Chronic anti-murine Aβ immunization preserves odor guided behaviors in an Alzheimer's β-amyloidosis model

Behavioural Brain Research

Volumn 237, Issue 1, 2013, Pages 96-102

  Wesson, Daniel W ^a,b   Morales Corraliza, Jose ^a,b   Mazzella, Matthew J ^a   Wilson, Donald A ^a,b,c   Mathews, Paul M ^a,b  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Amyloid beta; APP; Immunization; Neurodegeneration; Olfaction

Indexed keywords

AMYLOID BETA PROTEIN ANTIBODY; AMYLOID PRECURSOR PROTEIN; THIOFLAVINE;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOSMIA; ANTIBODY LABELING; ARTICLE; BIOACCUMULATION; BRAIN REGION; CONTROLLED STUDY; DRUG EFFECT; DRUG RESPONSE; ENTORHINAL CORTEX; FEMALE; MALE; MOUSE; NONHUMAN; ODOR; OLFACTORY BULB; PRIORITY JOURNAL; PYRIFORM CORTEX; SMELLING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIBODIES; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, TRANSGENIC; MUTATION; OLFACTION DISORDERS; TIME FACTORS;

EID: 84867058980     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.09.019     Document Type: Article

References (50)

1. Mesholam R.I., Moberg P.J., Mahr R.N., Doty R.L. Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer's and Parkinson's diseases. Archives of Neurology 1998, 55:84-90.
2. Murphy C. Loss of olfactory function in dementing disease. Physiology & Behavior 1999, 66:177-182.
3. Bacon A., Bondi M., Salmon D., Murphy C. Very early changes in olfactory functioning due to Alzheimer's disease and the role of apolipoprotein E in olfaction. Annals of the New York Academy of Sciences 1998, 855:723-731.
4. Devanand D.P., Liu X., Tabert M.H., Pradhaban G., Cuasay K., Bell K., et al. Combining early markers strongly predicts conversion from mild cognitive impairment to Alzheimer's disease. Biological Psychiatry 2008, 64:871-879.
5. Wesson D.W., Wilson D.A., Nixon R.A. Should olfactory dysfunction be used as a biomarker of Alzheimer's disease. Expert Review of Neurotherapeutics 2010, 10:633-635.
6. Wachowiak M., Shipley M.T. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Seminars in Cell & Developmental Biology 2006, 17:411-423.
7. Barnes D.C., Hofacer R.D., Zaman A.R., Rennaker R.L., Wilson D.A. Olfactory perceptual stability and discrimination. Nature Neuroscience 2008, 11:1378-1380.
8. Wilson D.A. Odor specificity of habituation in the rat anterior piriform cortex. Journal of Neurophysiology 2000, 83:139-145.
9. Gottfried J.A. Central mechanisms of odour object perception. Nature Reviews Neuroscience 2010, 11:628-641.
10. Li W., Howard J.D., Parrish T.B., Gottfried J.A. Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues. Science 2008, 319:1842-1845.
11. Schoenbaum G., Eichenbaum H. Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. Journal of Neurophysiology 1995, 74:733-750.
12. Chapuis J., Wilson D.A. Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nature Neuroscience 2011, 15:155-161.
13. Ghosh S., Larson S.D., Hefzi H., Marnoy Z., Cutforth T., Dokka K., et al. Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 2011, 472:217-220.
14. Sosulski D.L., Lissitsyna Bloom M., Cutforth T., Axel R., Datta S.R. Distinct representations of olfactory information in different cortical centres. Nature 2011, 472:213-216.
15. Staubli U., Ivy G., Lynch G. Hippocampal denervation causes rapid forgetting of olfactory information in rats. Proceedings of the National Academy of Sciences of the United States of America 1984, 81:5885-5887.
16. Eichenbaum H.B., Otto T.A., Wible C.G., Piper J.M. Building a model of the hippocampus in olfaction and memory. Olfaction: a model system for computational neuroscience 1991, 167-210. The MIT Press, Cambridge. J.L. Davis, H.B. Eichenbaum (Eds.).
17. Ache B.W., Young J.M. Olfaction: diverse species, conserved principles. Neuron 2005, 48:417-430.
18. Eichenbaum H., Fagan A., Mathews P., Cohen N.J. Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands. Behavioral Neuroscience 1988, 102:331-339.
19. Otto T., Schottler F., Staubli U., Eichenbaum H., Lynch G. Hippocampus and olfactory discrimination learning: effects of entorhinal cortex lesions on olfactory learning and memory in a successive-cue, go-no-go task. Behavioral Neuroscience 1991, 105:111-119.
20. Doucette W., Milder J., Restrepo D. Adrenergic modulation of olfactory bulb circuitry affects odor discrimination. Learning & Memory 2007, 14:539-547.
21. McNamara A.M., Magidson P.D., Linster C., Wilson D.A., Cleland T.A. Distinct neural mechanisms mediate olfactory memory formation at different timescales. Learning & Memory 2008, 15:117-125.
22. Wilson D.A. Scopolamine enhances generalization between odor representations in rat olfactory cortex. Learning & Memory 2001, 8:279-285.
23. Wesson D.W., Borkowski A.H., Landreth G.E., Nixon R.A., Levy E., Wilson D.A. Sensory network dysfunction, behavioral impairments, and their reversibility in an Alzheimer's beta-amyloidosis mouse model. The Journal of Neuroscience 2011, 31:15962-15971.
24. Yang D.S., Stavrides P., Mohan P.S., Kaushik S., Kumar A., Ohno M., et al. Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 2011, 134:258-277.
