et al,. (2000) A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408, 982-985.
39. Oddo S., Caccamo A., Shepherd J. D., Murphy M. P., Golde T. E., Kayed R., Metherate R., Mattson M. P., Akbari Y., and, LaFerla F. M., (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39, 409-421.
40. Oddo S., Billings L., Kesslak J. P., Cribbs D. H., and, LaFerla F. M., (2004) Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43, 321-332.
41. Oddo S., Caccamo A., Tran L., Lambert M. P., Glabe C. G., Klein W. L., and, LaFerla F. M., (2006a) Temporal profile of amyloid-beta (Abeta) oligomerization in an in vivo model of Alzheimer disease. A link between Abeta and tau pathology. J. Biol. Chem. 281, 1599-1604.
42. Oddo S., Vasilevko V., Caccamo A., Kitazawa M., Cribbs D. H., and, LaFerla F. M., (2006b) Reduction of soluble Abeta and tau, but not soluble Abeta alone, ameliorates cognitive decline in transgenic mice with plaques and tangles. J. Biol. Chem. 281, 39413-39423.
43. Pfeifer M., Boncristiano S., Bondolfi L., Stalder A., Deller T., Staufenbiel M., Mathews P. M., and, Jucker M., (2002) Cerebral hemorrhage after passive anti-Abeta immunotherapy. Science 298, 1379.
44. Philipson O., Hammarström P., Nilsson K. P., et al,. (2009) A highly insoluble state of Abeta similar to that of Alzheimer's disease brain is found in Arctic APP transgenic mice. Neurobiol. Aging 30, 1393-1405.
45. Racke M. M., Boone L. I., Hepburn D. L., et al,. (2005) Exacerbation of cerebral amyloid angiopathy-associated microhemorrhage in amyloid precursor protein transgenic mice by immunotherapy is dependent on antibody recognition of deposited forms of amyloid beta. J. Neurosci. 25, 629-636.
46. Rasool S., Albay R., 3rd, Martinez-Coria H., et al,. (2012) Vaccination with a non-human random sequence amyloid oligomer mimic results in improved cognitive function and reduced plaque deposition and micro hemorrhage in Tg2576 mice. Mol. Neurodegener. 7, 37.
47. Schenk D., (2002) Amyloid-beta immunotherapy for Alzheimer's disease: the end of the beginning. Nat. Rev. Neurosci. 3, 824-828.
48. Schenk D., Barbour R., Dunn W., et al,. (1999) Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400, 173-177.
49. Shipton O. A., Leitz J. R., Dworzak J., et al,. (2011) Tau protein is required for amyloid {beta}-induced impairment of hippocampal long-term potentiation. J. Neurosci. 31, 1688-1692.
50. Sigurdsson E. M., Lee J. M., Dong X. W., Hejna M. J., and, Lorens S. A., (1997) Bilateral injections of amyloid-beta 25-35 into the amygdala of young Fischer rats: behavioral, neurochemical, and time dependent histopathological effects. Neurobiol. Aging 18, 591-608.
51. Spillantini M. G., and, Goedert M., (1998) Tau protein pathology in neurodegenerative diseases. Trends Neurosci. 21, 428-433.
52. Tucker S. M., Borchelt D. R., and, Troncoso J. C., (2008) Limited clearance of pre-existing amyloid plaques after intracerebral injection of Abeta antibodies in two mouse models of Alzheimer disease. J. Neuropathol. Exp. Neurol. 67, 30-40.
53. Vasilevko V., and, Cribbs D. H., (2006) Novel approaches for immunotherapeutic intervention in Alzheimer's disease. Neurochem. Int. 49, 113-126.
54. Vossel K. A., Zhang K., Brodbeck J., Daub A. C., Sharma P., Finkbeiner S., Cui B., and, Mucke L., (2010) Tau reduction prevents Abeta-induced defects in axonal transport. Science 330, 198.
55. Wilcock D. M., Gordon M. N., Ugen K. E., et al,. (2001) Number of Abeta inoculations in APP+PS1 transgenic mice influences antibody titers, microglial activation, and congophilic plaque levels. DNA Cell Biol. 20, 731-736.
56. Wilcock D. M., DiCarlo G., Henderson D., Jackson J., Clarke K., Ugen K. E., Gordon M. N., and, Morgan D., (2003) Intracranially administered anti-Abeta antibodies reduce beta-amyloid deposition by mechanisms both independent of and associated with microglial activation. J. Neurosci. 23, 3745-3751.
57. Wilcock D. M., Rojiani A., Rosenthal A., Subbarao S., Freeman M. J., Gordon M. N., and, Morgan D., (2004) Passive immunotherapy against Abeta in aged APP-transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage. J. Neuroinflammation 1, 24.
58. Wilcock D. M., Alamed J., Gottschall P. E., Grimm J., Rosenthal A., Pons J., Ronan V., Symmonds K., Gordon M. N., and, Morgan D., (2006) Deglycosylated anti-amyloid-beta antibodies eliminate cognitive deficits and reduce parenchymal amyloid with minimal vascular consequences in aged amyloid precursor protein transgenic mice. J. Neurosci. 26, 5340-5346.
59. Wilcock D. M., Gharkholonarehe N., Van Nostrand W. E., Davis J., Vitek M. P., and, Colton C. A., (2009) Amyloid reduction by amyloid-beta vaccination also reduces mouse tau pathology and protects from neuron loss in two mouse models of Alzheimer's disease. J. Neurosci. 29, 7957-7965.
60. Zempel H., Thies E., Mandelkow E., and, Mandelkow E. M., (2010) Abeta oligomers cause localized Ca(2 +) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J. Neurosci. 30, 11938-11950.
61. Zheng W. H., Bastianetto S., Mennicken F., Ma W., and, Kar S., (2002) Amyloid beta peptide induces tau phosphorylation and loss of cholinergic neurons in rat primary septal cultures. Neuroscience 115, 201-211.