IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-30153-6.html
   My bibliography  Save this article

A negative-solvatochromic fluorescent probe for visualizing intracellular distributions of fatty acid metabolites

Author

Listed:
  • Keiji Kajiwara

    (Nagoya University)

  • Hiroshi Osaki

    (Nagoya University)

  • Steffen Greßies

    (Westfälische Wilhelms-Universität Münster)

  • Keiko Kuwata

    (Nagoya University)

  • Ju Hyun Kim

    (Westfälische Wilhelms-Universität Münster
    Gyeongsang National University)

  • Tobias Gensch

    (Westfälische Wilhelms-Universität Münster
    TU Berlin)

  • Yoshikatsu Sato

    (Nagoya University)

  • Frank Glorius

    (Westfälische Wilhelms-Universität Münster)

  • Shigehiro Yamaguchi

    (Nagoya University
    Nagoya University)

  • Masayasu Taki

    (Nagoya University)

Abstract

Metabolic distribution of fatty acid to organelles is an essential biological process for energy homeostasis as well as for the maintenance of membrane integrity, and the metabolic pathways are strictly regulated in response to environmental stimuli. Herein, we report a fluorescent fatty acid probe, which bears an azapyrene dye that changes its absorption and emission features depending on the microenvironment polarity of the organelle into which it is transported. Owing to the environmental sensitivity of this dye, the distribution of the metabolically incorporated probe in non-polar lipid droplets, medium-polarity membranes, and the polar aqueous regions, can be visualized in different colors. Based on density scatter plots of the fluorophore, we demonstrate that the degradation of triacylglycerols in lipid droplets occurs predominantly via lipolysis rather than lipophagy in nutrition-starved hepatocytes. This tool can thus be expected to significantly advance our understanding of the lipid metabolism in living organisms.

