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Featured ArticleArticles, Neurobiology of Disease

Inhibitory Interneuron Progenitor Transplantation Restores Normal Learning and Memory in ApoE4 Knock-In Mice without or with Aβ Accumulation

Leslie M. Tong, Biljana Djukic, Christine Arnold, Anna K. Gillespie, Seo Yeon Yoon, Max M. Wang, Olivia Zhang, Johanna Knoferle, John L.R. Rubenstein, Arturo Alvarez-Buylla and Yadong Huang
Journal of Neuroscience 16 July 2014, 34 (29) 9506-9515; https://doi.org/10.1523/JNEUROSCI.0693-14.2014
Leslie M. Tong
1Gladstone Institute of Neurological Disease, San Francisco, California 94158,
2Biomedical Sciences Graduate Program,
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Biljana Djukic
1Gladstone Institute of Neurological Disease, San Francisco, California 94158,
3Departments of Neurology,
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Christine Arnold
3Departments of Neurology,
4Psychiatry,
5Neurological Surgery, and
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Anna K. Gillespie
1Gladstone Institute of Neurological Disease, San Francisco, California 94158,
2Biomedical Sciences Graduate Program,
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Seo Yeon Yoon
1Gladstone Institute of Neurological Disease, San Francisco, California 94158,
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Max M. Wang
1Gladstone Institute of Neurological Disease, San Francisco, California 94158,
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Olivia Zhang
1Gladstone Institute of Neurological Disease, San Francisco, California 94158,
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Johanna Knoferle
1Gladstone Institute of Neurological Disease, San Francisco, California 94158,
3Departments of Neurology,
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John L.R. Rubenstein
4Psychiatry,
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Arturo Alvarez-Buylla
3Departments of Neurology,
5Neurological Surgery, and
7The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, California 94143
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Yadong Huang
1Gladstone Institute of Neurological Disease, San Francisco, California 94158,
2Biomedical Sciences Graduate Program,
3Departments of Neurology,
6Pathology, and
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Abstract

Excitatory and inhibitory balance of neuronal network activity is essential for normal brain function and may be of particular importance to memory. Apolipoprotein (apo) E4 and amyloid-β (Aβ) peptides, two major players in Alzheimer's disease (AD), cause inhibitory interneuron impairments and aberrant neuronal activity in the hippocampal dentate gyrus in AD-related mouse models and humans, leading to learning and memory deficits. To determine whether replacing the lost or impaired interneurons rescues neuronal signaling and behavioral deficits, we transplanted embryonic interneuron progenitors into the hippocampal hilus of aged apoE4 knock-in mice without or with Aβ accumulation. In both conditions, the transplanted cells developed into mature interneurons, functionally integrated into the hippocampal circuitry, and restored normal learning and memory. Thus, restricted hilar transplantation of inhibitory interneurons restores normal cognitive function in two widely used AD-related mouse models, highlighting the importance of interneuron impairments in AD pathogenesis and the potential of cell replacement therapy for AD. More broadly, it demonstrates that excitatory and inhibitory balance are crucial for learning and memory, and suggests an avenue for investigating the processes of learning and memory and their alterations in healthy aging and diseases.

  • Alzheimer's disease
  • apoE
  • apoE knock-in mice
  • cell transplantation
  • learning and memory
  • MGE-derived GABAergic progenitor
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The Journal of Neuroscience: 34 (29)
Journal of Neuroscience
Vol. 34, Issue 29
16 Jul 2014
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Inhibitory Interneuron Progenitor Transplantation Restores Normal Learning and Memory in ApoE4 Knock-In Mice without or with Aβ Accumulation
Leslie M. Tong, Biljana Djukic, Christine Arnold, Anna K. Gillespie, Seo Yeon Yoon, Max M. Wang, Olivia Zhang, Johanna Knoferle, John L.R. Rubenstein, Arturo Alvarez-Buylla, Yadong Huang
Journal of Neuroscience 16 July 2014, 34 (29) 9506-9515; DOI: 10.1523/JNEUROSCI.0693-14.2014

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Inhibitory Interneuron Progenitor Transplantation Restores Normal Learning and Memory in ApoE4 Knock-In Mice without or with Aβ Accumulation
Leslie M. Tong, Biljana Djukic, Christine Arnold, Anna K. Gillespie, Seo Yeon Yoon, Max M. Wang, Olivia Zhang, Johanna Knoferle, John L.R. Rubenstein, Arturo Alvarez-Buylla, Yadong Huang
Journal of Neuroscience 16 July 2014, 34 (29) 9506-9515; DOI: 10.1523/JNEUROSCI.0693-14.2014
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Keywords

  • Alzheimer's disease
  • ApoE
  • apoE knock-in mice
  • cell transplantation
  • learning and memory
  • MGE-derived GABAergic progenitor

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