IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45863-2.html
   My bibliography  Save this article

ALLO-1- and IKKE-1-dependent positive feedback mechanism promotes the initiation of paternal mitochondrial autophagy

Author

Listed:
  • Taeko Sasaki

    (Gunma University, Maebashi
    Gunma University, Maebashi)

  • Yasuharu Kushida

    (Gunma University, Maebashi)

  • Takuya Norizuki

    (Gunma University, Maebashi)

  • Hidetaka Kosako

    (Tokushima University)

  • Ken Sato

    (Gunma University, Maebashi)

  • Miyuki Sato

    (Gunma University, Maebashi)

Abstract

Allophagy is responsible for the selective removal of paternally inherited organelles, including mitochondria, in Caenorhabditis elegans embryos, thereby facilitating the maternal inheritance of mitochondrial DNA. We previously identified two key factors in allophagy: an autophagy adaptor allophagy-1 (ALLO-1) and TBK1/IKKε family kinase IKKE-1. However, the precise mechanisms by which ALLO-1 and IKKE-1 regulate local autophagosome formation remain unclear. In this study, we identify two ALLO-1 isoforms with different substrate preferences during allophagy. Live imaging reveals a stepwise mechanism of ALLO-1 localization with rapid cargo recognition, followed by ALLO-1 accumulation around the cargo. In the ikke-1 mutant, the accumulation of ALLO-1, and not the recognition of cargo, is impaired, resulting in the failure of isolation membrane formation. Our results also suggest a feedback mechanism for ALLO-1 accumulation via EPG-7/ATG-11, a worm homolog of FIP200, which is a candidate for IKKE-1-dependent phosphorylation. This feedback mechanism may underlie the ALLO-1-dependent initiation and progression of autophagosome formation around paternal organelles.

