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Activity-Dependent Protein Transport as a Synaptic Tag

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Synaptic Tagging and Capture

Abstract

The “synaptic tagging and capture” hypothesis proposed that a hypothetical, cell biological mark is activated in the synapses undergoing early-phase plasticity. Newly synthesized plasticity-related proteins (PRPs) are assumed to establish late plasticity only in the marked synapses after unspecific transport along dendrites from soma. Demonstration of the “synaptic tagging and capture” hypothesis will be achieved by showing that a specific cell biological activity regulates behaviors of an exemplifying PRP in accordance with several unique characteristics assumed by the original hypothesis. We hypothesized that synaptic activity affects synaptic localization of PRPs on transport, namely, active spines receive PRPs, while no transport to inactive spines. We observed transport of Vesl-1S (also called Homer-1a) protein, one of PRPs, by measuring fluorescence of fused protein with EGFP (VE) in spines, and found that somatic Vesl-1S protein prevailed in most dendritic branches, and was translocated into spines where NMDA receptors were activated. The NMDA receptor-dependent translocation of VE protein from dendrite to spine fulfilled many of the hypothesized conditions of synaptic tagging, demonstrating the synaptic tagging hypothesis with Vesl-1S as an exemplifying PRP.

In addition to summarizing our findings, we would like to discuss the relevance of synaptic tagging as an input-specificity mechanism of late plasticity. An input-specificity mechanism restricts synapses where the expression mechanism of plasticity is activated. An essential feature of late plasticity is that it depends on synaptic functions of multiple PRPs, which is newly synthesized in various loci and lags. Late expression mechanism may require integrated functions of multiple PRPs, each of which likely has distinct localization, regulation, and function in the synapse. Synaptic tagging is a mechanism that allows synapse-specific function of PRPs, thereby assumed as a late input-specificity mechanism. Considering diversity in cell biological and biochemical properties of PRPs, it is suggested that multiple cell biological activities work as synaptic tagging, each of which is specific to a subset of PRPs and differently regulates synaptic localization and function of the PRPs at distinct timing. Activity-dependent spine translocation of Vesl-1S/Homer-1a may be an example of the diverse spectrum of synaptic tagging mechanisms.

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Acknowledgements

Authors are grateful to Jullietta Frey and Richard G.M. Morris for discussion and Fumiko Ozawa for outstanding technical assistance. D.O. thanks Kazuo Okanoya and Masami Takahashi for discussion and support. The work was done in Mitsubishi Kagaku Institute of Life Sciences. Authors are supported by the Special Coordinate Funds for Promoting Science and Technology from MEXT of the Japanese Government, the Core Research for Evolutional Science and Technology (CREST) program of the Japan Science and Technology Agency (JST), JSPS KAKENHI grant number 23220009, a Grant-in-Aid for Scientific Research on Innovative Areas “Memory dynamism” (25115002) from the MEXT the Mitsubishi Foundation, the Uehara Memorial Foundation, and Takeda Foundation to K.I., and Brain Science Foundation and NeuroCreative Laboratory to D.O.

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Authors and Affiliations

  1. Department of Biochemistry, Graduate School of Kitasato University, Laboratory for Molecular Neurobiology, Kitasato University School of Medicine, 1-15-1 Kitasato, Minami, Sagamihara, Kanagawa, 252-0374, Japan

    Daisuke Okada

  2. Department of Biochemistry, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, 2630 Sugitani, Toyama, 930-0194, Japan

    Kaoru Inokuchi

  3. CREST, JST, University of Toyama, 2630 Sugitani, Toyama, 930-0194, Japan

    Kaoru Inokuchi

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  1. Daisuke Okada
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  2. Kaoru Inokuchi
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Correspondence to Daisuke Okada or Kaoru Inokuchi .

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  1. Yong Loo Lin School of Medicine Department of Physiology, National University of Singapore, Singapore, Singapore

    Sreedharan Sajikumar

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Okada, D., Inokuchi, K. (2015). Activity-Dependent Protein Transport as a Synaptic Tag. In: Sajikumar, S. (eds) Synaptic Tagging and Capture. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1761-7_6

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