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Articles, Behavioral/Cognitive

Compartmentalized PDE4A5 Signaling Impairs Hippocampal Synaptic Plasticity and Long-Term Memory

Robbert Havekes, Alan J. Park, Rosa E. Tolentino, Vibeke M. Bruinenberg, Jennifer C. Tudor, Yool Lee, Rolf T. Hansen, Leonardo A. Guercio, Edward Linton, Susana R. Neves-Zaph, Peter Meerlo, George S. Baillie, Miles D. Houslay and Ted Abel
Journal of Neuroscience 24 August 2016, 36 (34) 8936-8946; DOI: https://doi.org/10.1523/JNEUROSCI.0248-16.2016
Robbert Havekes
1Groningen Institute for Evolutionary Life Sciences, University of Groningen, 9700 AB, Groningen, The Netherlands,
2Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Alan J. Park
2Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Rosa E. Tolentino
3Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Vibeke M. Bruinenberg
1Groningen Institute for Evolutionary Life Sciences, University of Groningen, 9700 AB, Groningen, The Netherlands,
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Jennifer C. Tudor
2Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Yool Lee
3Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Rolf T. Hansen
2Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Leonardo A. Guercio
2Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Edward Linton
2Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Susana R. Neves-Zaph
4Departments of Pharmacology and Systems Therapeutics, Friedman Brain Institute, and System Biology Center New York, Icahn School of Medicine at Mount Sinai, New York, New York 10029,
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Peter Meerlo
1Groningen Institute for Evolutionary Life Sciences, University of Groningen, 9700 AB, Groningen, The Netherlands,
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George S. Baillie
5Institute of Cardiovascular and Medical Science, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United Kingdom, and
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Miles D. Houslay
6Institute of Pharmaceutical Science, King's College London, London SE1 9NH, United Kingdom
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Ted Abel
2Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Article Information

DOI 
https://doi.org/10.1523/JNEUROSCI.0248-16.2016
PubMed 
27559174
Published By 
Society for Neuroscience
History 
  • Received January 23, 2016
  • Revision received June 26, 2016
  • Accepted June 29, 2016
  • First published August 24, 2016.
  • Version of record published August 24, 2016.
Copyright & Usage 
Copyright © 2016 Havekes et al. This article is freely available online through the J Neurosci Author Open Choice option.

Author Information

  1. Robbert Havekes1,2,
  2. Alan J. Park2,
  3. Rosa E. Tolentino3,
  4. Vibeke M. Bruinenberg1,
  5. Jennifer C. Tudor2,
  6. Yool Lee3,
  7. Rolf T. Hansen2,
  8. Leonardo A. Guercio2,
  9. Edward Linton2,
  10. Susana R. Neves-Zaph4,
  11. Peter Meerlo1,
  12. George S. Baillie5,
  13. Miles D. Houslay6, and
  14. Ted Abel2
  1. 1Groningen Institute for Evolutionary Life Sciences, University of Groningen, 9700 AB, Groningen, The Netherlands,
  2. 2Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
  3. 3Department of Systems Pharmacology and Translational Therapeutics, Institute for Translational Medicine and Therapeutics, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania 19104,
  4. 4Departments of Pharmacology and Systems Therapeutics, Friedman Brain Institute, and System Biology Center New York, Icahn School of Medicine at Mount Sinai, New York, New York 10029,
  5. 5Institute of Cardiovascular and Medical Science, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United Kingdom, and
  6. 6Institute of Pharmaceutical Science, King's College London, London SE1 9NH, United Kingdom
  • A. J. Park's present address: Department of Psychiatry, Columbia University, and the New York State Psychiatric Institute, 1051 Riverside Drive, New York, NY 10032.

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Author contributions

  1. Author contributions: R.H., A.J.P., J.C.T., R.T.H., S.R.N.-Z., P.M., G.S.B., M.D.H., and T.A. designed research; R.H., A.J.P., R.E.T., V.M.B., J.C.T., Y.L., L.A.G., and E.L. performed research; G.S.B. and M.D.H. contributed unpublished reagents/analytic tools; R.H., A.J.P., R.E.T., V.M.B., J.C.T., and S.R.N.-Z. analyzed data; R.H., P.M., M.D.H., and T.A. wrote the paper.

  • A. J. Park's present address: Department of Psychiatry, Columbia University, and the New York State Psychiatric Institute, 1051 Riverside Drive, New York, NY 10032.

