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In vivo reduction of striatal D1R by RNA interference alters expression of D1R signaling-related proteins and enhances methamphetamine addiction in male rats

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Abstract

This study sought to determine if reducing dopamine D1 receptor (D1R) expression in the dorsal striatum (DS) via RNA-interference alters methamphetamine self-administration. A lentiviral construct containing a short hairpin RNA (shRNA) was used to knock down D1R expression (D1RshRNA). D1RshRNA in male rats increased responding for methamphetamine (i.v.) under a fixed-ratio schedule in an extended access paradigm, compared to D1R-intact rats. D1RshRNA also produced a vertical shift in a dose–response paradigm and enhanced responding for methamphetamine in a progressive-ratio schedule, generating a drug-vulnerable phenotype. D1RshRNA did not alter responding for sucrose (oral) under a fixed-ratio schedule compared to D1R-intact rats. Western blotting confirmed reduced D1R expression in methamphetamine and sucrose D1RshRNA rats. D1RshRNA reduced the expression of PSD-95 and MAPK-1 and increased the expression of dopamine transporter (DAT) in the DS from methamphetamine, but not sucrose rats. Sucrose density gradient fractionation was performed in behavior-naïve controls, D1RshRNA- and D1R-intact rats to determine the subcellular localization of D1Rs, DAT and D1R signaling proteins. D1Rs, DAT, MAPK-1 and PSD-95 predominantly localized to heavy fractions, and the membrane/lipid raft protein caveolin-1 (Cav-1) and flotillin-1 were distributed equally between buoyant and heavy fractions in controls. Methamphetamine increased localization of PSD-95, Cav-1, and flotillin-1 in D1RshRNA and D1R-intact rats to buoyant fractions. Our studies indicate that reduced D1R expression in the DS increases vulnerability to methamphetamine addiction-like behavior, and this is accompanied by striatal alterations in the expression of DAT and D1R signaling proteins and is independent of the subcellular localization of these proteins.

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Acknowledgements

Funds from the Department of Veterans Affairs (BX003304 to CDM), National Institute on Drug Abuse and National Institute on Alcoholism and Alcohol Abuse (AA020098 and DA034140 to CDM) and start-up funds from VMRF (to CDM) supported the study. The authors thank Dr. Atsushi Miyanohara, Director, UCSD viral vector core, for his assistance with plasmid generation and virus production. The authors thank McKenzie Fannon for assistance with animal surgeries, animal behavior and tissue processing, and Wulfran Trenet and Rocio Erandi Heyer Osorno for immunohistochemistry and Western blotting analysis. A significant proportion of this work was submitted in part as Master’s Thesis by M.J.T. to the Division of Biological Sciences, University of California, San Diego.

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Authors and Affiliations

  1. VA San Diego Healthcare System, San Diego, CA, 92161, USA

    Alison D. Kreisler, Michael J. Terranova, Sucharita S. Somkuwar, Dvijen C. Purohit, Shanshan Wang, Brian P. Head & Chitra D. Mandyam

  2. Department of Anesthesiology, University of California San Diego, San Diego, CA, 92161, USA

    Shanshan Wang, Brian P. Head & Chitra D. Mandyam

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  1. Alison D. Kreisler
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  2. Michael J. Terranova
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  3. Sucharita S. Somkuwar
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  4. Dvijen C. Purohit
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  7. Chitra D. Mandyam
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Correspondence to Chitra D. Mandyam.

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The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

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Kreisler, A.D., Terranova, M.J., Somkuwar, S.S. et al. In vivo reduction of striatal D1R by RNA interference alters expression of D1R signaling-related proteins and enhances methamphetamine addiction in male rats. Brain Struct Funct 225, 1073–1088 (2020). https://doi.org/10.1007/s00429-020-02059-w

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