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Altered Hippocampal Transcript Profile Accompanies an Age-Related Spatial Memory Deficit in Mice

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Verbitsky, Miguel, Yonan, Amanda L., Malleret, Gaël, Kandel, Eric R., Gilliam, T. Conrad, Pavlidis, Paul·2004·Learning & Memory

DOI 10.1101/lm.68204PMC PMC419727

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Abstract

We have carried out a global survey of age-related changes in mRNA levels in the C57BL/6NIA mouse hippocampus and found a difference in the hippocampal gene expression profile between 2-month-old young mice and 15-month-old middle-aged mice correlated with an age-related cognitive deficit in hippocampal-based explicit memory formation. Middle-aged mice displayed a mild but specific deficit in spatial memory in the Morris water maze. By using Affymetrix GeneChip microarrays, we found a distinct pattern of age-related change, consisting mostly of gene overexpression in the middle-aged mice, suggesting that the induction of negative regulators in the middle-aged hippocampus could be involved in impairment of learning. Interestingly, we report changes in transcript levels for genes that could affect synaptic plasticity. Those changes could be involved in the memory deficits we observed in the 15-month-old mice. In agreement with previous reports, we also found altered expression in genes related to inflammation, protein processing, and oxidative stress.

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Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206
Place navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340
Inflammation and Alzheimer’s disease
Akiyama, H. (2000) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00124-x · Cited by 4,514
Controlling the false discovery rate in behavior genetics research
Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N., & Golani, I. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00297-2 · Cited by 4,146
The human hippocampus and spatial and episodic memory
Burgess, N., Maguire, E. A., & O'Keefe, J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00830-9 · Cited by 2,401
The cholinergic hypothesis of Alzheimer’s disease: A review of progress
Francis, P. T., Palmer, A. M., Snape, M., & Wilcock, G. K. (1999) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.66.2.137 · Cited by 2,198 · cited 2×
“A cholinergic deficit is observed in AD (Francis et al. 1999) and is also believed to play a role in the memory decline seen in normal aging (Decker 1987; Casu et al. 2002) and in modulating LTP (Ji et al. 2001).”
Background
Iron accumulation in Alzheimer disease is a source of redox-generated free radicals
Smith, M. A., Harris, P. L. R., Sayre, L. M., & Perry, G. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.18.9866 · Cited by 1,365
Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease
West, M. J., Coleman, P. D., Flood, D. G., & Troncoso, J. C. (1994) · The Lancet · doi:10.1016/s0140-6736(94)92338-8 · Cited by 1,267 · cited 1×
“There is now considerable evidence supporting the view that normal age-related memory deficits can be caused by functional changes, without the occurrence of major structural alterations such as neuronal loss (West et al. 1994; Rapp et al. 2002).”
Background
Gene-expression profile of the ageing brain in mice
Lee, C.-K., Weindruch, R., & Prolla, T. A. (2000) · Nature Genetics · doi:10.1038/77046 · Cited by 1,055
Functional requirement for class I MHC in CNS development and plasticity
Huh, G. S., Boulanger, L. M., Du, H., Riquelme, P. A., Brotz, T. M., & Shatz, C. J. (2000) · Science · doi:10.1126/science.290.5499.2155 · Cited by 828

Show all 72 references

Research works printed but not linked: 8

2002, J. Nutr. Health Aging, 6, 136
1993, Nutr. Rev., 51, 157
1995, J. Neurol. Sci., 134, 33
1987, Brain Res., 434, 423
2002, Pac. Symp. Biocomput., 7, 474
1996, Physiol. Behav., 60, 611
1972, Psychologie Française, 17, 175
1998, News Physiol. Sci., 13, 118

