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Local translation provides the asymmetric distribution of CaMKII required for associative memory formation

Nannan Chen, Yunpeng Zhang, Mohamed Adel, Elena A. Kuklin, Martha L. Reed, Jacob D. Mardovin, Baskar Bakthavachalu, K. VijayRaghavan, Mani Ramaswami, View ORCID ProfileLeslie C. Griffith
doi: https://doi.org/10.1101/2022.03.28.486096
Nannan Chen
1Department of Biology, Volen National Center for Complex Systems, Brandeis University, Waltham, MA 02454-9110, USA
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Yunpeng Zhang
1Department of Biology, Volen National Center for Complex Systems, Brandeis University, Waltham, MA 02454-9110, USA
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Mohamed Adel
1Department of Biology, Volen National Center for Complex Systems, Brandeis University, Waltham, MA 02454-9110, USA
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Elena A. Kuklin
1Department of Biology, Volen National Center for Complex Systems, Brandeis University, Waltham, MA 02454-9110, USA
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Martha L. Reed
1Department of Biology, Volen National Center for Complex Systems, Brandeis University, Waltham, MA 02454-9110, USA
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Jacob D. Mardovin
1Department of Biology, Volen National Center for Complex Systems, Brandeis University, Waltham, MA 02454-9110, USA
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Baskar Bakthavachalu
3National Centre for Biological Sciences, Tata Institute of Fundamental Research Bellary Road, Bangalore 560065, India and School of Basic Science, Indian Institute of Technology Mandi, India
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K. VijayRaghavan
3National Centre for Biological Sciences, Tata Institute of Fundamental Research Bellary Road, Bangalore 560065, India and School of Basic Science, Indian Institute of Technology Mandi, India
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Mani Ramaswami
2Trinity College Institute of Neuroscience, School of Genetics and Microbiology and School of Natural Sciences, Trinity College Dublin, Dublin-2, Ireland
3National Centre for Biological Sciences, Tata Institute of Fundamental Research Bellary Road, Bangalore 560065, India and School of Basic Science, Indian Institute of Technology Mandi, India
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Leslie C. Griffith
1Department of Biology, Volen National Center for Complex Systems, Brandeis University, Waltham, MA 02454-9110, USA
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  • ORCID record for Leslie C. Griffith
  • For correspondence: griffith@brandeis.edu
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SUMMARY

How compartment-specific local proteomes are generated and maintained is inadequately understood, particularly in neurons, which display extreme asymmetries. Here we show that local enrichment of Ca2+/calmodulin-dependent protein kinase II (CaMKII) in axons of Drosophila mushroom body neurons is necessary for cellular plasticity and associative memory formation. Enrichment is achieved via enhanced axoplasmic translation of CaMKII mRNA, through a mechanism requiring the RNA-binding protein Mub and a 23-base Mub-recognition element in the CaMKII 3’UTR. Perturbation of either dramatically reduces axonal, but not somatic, CaMKII protein without altering the distribution or amount of mRNA in vivo and both are necessary and sufficient to enhance axonal translation of reporter mRNA. Together, these data identify elevated levels of translation of an evenly distributed mRNA as a novel strategy for generating subcellular biochemical asymmetries. They further demonstrate the importance of distributional asymmetry in the computational and biological functions of neurons.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 29, 2022.
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Local translation provides the asymmetric distribution of CaMKII required for associative memory formation
Nannan Chen, Yunpeng Zhang, Mohamed Adel, Elena A. Kuklin, Martha L. Reed, Jacob D. Mardovin, Baskar Bakthavachalu, K. VijayRaghavan, Mani Ramaswami, Leslie C. Griffith
bioRxiv 2022.03.28.486096; doi: https://doi.org/10.1101/2022.03.28.486096
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Local translation provides the asymmetric distribution of CaMKII required for associative memory formation
Nannan Chen, Yunpeng Zhang, Mohamed Adel, Elena A. Kuklin, Martha L. Reed, Jacob D. Mardovin, Baskar Bakthavachalu, K. VijayRaghavan, Mani Ramaswami, Leslie C. Griffith
bioRxiv 2022.03.28.486096; doi: https://doi.org/10.1101/2022.03.28.486096

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