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Nanopore formation in the cuticle of an insect olfactory sensillum

Toshiya Ando, Sayaka Sekine, Sachi Inagaki, Kazuyo Misaki, Laurent Badel, Hiroyuki Moriya, Mustafa M. Sami, Yuki Itakura, Takahiro Chihara, Hokto Kazama, Shigenobu Yonemura, View ORCID ProfileShigeo Hayashi
doi: https://doi.org/10.1101/444729
Toshiya Ando
1RIKEN Center for Biosystems Dynamics Research, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan
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Sayaka Sekine
1RIKEN Center for Biosystems Dynamics Research, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan
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Sachi Inagaki
1RIKEN Center for Biosystems Dynamics Research, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan
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Kazuyo Misaki
1RIKEN Center for Biosystems Dynamics Research, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan
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Laurent Badel
2RIKEN Center for Brain Science, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan
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Hiroyuki Moriya
3Department of Genetics, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo, Japan
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Mustafa M. Sami
1RIKEN Center for Biosystems Dynamics Research, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan
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Yuki Itakura
1RIKEN Center for Biosystems Dynamics Research, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan
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Takahiro Chihara
3Department of Genetics, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo, Japan
4Department of Biological Science, Graduate School of Science, Hiroshima University, Higashi-Hiroshima, Hiroshima 739-8526, Japan
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Hokto Kazama
2RIKEN Center for Brain Science, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan
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Shigenobu Yonemura
1RIKEN Center for Biosystems Dynamics Research, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan
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Shigeo Hayashi
1RIKEN Center for Biosystems Dynamics Research, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan
5Department of Biology, Kobe University Graduate School of Science, Kobe, Hyogo 657-8501, Japan
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  • ORCID record for Shigeo Hayashi
  • For correspondence: shigeo.hayashi@riken.jp
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Summary

Nanometer-level patterned surface structures form the basis of biological functions including superhydrophobicity, structural coloration, and light absorption [1-3]. In insects, the cuticle overlying the olfactory sensilla has multiple small (50–200-nm diameter) pores [4-8], which are supposed to function as a filter that admits odorant molecules, while preventing the entry of larger airborne particles and limiting water loss. However, the cellular processes underlying the patterning of extracellular matrices into functional nano-structures remain unknown. Here we show that cuticular nanopores in Drosophila olfactory sensilla originate from a curved ultrathin film that is formed in the outermost envelope layer of the cuticle, and secreted from specialized protrusions in the plasma membrane of the hair forming (trichogen) cell. The envelope curvature coincides with plasma membrane undulations associated with endocytic structures. The gore-tex/Osiris23 gene encodes an endosomal protein that is essential for envelope curvature, nanopore formation, and odor receptivity, and is expressed specifically in developing olfactory trichogen cells. The 24-member Osiris gene family is expressed in cuticle-secreting cells, and is found only in insect genomes. These results reveal an essential requirement for nanopores for odor reception and identify Osiris genes as a platform for investigating the evolution of surface nano-fabrication in insects.

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Posted March 13, 2019.
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Nanopore formation in the cuticle of an insect olfactory sensillum
Toshiya Ando, Sayaka Sekine, Sachi Inagaki, Kazuyo Misaki, Laurent Badel, Hiroyuki Moriya, Mustafa M. Sami, Yuki Itakura, Takahiro Chihara, Hokto Kazama, Shigenobu Yonemura, Shigeo Hayashi
bioRxiv 444729; doi: https://doi.org/10.1101/444729
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Nanopore formation in the cuticle of an insect olfactory sensillum
Toshiya Ando, Sayaka Sekine, Sachi Inagaki, Kazuyo Misaki, Laurent Badel, Hiroyuki Moriya, Mustafa M. Sami, Yuki Itakura, Takahiro Chihara, Hokto Kazama, Shigenobu Yonemura, Shigeo Hayashi
bioRxiv 444729; doi: https://doi.org/10.1101/444729

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