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Hippocampal gene expression changes during age-related cognitive decline
Pawlowski, T. L., Bellush, L. L., Wright, A. W., Walker, J. P., Colvin, R. A., & Huentelman, M. J. (2008) · Brain Research · doi:10.1016/j.brainres.2008.12.039 · Cited by 40
Expression of the snoRNA host gene gas5 in the hippocampus is upregulated by age and psychogenic stress and correlates with reduced novelty‐induced behavior in C57BL/6 mice
Meier, I., Fellini, L., Jakovcevski, M., Schachner, M., & Morellini, F. (2009) · Hippocampus · doi:10.1002/hipo.20701 · Cited by 39
Proteomic approaches to oxidative protein modifications implicated in the mechanism of aging
Toda, T., Nakamura, M., Morisawa, H., Hirota, M., Nishigaki, R., & Yoshimi, Y. (2010) · Geriatrics and gerontology international/Geriatrics & gerontology international · doi:10.1111/j.1447-0594.2010.00606.x · Cited by 38
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Fouquet, C., Petit, G. H., Auffret, A., Gaillard, E., Rovira, C., Mariani, J., & Rondi‐Reig, L. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.11.001 · Cited by 34
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Pardo, J., Abba, M. C., Lacunza, E., Ogundele, O. M., Paiva, I., Morel, G. R., Outeiro, T. F., & Goya, R. G. (2017) · The Journals of Gerontology Series A · doi:10.1093/gerona/glx125 · Cited by 31
C57BL/6 mice as a preclinical model to study age-related cognitive deficits: Executive functions impairment and inter-individual differences
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Ennaceur, A., Michalíková, S., VANRENSBURG, R., & Chazot, P. L. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.09.025 · Cited by 32
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Shi, Q., Hu, X., Prior, M., & Yan, R. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5887-08.2009 · Cited by 31
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Gros, A., & Wang, S. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.02.023 · Cited by 30
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Gereñu, G., Dobarro, M., Ramírez, M. J., & Gil-Bea, F. J. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.02.018 · Cited by 29
Female CREBαδ− deficient mice show earlier age-related cognitive deficits than males
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Diet-induced obesity attenuates cytokine production following an immune challenge
Baumgarner, K. M., Setti, S. E., Diaz, C., Littlefield, A. M., Jones, A. C., & Kohman, R. A. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.03.017 · Cited by 27
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Qiu, J., Dunbar, D. R., Noble, J., Cairns, C., Carter, R., Kelly, V., Chapman, K. E., Seckl, J. R., & Yau, J. L. W. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12339 · Cited by 28
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Turan, Z. G., Parvizi, P., Dönertaş, H. M., Tung, J., Khaitovich, P., & Somel, M. (2019) · Aging Cell · doi:10.1111/acel.12965 · Cited by 28
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Peng, S., Zeng, L., Haure‐Mirande, J., Wang, M., Huffman, D. M., Haroutunian, V. H., Ehrlich, M. E., Zhang, B., & Tu, Z. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.711524 · Cited by 29
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Dempsey, K., Duraisamy, K., Ali, H., & Bhowmick, S. (2011) · Procedia Computer Science · doi:10.1016/j.procs.2011.04.015 · Cited by 21
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Kumari, E., Shang, Y., Cheng, Z., & Zhang, T. (2019) · Cognitive Neurodynamics · doi:10.1007/s11571-019-09528-x · Cited by 21
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Authors: Verbitsky, M., Yonan, A. L., Malleret, G., Kandel, E. R., Gilliam, T. C., & Pavlidis, P.
Affiliations: Howard Hughes Medical Institute (US)
ORCID: Verbitsky, Miguel
Malleret, Gaël
Kandel, Eric R.
Pavlidis, Paul
Venue: Learning & Memory
Publisher: Cold Spring Harbor Laboratory
Published: 2004-05
Volume: 11
Issue: 3
Pages: 253-260
ISSN: 1072-0502 (ISSN-L)
1549-5485
DOI: 10.1101/lm.68204
PMC: PMC419727
OpenAlex: W2039296833
Cited by: 158
References: 72
Citations by year: 2026: 2 · 2025: 1 · 2024: 4 · 2023: 10 · 2022: 6 · 2021: 12 · 2020: 4 · 2019: 9 · 2018: 5 · 2017: 10 · 2016: 4 · 2015: 7 · 2014: 6 · 2013: 9 · 2012: 11
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Learning & Memory (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: hippocampus, aging, spatial memory, gene expression profiles, declarative memory, synaptic plasticity, inflammation, oxidative stress, protein processing, learning disabilities, age-related cognitive decline
MeSH terms: Aging, Animals, Discrimination Learning, Gene Expression Regulation, Hippocampus, Learning Disabilities, Memory Disorders, Mice, Inbred C57BL, RNA, Messenger, Space Perception, Spatial Behavior, Maze Learning, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Mice

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Altered Hippocampal Transcript Profile Accompanies an Age-Related Spatial Memory Deficit in Mice

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