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A multivesicular body-like organelle mediates stimulus-regulated trafficking of olfactory ciliary transduction proteins

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  • Devendra Kumar Maurya

    (Umeå University)

  • Anna Berghard

    (Umeå University)

  • Staffan Bohm

    (Umeå University)

Abstract

Stimulus transduction in cilia of olfactory sensory neurons is mediated by odorant receptors, Gαolf, adenylate cyclase-3, cyclic nucleotide-gated and chloride ion channels. Mechanisms regulating trafficking and localization of these proteins in the dendrite are unknown. By lectin/immunofluorescence staining and in vivo correlative light-electron microscopy (CLEM), we identify a retinitis pigmentosa-2 (RP2), ESCRT-0 and synaptophysin-containing multivesicular organelle that is not part of generic recycling/degradative/exosome pathways. The organelle’s intraluminal vesicles contain the olfactory transduction proteins except for Golf subunits Gγ13 and Gβ1. Instead, Gβ1 colocalizes with RP2 on the organelle’s outer membrane. The organelle accumulates in response to stimulus deprivation, while odor stimuli or adenylate cyclase activation cause outer membrane disintegration, release of intraluminal vesicles, and RP2/Gβ1 translocation to the base of olfactory cilia. Together, these findings reveal the existence of a dendritic organelle that mediates both stimulus-regulated storage of olfactory ciliary transduction proteins and membrane-delimited sorting important for G protein heterotrimerization.

Suggested Citation

  • Devendra Kumar Maurya & Anna Berghard & Staffan Bohm, 2022. "A multivesicular body-like organelle mediates stimulus-regulated trafficking of olfactory ciliary transduction proteins," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34604-y
    DOI: 10.1038/s41467-022-34604-y
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    References listed on IDEAS

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    1. Thomas Wollert & James H. Hurley, 2010. "Molecular mechanism of multivesicular body biogenesis by ESCRT complexes," Nature, Nature, vol. 464(7290), pages 864-869, April.
    2. Noriyuki Nakashima & Kie Nakashima & Akiko Taura & Akiko Takaku-Nakashima & Harunori Ohmori & Makoto Takano, 2020. "Olfactory marker protein directly buffers cAMP to avoid depolarization-induced silencing of olfactory receptor neurons," Nature Communications, Nature, vol. 11(1), pages 1-18, December.
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