Disclosures

    • Received January 23, 2016.
    • Revision received June 26, 2016.
    • Accepted June 29, 2016.
  • This research was supported by Netherlands Organization for Scientific Research NWO-Rubicon Grant 825.07.029 (to R.H.); the University of Pennsylvania Research Foundation (to R.H. and T.A.); National Institutes of Health Grants 1R01-MH-086415 9 (to T.A.), AG-017628 (to T.A., A.I. Pack Principal Investigator), 5K12-GM-081529 (to J.C.T., Y. Paterson Principal Investigator), and 5R01-DK-087650 (to S.R.N.-Z.); and Systems Biology Center of New York Grant PSDGM071558 (to S.R.N.-Z.). G.S.B. is supported by Medical Research Council Grant MR/J007412/1. R.H. is supported by the Einsteinium Foundation. T.A. is the Brush Family Professor of Biology at the University of Pennsylvania. We thank other Abel laboratory members for their help with these experiments and for their comments on this manuscript. We also thank Jin Zhang for providing pICUE3.

  • The authors declare no competing financial interests.

  • This is an Open Access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

  • Correspondence should be addressed to either of the following: Robbert Havekes, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, 9700 AB, Groningen, The Netherlands, r.havekes{at}rug.nl; or Ted Abel, Department of Biology, University of Pennsylvania, Philadelphia, PA 19104-6018. abele{at}sas.upenn.edu

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AbstractFullPdf
Aug 20162348111160
Sep 20161135112106
Oct 20162126772
Nov 20168714873
Dec 2016586126
Total 20163840499437
Jan 2017664927
Feb 2017457033
Mar 2017284722
Apr 2017154910
May 2017255320
Jun 2017163013
Jul 2017163730
Aug 2017113517
Sep 2017122517
Oct 2017144715
Nov 2017162822
Dec 2017102617
Total 2017274496243
Jan 2018112611
Feb 20189179
Mar 2018134415
Apr 20189426
May 201811566
Jun 201893614
Jul 201842412
Aug 201882316
Sep 201810488
Oct 201896512
Nov 201812779
Dec 201825811
Total 2018107516129
Jan 20195519
Feb 201915467
Mar 201963911
Apr 201912328
May 2019163617
Jun 201972713
Jul 201932926
Aug 201914177
Sep 2019125510
Oct 2019129521
Nov 201982118
Dec 201982515
Total 2019118473162
Jan 2020144222
Feb 20204219
Mar 2020123914
Apr 202071713
May 202073731
Jun 202042013
Jul 202032116
Aug 20202108
Sep 20209138
Oct 202032819
Nov 202052316
Dec 202053230
Total 202075303199
Jan 202152916
Feb 202171611
Mar 2021114332
Apr 202133923
May 202162415
Jun 20212268
Jul 202141817
Aug 202131814
Sep 202183233
Oct 2021113447
Nov 202171922
Dec 2021744213
Total 202174740251
Jan 2022288812
Feb 20228108812
Mar 202223319
Apr 20222298
May 202211114
Total 202215204965
Total450350761486
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The Journal of Neuroscience: 36 (34)
Journal of Neuroscience
Vol. 36, Issue 34
24 Aug 2016
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Compartmentalized PDE4A5 Signaling Impairs Hippocampal Synaptic Plasticity and Long-Term Memory
Robbert Havekes, Alan J. Park, Rosa E. Tolentino, Vibeke M. Bruinenberg, Jennifer C. Tudor, Yool Lee, Rolf T. Hansen, Leonardo A. Guercio, Edward Linton, Susana R. Neves-Zaph, Peter Meerlo, George S. Baillie, Miles D. Houslay, Ted Abel
Journal of Neuroscience 24 August 2016, 36 (34) 8936-8946; DOI: 10.1523/JNEUROSCI.0248-16.2016

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Compartmentalized PDE4A5 Signaling Impairs Hippocampal Synaptic Plasticity and Long-Term Memory
Robbert Havekes, Alan J. Park, Rosa E. Tolentino, Vibeke M. Bruinenberg, Jennifer C. Tudor, Yool Lee, Rolf T. Hansen, Leonardo A. Guercio, Edward Linton, Susana R. Neves-Zaph, Peter Meerlo, George S. Baillie, Miles D. Houslay, Ted Abel
Journal of Neuroscience 24 August 2016, 36 (34) 8936-8946; DOI: 10.1523/JNEUROSCI.0248-16.2016
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Keywords

  • cAMP
  • hippocampus
  • LTP
  • memory
  • PDE
  • phosphodiesterase

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