Suggested Citation

  • Taeko Sasaki & Yasuharu Kushida & Takuya Norizuki & Hidetaka Kosako & Ken Sato & Miyuki Sato, 2024. "ALLO-1- and IKKE-1-dependent positive feedback mechanism promotes the initiation of paternal mitochondrial autophagy," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45863-2
    DOI: 10.1038/s41467-024-45863-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45863-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-45863-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Keisuke Mochida & Yu Oikawa & Yayoi Kimura & Hiromi Kirisako & Hisashi Hirano & Yoshinori Ohsumi & Hitoshi Nakatogawa, 2015. "Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus," Nature, Nature, vol. 522(7556), pages 359-362, June.
    2. Zixuan Zhou & Jianping Liu & Tao Fu & Ping Wu & Chao Peng & Xinyu Gong & Yingli Wang & Mingfang Zhang & Ying Li & Yaru Wang & Xiaolong Xu & Miao Li & Lifeng Pan, 2021. "Phosphorylation regulates the binding of autophagy receptors to FIP200 Claw domain for selective autophagy initiation," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Benjamin Scott Padman & Thanh Ngoc Nguyen & Louise Uoselis & Marvin Skulsuppaisarn & Lan K. Nguyen & Michael Lazarou, 2019. "LC3/GABARAPs drive ubiquitin-independent recruitment of Optineurin and NDP52 to amplify mitophagy," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    4. Michael Lazarou & Danielle A. Sliter & Lesley A. Kane & Shireen A. Sarraf & Chunxin Wang & Jonathon L. Burman & Dionisia P. Sideris & Adam I. Fogel & Richard J. Youle, 2015. "The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy," Nature, Nature, vol. 524(7565), pages 309-314, August.
    5. Keisuke Mochida & Akinori Yamasaki & Kazuaki Matoba & Hiromi Kirisako & Nobuo N. Noda & Hitoshi Nakatogawa, 2020. "Super-assembly of ER-phagy receptor Atg40 induces local ER remodeling at contacts with forming autophagosomal membranes," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Ning Wang & Yoko Shibata & Joao A. Paulo & Steven P. Gygi & Tom A. Rapoport, 2023. "A conserved membrane curvature-generating protein is crucial for autophagosome formation in fission yeast," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Hayden Weng Siong Tan & Guang Lu & Han Dong & Yik-Lam Cho & Auginia Natalia & Liming Wang & Charlene Chan & Dennis Kappei & Reshma Taneja & Shuo-Chien Ling & Huilin Shao & Shih-Yin Tsai & Wen-Xing Din, 2022. "A degradative to secretory autophagy switch mediates mitochondria clearance in the absence of the mATG8-conjugation machinery," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Shuangcheng Alivia Wu & Chenchen Shen & Xiaoqiong Wei & Xiawei Zhang & Siwen Wang & Xinxin Chen & Mauricio Torres & You Lu & Liangguang Leo Lin & Huilun Helen Wang & Allen H. Hunter & Deyu Fang & Shen, 2023. "The mechanisms to dispose of misfolded proteins in the endoplasmic reticulum of adipocytes," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Kyla Germain & Raphaella W. L. So & Laura F. DiGiovanni & Joel C. Watts & Robert H. J. Bandsma & Peter K. Kim, 2024. "Upregulated pexophagy limits the capacity of selective autophagy," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Qiang Zhu & Matthew E. Combs & Juan Liu & Xue Bai & Wenbo B. Wang & Laura E. Herring & Jiandong Liu & Jason W. Locasale & Dawn E. Bowles & Ryan T. Gross & Michelle Mendiola Pla & Christopher P. Mack &, 2023. "GRAF1 integrates PINK1-Parkin signaling and actin dynamics to mediate cardiac mitochondrial homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    6. Remzi Onur Eren & Göksu Gökberk Kaya & Robin Schwarzer & Manolis Pasparakis, 2024. "IKKε and TBK1 prevent RIPK1 dependent and independent inflammation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Rayene Berkane & Hung Ho-Xuan & Marius Glogger & Pablo Sanz-Martinez & Lorène Brunello & Tristan Glaesner & Santosh Kumar Kuncha & Katharina Holzhüter & Sara Cano-Franco & Viviana Buonomo & Paloma Cab, 2023. "The function of ER-phagy receptors is regulated through phosphorylation-dependent ubiquitination pathways," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Huan Yang & Caroline Sibilla & Raymond Liu & Jina Yun & Bruce A. Hay & Craig Blackstone & David C. Chan & Robert J. Harvey & Ming Guo, 2022. "Clueless/CLUH regulates mitochondrial fission by promoting recruitment of Drp1 to mitochondria," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    9. Yun Xiang & Rui Lyu & Junjie Hu, 2023. "Oligomeric scaffolding for curvature generation by ER tubule-forming proteins," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    10. Zhen Yuan & Kun Cai & Jiajia Li & Ruifeng Chen & Fuhai Zhang & Xuan Tan & Yaming Jiu & Haishuang Chang & Bing Hu & Weiyi Zhang & Binbin Ding, 2024. "ATG14 targets lipid droplets and acts as an autophagic receptor for syntaxin18-regulated lipid droplet turnover," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Michael J. Munson & Benan J. Mathai & Matthew Yoke Wui Ng & Laura Trachsel-Moncho & Laura R. Ballina & Sebastian W. Schultz & Yahyah Aman & Alf H. Lystad & Sakshi Singh & Sachin Singh & Jørgen Wesche , 2021. "GAK and PRKCD are positive regulators of PRKN-independent mitophagy," Nature Communications, Nature, vol. 12(1), pages 1-22, December.
    12. Patricia González-Rodríguez & Daniel J. Klionsky & Bertrand Joseph, 2022. "Autophagy regulation by RNA alternative splicing and implications in human diseases," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    13. Shuang-zhou Peng & Xiao-hui Chen & Si-jie Chen & Jie Zhang & Chuan-ying Wang & Wei-rong Liu & Duo Zhang & Ying Su & Xiao-kun Zhang, 2021. "Phase separation of Nur77 mediates celastrol-induced mitophagy by promoting the liquidity of p62/SQSTM1 condensates," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    14. Shuai Gao & Lingyu Gao & Dailin Yuan & Xu’ai Lin & Stijn Veen, 2024. "Gonococcal OMV-delivered PorB induces epithelial cell mitophagy," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    15. Kihyoun Park & Hyejin Lim & Jinyoung Kim & Yeseong Hwang & Yu Seol Lee & Soo Han Bae & Hyeongseok Kim & Hail Kim & Shin-Wook Kang & Joo Young Kim & Myung-Shik Lee, 2022. "Lysosomal Ca2+-mediated TFEB activation modulates mitophagy and functional adaptation of pancreatic β-cells to metabolic stress," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    16. Simon Maria Kienle & Tobias Schneider & Katrin Stuber & Christoph Globisch & Jasmin Jansen & Florian Stengel & Christine Peter & Andreas Marx & Michael Kovermann & Martin Scheffner, 2022. "Electrostatic and steric effects underlie acetylation-induced changes in ubiquitin structure and function," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45863-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.