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Structure, interaction and nervous connectivity of beta cell primary cilia

Author

Listed:
  • Andreas Müller

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.))

  • Nikolai Klena

    (Human Technopole (HT))

  • Song Pang

    (Howard Hughes Medical Institute
    Yale School of Medicine)

  • Leticia Elizabeth Galicia Garcia

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.)
    TU Dresden)

  • Oleksandra Topcheva

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.))

  • Solange Aurrecoechea Duran

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.))

  • Davud Sulaymankhil

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.)
    Cooper Union)

  • Monika Seliskar

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.))

  • Hassan Mziaut

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.))

  • Eyke Schöniger

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.))

  • Daniela Friedland

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.))

  • Nicole Kipke

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.))

  • Susanne Kretschmar

    (TU Dresden)

  • Carla Münster

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.))

  • Jürgen Weitz

    (TU Dresden)

  • Marius Distler

    (TU Dresden)

  • Thomas Kurth

    (TU Dresden)

  • Deborah Schmidt

    (Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association)

  • Harald F. Hess

    (Howard Hughes Medical Institute)

  • C. Shan Xu

    (Howard Hughes Medical Institute
    Yale School of Medicine)

  • Gaia Pigino

    (Human Technopole (HT))

  • Michele Solimena

    (TU Dresden
    TU Dresden
    German Center for Diabetes Research (DZD e.V.)
    TU Dresden)

Abstract

Primary cilia are sensory organelles present in many cell types, partaking in various signaling processes. Primary cilia of pancreatic beta cells play pivotal roles in paracrine signaling and their dysfunction is linked to diabetes. Yet, the structural basis for their functions is unclear. We present three-dimensional reconstructions of beta cell primary cilia by electron and expansion microscopy. These cilia are spatially confined within deep ciliary pockets or narrow spaces between cells, lack motility components and display an unstructured axoneme organization. Furthermore, we observe a plethora of beta cell cilia-cilia and cilia-cell interactions with other islet and non-islet cells. Most remarkably, we have identified and characterized axo-ciliary synapses between beta cell cilia and the cholinergic islet innervation. These findings highlight the beta cell cilia’s role in islet connectivity, pointing at their function in integrating islet intrinsic and extrinsic signals and contribute to understanding their significance in health and diabetes.

Suggested Citation

  • Andreas Müller & Nikolai Klena & Song Pang & Leticia Elizabeth Galicia Garcia & Oleksandra Topcheva & Solange Aurrecoechea Duran & Davud Sulaymankhil & Monika Seliskar & Hassan Mziaut & Eyke Schöniger, 2024. "Structure, interaction and nervous connectivity of beta cell primary cilia," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53348-5
    DOI: 10.1038/s41467-024-53348-5
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    as
    1. Ilya Belevich & Merja Joensuu & Darshan Kumar & Helena Vihinen & Eija Jokitalo, 2016. "Microscopy Image Browser: A Platform for Segmentation and Analysis of Multidimensional Datasets," PLOS Biology, Public Library of Science, vol. 14(1), pages 1-13, January.
    2. Vincent Louvel & Romuald Haase & Olivier Mercey & Marine H. Laporte & Thibaut Eloy & Étienne Baudrier & Denis Fortun & Dominique Soldati-Favre & Virginie Hamel & Paul Guichard, 2023. "iU-ExM: nanoscopy of organelles and tissues with iterative ultrastructure expansion microscopy," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Travis Walton & Hao Wu & Alan Brown, 2021. "Structure of a microtubule-bound axonemal dynein," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    4. Marten Postma & Joachim Goedhart, 2019. "PlotsOfData—A web app for visualizing data together with their summaries," PLOS Biology, Public Library of Science, vol. 17(3), pages 1-8, March.
    5. Travis Walton & Miao Gui & Simona Velkova & Mahmoud R. Fassad & Robert A. Hirst & Eric Haarman & Christopher O’Callaghan & Mathieu Bottier & Thomas Burgoyne & Hannah M. Mitchison & Alan Brown, 2023. "Axonemal structures reveal mechanoregulatory and disease mechanisms," Nature, Nature, vol. 618(7965), pages 625-633, June.
    6. Jantje M. Gerdes & Sonia Christou-Savina & Yan Xiong & Tilo Moede & Noah Moruzzi & Patrick Karlsson-Edlund & Barbara Leibiger & Ingo B. Leibiger & Claes-Göran Östenson & Philip L. Beales & Per-Olof Be, 2014. "Ciliary dysfunction impairs beta-cell insulin secretion and promotes development of type 2 diabetes in rodents," Nature Communications, Nature, vol. 5(1), pages 1-13, December.
    7. Francesco Volta & M. Julia Scerbo & Anett Seelig & Robert Wagner & Nils O’Brien & Felicia Gerst & Andreas Fritsche & Hans-Ulrich Häring & Anja Zeigerer & Susanne Ullrich & Jantje M. Gerdes, 2019. "Glucose homeostasis is regulated by pancreatic β-cell cilia via endosomal EphA-processing," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    8. John T. Walker & Diane C. Saunders & Vivek Rai & Hung-Hsin Chen & Peter Orchard & Chunhua Dai & Yasminye D. Pettway & Alexander L. Hopkirk & Conrad V. Reihsmann & Yicheng Tao & Simin Fan & Shristi Shr, 2023. "Genetic risk converges on regulatory networks mediating early type 2 diabetes," Nature, Nature, vol. 624(7992), pages 621-629, December.
    9. Joris Roels & Frank Vernaillen & Anna Kremer & Amanda Gonçalves & Jan Aelterman & Hiêp Q. Luong & Bart Goossens & Wilfried Philips & Saskia Lippens & Yvan Saeys, 2020. "An interactive ImageJ plugin for semi-automated image denoising in electron microscopy," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    10. Keiichi Katsumoto & Siham Yennek & Chunguang Chen & Luis Fernando Delgadillo Silva & Sofia Traikov & Dror Sever & Ajuna Azad & Jingdong Shan & Seppo Vainio & Nikolay Ninov & Stephan Speier & Anne Grap, 2022. "Wnt4 is heterogeneously activated in maturing β-cells to control calcium signaling, metabolism and function," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. C. Shan Xu & Song Pang & Gleb Shtengel & Andreas Müller & Alex T. Ritter & Huxley K. Hoffman & Shin-ya Takemura & Zhiyuan Lu & H. Amalia Pasolli & Nirmala Iyer & Jeeyun Chung & Davis Bennett & Aubrey , 2021. "An open-access volume electron microscopy atlas of whole cells and tissues," Nature, Nature, vol. 599(7883), pages 147-151, November.
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