Cited by 171Neuroscience and Neuropharmacology ResearchGenetics and Neurodevelopmental DisordersNerve injury and regeneration

Local Presynaptic Activity Gates Homeostatic Changes in Presynaptic Function Driven by Dendritic BDNF Synthesis

Open access
Jakawich, Sonya K., Nasser, Hassan B., Strong, Michael J., McCartney, Amber J., Perez, Amanda S., Rakesh, Neal, Carruthers, Cynthia J.L., Sutton, Michael A.·2010·Neuron

Abstract

Homeostatic synaptic plasticity is important for maintaining stability of neuronal function, but heterogeneous expression mechanisms suggest that distinct facets of neuronal activity may shape the manner in which compensatory synaptic changes are implemented. Here, we demonstrate that local presynaptic activity gates a retrograde form of homeostatic plasticity induced by blockade of AMPA receptors (AMPARs) in cultured hippocampal neurons. We show that AMPAR blockade produces rapid (<3 hr) protein synthesis-dependent increases in both presynaptic and postsynaptic function and that the induction of presynaptic, but not postsynaptic, changes requires coincident local activity in presynaptic terminals. This "state-dependent" modulation of presynaptic function requires postsynaptic release of brain-derived neurotrophic factor (BDNF) as a retrograde messenger, which is locally synthesized in dendrites in response to AMPAR blockade. Taken together, our results reveal a local crosstalk between active presynaptic terminals and postsynaptic signaling that dictates the manner by which homeostatic plasticity is implemented at synapses.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.neuron.2010.11.034

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Postsynaptic BDNF release has been implicated in the rapid local regulation of Pr.

    “Interestingly, postsynaptic BDNF release has recently been implicated in the rapid local regulation of P r (Jakawich et al. 2010), and BDNF is clearly important for the development and regulation of inhibitory synaptic transmission (Huang et al. 1999).”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 48 · Cited by 171

