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BIG2-ARF1-RhoA-mDia1 Signaling Regulates Dendritic Golgi Polarization in Hippocampal Neurons

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Abstract

Proper dendrite development is essential for establishing neural circuitry, and Rho GTPases play key regulatory roles in this process. From mouse brain lysates, we identified Brefeldin A-inhibited guanine exchange factor 2 (BIG2) as a novel Rho GTPase regulatory protein involved in dendrite growth and maintenance. BIG2 was highly expressed during early development, and knockdown of the ARFGEF2 gene encoding BIG2 significantly reduced total dendrite length and the number of branches. Expression of the constitutively active ADP-ribosylation factor 1 ARF1 Q71L rescued the defective dendrite morphogenesis of ARFGEF2-null neurons, indicating that BIG2 controls dendrite growth and maintenance by activating ARF1. Moreover, BIG2 co-localizes with the Golgi apparatus and is required for Golgi deployment into major dendrites in cultured hippocampal neurons. Simultaneous overexpression of BIG2 and ARF1 activated RhoA, and treatment with the RhoA activator lysophosphatidic acid in neurons lacking BIG2 or ARF1 increased the number of cells with dendritic Golgi, suggesting that BIG2 and ARF1 activate RhoA to promote dendritic Golgi polarization. mDia1 was identified as a downstream effector of BIG2-ARF1-RhoA axis, mediating Golgi polarization and dendritic morphogenesis. Furthermore, in utero electroporation of ARFGEF2 shRNA into the embryonic mouse brain confirmed an in vivo role of BIG2 for Golgi deployment into the apical dendrite. Taken together, our results suggest that BIG2-ARF1-RhoA-mDia1 signaling regulates dendritic Golgi polarization and dendrite growth and maintenance in hippocampal neurons.

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Acknowledgements

We thank Dr. Keith Burridge at University of North Carolina for GST-tagged RhoA, Rac1, and Cdc42 mutant DNAs, Dr. Myeong-Gu Kang at Institute of Basic Science for GEF-H1 shRNA, and Dr. Naoki Watanabe at Kyoto University for mDia1 plasmids. This study was supported by Chungnam National University.

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  1. Department of Microbiology and Molecular Biology, Chungnam National University, 99 Daehak-ro, Yuseong-gu, Daejeon, South Korea

    Eun-Hye Hong, Ji-Ye Kim & Jeong-Yoon Kim

  2. Korea Research Institute of Bioscience and Biotechnology, 125 Gwahak-ro, Yuseong-gu, Daejeon, South Korea

    Jeong-Hoon Kim

  3. Department of Biological Sciences, KAIST, 291 Daehak-ro, Yuseong-gu, Daejeon, South Korea

    Dae-Sik Lim

  4. Divison of Animal and Dairy Science, Chungnam National University, 99 Daehak-ro, Yuseong-gu, Daejeon, South Korea

    Minkyu Kim

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Hong, EH., Kim, JY., Kim, JH. et al. BIG2-ARF1-RhoA-mDia1 Signaling Regulates Dendritic Golgi Polarization in Hippocampal Neurons. Mol Neurobiol 55, 7701–7716 (2018). https://doi.org/10.1007/s12035-018-0954-7

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