25. Cramer P.E., Cirrito J.R., Wesson D.W., Lee C.Y.D., Karlo J.C., Zinn A.E., et al. ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models. Science 2012, 335:1503-1506.
26. Wesson D.W., Levy E., Nixon R.A., Wilson D.A. Olfactory dysfunction correlates with β-amyloid plaque burden in an Alzheimer's disease mouse model. The Journal of Neuroscience 2010, 30:505-514.
27. Montgomery K.S., Simmons R.K., Edwards G., Nicolle M.M., Gluck M.A., Myers C.E., et al. Novel age-dependent learning deficits in a mouse model of Alzheimer's disease: implications for translational research. Neurobiology of Aging 2011, 32:1273-1285.
28. Guérin D., Sacquet J., Mandairon N., Jourdan F., Didier A. Early locus coeruleus degeneration and olfactory dysfunctions in Tg2576 mice. Neurobiology of Aging 2009, 30:272-283.
29. Young J., Sharkey J., Finlayson K. Progressive impairment in olfactory working memory in a mouse model of mild cognitive impairment. Neurobiology of Aging 2009, 30:1430-1443.
30. Kameshima N., Nanjou T., Fukuhara T., Yanagisawa D., Tooyama I. Correlation of Aβ deposition in the nasal cavity with the formation of senile plaques in the brain of a transgenic mouse model of Alzheimer's disease. Neuroscience Letters 2012, 513:166-169.
31. Morales-Corraliza J, Schmidt SD, Mazzella MJ, Berger JD, Wilson DA, Wesson DW, et al. Immunization targeting a minor plaque constituent clears β-amyloid and rescues behavioral deficits in an Alzheimer's disease mouse model. Neurobiology of Aging, in press, Epub ahead of print.
32. Morales-Corraliza J., Mazzella M.J., Berger J.D., Diaz N.S., Choi J.H.K., Levy E., et al. In vivo turnover of Tau and APP metabolites in the brains of wild-type and Tg2576 mice: greater stability of sAPP in the beta-amyloid depositing mice. PLoS ONE 2009, 4:e7134.
33. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., et al. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
34. Mathews P.M., Cataldo A.M., Kao B.H., Rudnicki A.G., Qin X., Yang J.L., et al. Brain expression of presenilins in sporadic and early-onset, familial Alzheimer's disease. Molecular Medicine 2000, 6:878-891.
35. Mi W., Pawlik M., Sastre M., Jung S.S., Radvinsky D.S., Klein A.M., et al. Cystatin C inhibits amyloid-[beta] deposition in Alzheimer's disease mouse models. Nature Genetics 2007, 39:1440-1442.
36. Schmidt S.D., Nixon R.A., Mathews P.M. Tissue processing prior to analysis of Alzheimer's disease associated proteins and metabolites, including Aβ. Amyloid proteins: methods and protocols 2012, Humana Press, New York, NY. E.M. Sigurdsson, M. Calero, M. Gasset (Eds.).
37. Mathews P.M., Jiang Y., Schmidt S.D., Grbovic O.M., Mercken M., Nixon R.A. Calpain activity regulates the cell surface distribution of amyloid precursor protein: inhibition of calpains enhances endosomal generation of beta-cleaved C-terminal APP fragments. The Journal of Biological Chemistry 2002, 277:36415-36424.
38. Paxinos G., Franklin K. The mouse brain in stereotaxic coordinates 2000, Academic Press, San Diego. 2nd ed.
39. Baum M.J., Keverne E.B. Sex difference in attraction thresholds for volatile odors from male and estrous female mouse urine. Hormones and Behavior 2002, 41:213-219.
40. Wilson D.A., Linster C. Neurobiology of a simple memory. Journal of Neurophysiology 2008, 100:2-7.
41. Linster C., Menon A.V., Singh C.Y., Wilson D.A. Odor-specific habituation arises from interaction of afferent synaptic adaptation and intrinsic synaptic potentiation in olfactory cortex. Learning & Memory 2009, 16:452-459.
42. Li W., Howard J.D., Gottfried J.A. Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer's disease. Brain 2010, 133:2714-2726.
43. Vidal R., Sammeta N., Garringer H.J., Sambamurti K., Miravalle L., Lamb B.T., et al. The Psen1-L166P-knock-in mutation leads to amyloid deposition in human wild-type amyloid precursor protein YAC transgenic mice. The FASEB Journal 2012, 26:2899-2910.
44. Fung J., Frost D., Chakrabartty A., McLaurin J. Interaction of human and mouse Aβ peptides. Journal of Neurochemistry 2004, 91:1398-1403.
45. Selkoe D.J. Soluble oligomers of the amyloid [beta]-protein impair synaptic plasticity and behavior. Behavioural Brain Research 2008, 192:106-113.
46. Schenk D., Barbour R., Dunn W., Gordon G., Grajeda H., Guido T., et al. Immunization with amyloid-[beta] attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 1999, 400:173-177.
47. Morgan D., Diamond D.M., Gottschall P.E., Ugen K.E., Dickey C., Hardy J., et al. A[beta] peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 2000, 408:982-985.
48. Jankowsky J.L., Younkin L.H., Gonzales V., Fadale D.J., Slunt H.H., Lester H.A., et al. Rodent Aβ modulates the solubility and distribution of amyloid deposits in transgenic mice. Journal of Biological Chemistry 2007, 282:22707-22720.
49. Pype S., Moechars D., Dillen L., Mercken M. Characterization of amyloid β peptides from brain extracts of transgenic mice overexpressing the London mutant of human amyloid precursor protein. Journal of Neurochemistry 2003, 84:602-609.
50. Janus C., Pearson J., McLaurin J., Mathews P.M., Jiang Y., Schmidt S.D., et al. A[beta] peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 2000, 408:979-982.