Research works printed but not linked: 42

  1. Aakalu G Smith WB Jiang C Nguyen N Schuman EM 2001 Dynamic visualization of dendritic protein synthesis in hippocampal neurons Neuron 30 489 502 11395009
  2. Alder J Thakker-Varia S Crozier RA Shaheen A Plummer MR Black IB 2005 Early presynaptic and late postsynaptic components contribute independently to brain-derived neurotrophic factor-induced synaptic plasticity J Neurosci 25 3080 3085 15788764 PMC6725079
  3. An JJ Gharami K Liao GY Woo NH Lau AG Vanevski F Torre ER Jones KR Feng Y Lu B Xu B 2008 Distinct role of long 3′ UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons Cell 134 175 187 18614020 PMC2527207
  4. Aoto J Nam CI Poon MM Ting P Chen L 2008 Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity Neuron 60 308 320 18957222 PMC2634746
  5. Atasoy D Ertunc M Moulder KL Blackwell J Chung C Su J Kavalili E 2008 Spontaneous and evoked glutamate release activates two populations of NMDA receptors with limited overlap J Neurosci 28 10151 10166 18829973 PMC2578837
  6. Bacci A Coco S Pravettoni E Schenk U Armano S Frassoni C Verderio C De Camilli P Matteoli M 2001 Chronic blockade of glutamate receptors enhances presynaptic release and downregulates the interaction between synaptophysin-synaptobrevin-vesicle-associated membrane protein 2 J Neurosci 21 6588 6596 11517248 PMC6763110
  7. Bekinschtein P Cammarota M Igaz LM Bevilaqua LR Izquierdo I Medina JH 2007 Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus Neuron 53 261 277 17224407
  8. Branco T Staras K Darcy KJ Goda Y 2008 Local dendritic activity sets release probability at hippocampal synapses Neuron 59 475 485 18701072 PMC6390949
  9. Burrone J O’Byrne M Murthy VN 2002 Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons Nature 420 414 418 12459783
  10. Echegoyen J Neu A Graber KD Soltesz I 2007 Homeostatic plasticity studied using in vivo hippocampal activity-blockade: synaptic scaling, intrinsic plasticity, and age-dependence PLoS ONE 2 e700 17684547 PMC1933594
  11. Frank CA Kennedy MJ Goold CP Marek KW Davis GW 2006 Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis Neuron 52 663 677 17114050 PMC2673733
  12. Gong B Wang H Gu S Heximer SP Zhuo M 2007 Genetic evidence for the requirement of adenylyl cyclase 1 in synaptic scaling of forebrain cortical neurons Eur J Neurosci 26 275 288 17650106
  13. Ibata K Sun Q Turrigiano GG 2008 Rapid synaptic scaling induced by changes in postsynaptic firing Neuron 57 819 826 18367083
  14. Ju W Morishita W Tsui J Gaietta G Deerink TJ Adams SR Garner CC Tsien RY Ellisman MH Malenka RC 2004 Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors Nat Neurosci 7 244 253 14770185
  15. Kang H Schuman EM 1996 A requirement for local protein synthesis in neurotrophin-induced synaptic plasticity Science 273 1402 1406 8703078
  16. Lessman V Gottman K Heumann R 1994 BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurons Neuroreport 6 21 25 7703418
  17. Li YX Xu Y Ju D Lester HA Davidson N Schuman EM 1998 Expression of a dominant negative TrkB receptor, T1, reveals a requirement for presynaptic signaling in BDNF-induced synaptic potentiation in cultured hippocampal neurons Proc Natl Acad Sci USA 95 10884 10889 9724799 PMC27990
  18. Messaoudi E Ying SW Kanhema T Croll SD Bramham CR 2002 Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo J Neurosci 22 7453 7461 12196567 PMC6757978
  19. Murthy VN Schikorski T Stevens CF Zhu Y 2001 Inactivity produces increases in neurotransmitter release and synapse size Neuron 32 673 682 11719207
  20. O’Brien RJ Kamboj S Ehlers MD Rosen KR Fischbach GD Huganir RL 1998 Activity-dependent modulation of synaptic AMPA receptor accumulation Neuron 21 1067 1078 9856462
  21. Pang P Teng HK Zaitsev E Woo NT Sakata K Zhen S Teng KK Yung W Hempstead BL Lu B 2004 Cleavage of proBDNF by tPA/Plasmin is essential for long-term hippocampal plasticity Science 306 487 491 15486301
  22. Pereira DB Rebola N Rodrigues RJ Cunha RA Carvalho AP Duarte CB 2006 TrkB receptor modulation of glutamate release is limited to a subset of nerve terminals in the adult rat hippocampus J Neurosci Res 83 832 844 16477614
  23. Pozo K Goda Y 2010 Unraveling mechanisms of homeostatic synaptic plasticity Neuron 66 337 351 20471348 PMC3021747
  24. Pratt KG Watt AJ Griffith LC Nelson SB Turrigiano GG 2003 Activity-dependent remodeling of presynaptic inputs by postsynaptic expressionof activated CaMKII Neuron 269 281 12873384
  25. Rabinowitch I Segev I 2008 Two opposing plasticity mechanisms pulling a single synapse Trends Neurosci 31 377 383 18602704
  26. Rutherford LC Nelson SB Turrigiano GG 1998 BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses Neuron 21 521 530 9768839
  27. Schinder AF Berninger B Poo M 2000 Postsynaptic target specificity of neurotophin-induced presynaptic potentiation Neuron 25 151 163 10707980
  28. Shepherd JD Rumbaugh G Wu J Chowdhury S Plath N Kuhl D Huganir RL Worley PF 2006 Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors Neuron 52 475 484 17088213 PMC1764219
  29. Stellwagen D Malenka R 2006 Synaptic scaling mediated by glial TNF-alpha Nature 440 1054 1059 16547515
  30. Sutton MA Wall NR Aakalu GN Schuman EM 2004 Regulation of dendritic protein synthesis by miniature synaptic events Science 304 1979 1983 15218151
  31. Sutton MA Ito HT Cressy P Kempf C Woo JC Schuman EM 2006 Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis Cell 125 785 799 16713568
  32. Sutton MA Taylor AM Ito HT Pham A Schuman EM 2007 Postsynaptic decoding of neural activity: eEF2 as a biochemical sensor coupling miniature synaptic transmission to local protein synthesis Neuron 55 648 661 17698016
  33. Takei N Kawamura M Hara K Yonezawa K Nawa H 2001 Brain-derived neurotrophic factor enhances neuronal translation by activating multiple initiation processes: comparison with the effects of insulin J Biol Chem 276 42818 42825 11551908
  34. Thiagarajan TC Lindskog M Tsien RW 2005 Adaptation to synaptic inactivity in hippocampal neurons Neuron 47 725 737 16129401
  35. Tongiorgi E Righi M Cattaneo A 1997 Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons J Neurosci 17 9492 9505 9391005 PMC6573421
  36. Turrigiano GG 2008 The self-tuning neuron: synaptic scaling of excitatory synapses Cell 135 422 435 18984155 PMC2834419
  37. Turrigiano GG Leslie KR Desai NS Rutherford LC Nelson SB 1998 Activity-dependent scaling of quantal amplitude in neocortical neurons Nature 391 892 896 9495341
  38. Tyler WJ Pozzo-Miller LD 2001 BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses J Neurosci 21 4249 4258 11404410 PMC2806848
  39. Wheeler DB Randall A Tsien RW 1994 Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission Science 264 107 111 7832825
  40. Wierenga CJ Walsh MF Turrigiano GG 2006 Temporal regulation of the expression locus of homeostatic plasticity J Neurophysiol 96 2127 2133 16760351
  41. Yin Y Edelman GM Vanderklish PW 2002 The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes Proc Natl Acad Sci USA PMC122371 11842217
  42. Zhang XH Poo MM 2002 Localized synaptic potentiation by BDNF requires local protein synthesis in the developing axon Neuron 36 675 688 12441056

Authors
Jakawich, S. K., Nasser, H. B., Strong, M. J., McCartney, A. J., Perez, A. S., Rakesh, N., Carruthers, C. J. L., & Sutton, M. A.
Affiliations
University of Michigan (US)
Corresponding author
Sutton, Michael A.
Venue
Neuron
Publisher
Elsevier BV
Published
2010-12
Volume
68
Issue
6
Pages
1143-1158
ISSN
0896-6273 (ISSN-L)
OpenAlex
W2074581529
Cited by
171
References
48
Citations by year
2026: 2 · 2025: 1 · 2024: 9 · 2023: 2 · 2022: 9 · 2021: 4 · 2020: 12 · 2019: 9 · 2018: 15 · 2017: 16 · 2016: 10 · 2015: 11 · 2014: 12 · 2013: 25 · 2012: 20
FWCI
7.51
Type
journal article
Language
en
Open access
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Mental Health (R01MH085798)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Keywords
homeostatic plasticity, presynaptic terminals, retrograde signaling, AMPA receptor blockade, hippocampal neurons, presynaptic function
MeSH terms
Animals, Animals, Newborn, Cells, Cultured, Dendrites, Hippocampus, Homeostasis, Ion Channel Gating, Presynaptic Terminals, Receptors, AMPA, Brain-Derived Neurotrophic Factor, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review