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The dendritic spine morphogenic effects of repeated cocaine use occur through the regulation of serum response factor signaling

Molecular Psychiatry volume 23, pages 1474–1486 (2018)Cite this article

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Abstract

The nucleus accumbens (NAc) is a primary brain reward region composed predominantly of medium spiny neurons (MSNs). In response to early withdrawal from repeated cocaine administration, de novo dendritic spine formation occurs in NAc MSNs. Much evidence indicates that this new spine formation facilitates the rewarding properties of cocaine. Early withdrawal from repeated cocaine also produces dramatic alterations in the transcriptome of NAc MSNs, but how such alterations influence cocaine’s effects on dendritic spine formation remain unclear. Studies in non-neuronal cells indicate that actin cytoskeletal regulatory pathways in nuclei have a direct role in the regulation of gene transcription in part by controlling the access of co-activators to their transcription factor partners. In particular, actin state dictates the interaction between the serum response factor (SRF) transcription factor and one of its principal co-activators, MAL. Here we show that cocaine induces alterations in nuclear F-actin signaling pathways in the NAc with associated changes in the nuclear subcellular localization of SRF and MAL. Using in vivo optogenetics, the brain region-specific inputs to the NAc that mediate these nuclear changes are investigated. Finally, we demonstrate that regulated SRF expression, in turn, is critical for the effects of cocaine on dendritic spine formation and for cocaine-mediated behavioral sensitization. Collectively, these findings reveal a mechanism by which nuclear-based changes influence the structure of NAc MSNs in response to cocaine.

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Acknowledgements

This work was supported by NIH grants P01DA008227 (EJN), R01DA014133 (EJN) and R01DA037257 (DMD). We thank John Condeelis of the Albert Einstein College of Medicine for the active N-WASP antibody.

Author contributions

MEC and EJN conceived the study and wrote the manuscript. MEC, DMW, AMG, ZJW, CKL, RCB and DMD generated data. RLN designed essential constructs specifically for the experiments in this study.

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Authors and Affiliations

  1. Fishberg Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    M E Cahill, D M Walker, C K Lardner, R C Bagot & E J Nestler

  2. Department of Pharmacology and Toxicology, Research Institute on Addictions, Program in Neuroscience, State University at Buffalo, Buffalo, NY, USA

    A M Gancarz, Z J Wang & D M Dietz

  3. Department of Psychology, McGill University, Montréal, QC, Canada

    R C Bagot

  4. Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA

    R L Neve

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  1. M E Cahill
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Correspondence to E J Nestler.

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Cahill, M., Walker, D., Gancarz, A. et al. The dendritic spine morphogenic effects of repeated cocaine use occur through the regulation of serum response factor signaling. Mol Psychiatry 23, 1474–1486 (2018). https://doi.org/10.1038/mp.2017.116

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