Suggested Citation

  • Keiji Kajiwara & Hiroshi Osaki & Steffen Greßies & Keiko Kuwata & Ju Hyun Kim & Tobias Gensch & Yoshikatsu Sato & Frank Glorius & Shigehiro Yamaguchi & Masayasu Taki, 2022. "A negative-solvatochromic fluorescent probe for visualizing intracellular distributions of fatty acid metabolites," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30153-6
    DOI: 10.1038/s41467-022-30153-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-30153-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-30153-6?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. Akiko Kuma & Masahiko Hatano & Makoto Matsui & Akitsugu Yamamoto & Haruaki Nakaya & Tamotsu Yoshimori & Yoshinori Ohsumi & Takeshi Tokuhisa & Noboru Mizushima, 2004. "The role of autophagy during the early neonatal starvation period," Nature, Nature, vol. 432(7020), pages 1032-1036, December.
    2. Rajat Singh & Susmita Kaushik & Yongjun Wang & Youqing Xiang & Inna Novak & Masaaki Komatsu & Keiji Tanaka & Ana Maria Cuervo & Mark J. Czaja, 2009. "Autophagy regulates lipid metabolism," Nature, Nature, vol. 458(7242), pages 1131-1135, April.
    3. Kamil Sołtysik & Yuki Ohsaki & Tsuyako Tatematsu & Jinglei Cheng & Toyoshi Fujimoto, 2019. "Nuclear lipid droplets derive from a lipoprotein precursor and regulate phosphatidylcholine synthesis," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    4. Caroline Mauvezin & Péter Nagy & Gábor Juhász & Thomas P. Neufeld, 2015. "Autophagosome–lysosome fusion is independent of V-ATPase-mediated acidification," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
    5. Kamil Sołtysik & Yuki Ohsaki & Tsuyako Tatematsu & Jinglei Cheng & Toyoshi Fujimoto, 2019. "Author Correction: Nuclear lipid droplets derive from a lipoprotein precursor and regulate phosphatidylcholine synthesis," Nature Communications, Nature, vol. 10(1), pages 1-1, 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. Odeta Meçe & Diede Houbaert & Maria-Livia Sassano & Tania Durré & Hannelore Maes & Marco Schaaf & Sanket More & Maarten Ganne & Melissa García-Caballero & Mila Borri & Jelle Verhoeven & Madhur Agrawal, 2022. "Lipid droplet degradation by autophagy connects mitochondria metabolism to Prox1-driven expression of lymphatic genes and lymphangiogenesis," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Lin-lin Zhao & Ru Chen & Ziyu Bai & Junyi Liu & Yuhao Zhang & Yicheng Zhong & Meng-xiang Sun & Peng Zhao, 2024. "Autophagy-mediated degradation of integumentary tapetum is critical for embryo pattern formation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Hong Huang & Qinqin Ouyang & Min Zhu & Haijia Yu & Kunrong Mei & Rong Liu, 2021. "mTOR-mediated phosphorylation of VAMP8 and SCFD1 regulates autophagosome maturation," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    4. Aftab Nadeem & Athar Alam & Eric Toh & Si Lhyam Myint & Zia ur Rehman & Tao Liu & Marta Bally & Anna Arnqvist & Hui Wang & Jun Zhu & Karina Persson & Bernt Eric Uhlin & Sun Nyunt Wai, 2021. "Phosphatidic acid-mediated binding and mammalian cell internalization of the Vibrio cholerae cytotoxin MakA," PLOS Pathogens, Public Library of Science, vol. 17(3), pages 1-34, March.
    5. Scotland E. Farley & Jennifer E. Kyle & Hans C. Leier & Lisa M. Bramer & Jules B. Weinstein & Timothy A. Bates & Joon-Yong Lee & Thomas O. Metz & Carsten Schultz & Fikadu G. Tafesse, 2022. "A global lipid map reveals host dependency factors conserved across SARS-CoV-2 variants," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Yoshito Minami & Atsushi Hoshino & Yusuke Higuchi & Masahide Hamaguchi & Yusaku Kaneko & Yuhei Kirita & Shunta Taminishi & Toshiyuki Nishiji & Akiyuki Taruno & Michiaki Fukui & Zoltan Arany & Satoaki , 2023. "Liver lipophagy ameliorates nonalcoholic steatohepatitis through extracellular lipid secretion," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Elodie Mailler & Carlos M. Guardia & Xiaofei Bai & Michal Jarnik & Chad D. Williamson & Yan Li & Nunziata Maio & Andy Golden & Juan S. Bonifacino, 2021. "The autophagy protein ATG9A enables lipid mobilization from lipid droplets," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    8. Wenjun Wang & Junyang Tan & Xiaomin Liu & Wenqi Guo & Mengmeng Li & Xinjie Liu & Yanyan Liu & Wenyu Dai & Liubing Hu & Yimin Wang & Qiuxia Lu & Wen Xing Lee & Hong-Wen Tang & Qinghua Zhou, 2023. "Cytoplasmic Endonuclease G promotes nonalcoholic fatty liver disease via mTORC2-AKT-ACLY and endoplasmic reticulum stress," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Guanlan Hu & Catriona Ling & Lijun Chi & Mehakpreet K. Thind & Samuel Furse & Albert Koulman & Jonathan R. Swann & Dorothy Lee & Marjolein M. Calon & Celine Bourdon & Christian J. Versloot & Barbara M, 2022. "The role of the tryptophan-NAD + pathway in a mouse model of severe malnutrition induced liver dysfunction," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    10. Donghai Cui & Zixiang Wang & Qianli Dang & Jing Wang & Junchao Qin & Jianping Song & Xiangyu Zhai & Yachao Zhou & Ling Zhao & Gang Lu & Hongbin Liu & Gang Liu & Runping Liu & Changshun Shao & Xiyu Zha, 2023. "Spliceosome component Usp39 contributes to hepatic lipid homeostasis through the regulation of autophagy," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Marika K. Kucińska & Juliette Fedry & Carmela Galli & Diego Morone & Andrea Raimondi & Tatiana Soldà & Friedrich Förster & Maurizio Molinari, 2023. "TMX4-driven LINC complex disassembly and asymmetric autophagy of the nuclear envelope upon acute ER stress," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    12. Jialiu Zeng & Rebeca Acin-Perez & Essam A. Assali & Andrew Martin & Alexandra J. Brownstein & Anton Petcherski & Lucía Fernández-del-Rio & Ruiqing Xiao & Chih Hung Lo & Michaël Shum & Marc Liesa & Xue, 2023. "Restoration of lysosomal acidification rescues autophagy and metabolic dysfunction in non-alcoholic fatty liver disease," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Robin Caire & Estelle Audoux & Mireille Thomas & Elisa Dalix & Aurélien Peyron & Killian Rodriguez & Nicola Pordone & Johann Guillemot & Yann Dickerscheit & Hubert Marotte & François Vandenesch & Fréd, 2022. "YAP promotes cell-autonomous immune responses to tackle intracellular Staphylococcus aureus in vitro," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    14. Vanitha Nithianandam & Hassan Bukhari & Matthew J. Leventhal & Rachel A. Battaglia & Xianjun Dong & Ernest Fraenkel & Mel B. Feany, 2023. "Integrative analysis reveals a conserved role for the amyloid precursor protein in proteostasis during aging," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    15. Youping Lin & Haixu Chen & Lei Wang & Jiaojiao Su & Junbo Li & Xin Huang, 2024. "Lipase activated endocytosis-like behavior of oil-in-water emulsion," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    16. Leslie A. Rowland & Adilson Guilherme & Felipe Henriques & Chloe DiMarzio & Sean Munroe & Nicole Wetoska & Mark Kelly & Keith Reddig & Gregory Hendricks & Meixia Pan & Xianlin Han & Olga R. Ilkayeva &, 2023. "De novo lipogenesis fuels adipocyte autophagosome and lysosome membrane dynamics," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    17. Yahui Li & Chunyan Li & Chenchen Zhao & Jiayu Wu & Ya Zhu & Fei Wang & Jiepeng Zhong & Yan Yan & Yulan Jin & Weiren Dong & Jinyang Chen & Xianghong Yang & Jiyong Zhou & Boli Hu, 2024. "Coronavirus M protein promotes mitophagy over virophagy by recruiting PDPK1 to phosphorylate SQSTM1 at T138," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    18. Yun Seok Kim & Bongsub Ko & Da Jung Kim & Jihoon Tak & Chang Yeob Han & Joo-Youn Cho & Won Kim & Sang Geon Kim, 2022. "Induction of the hepatic aryl hydrocarbon receptor by alcohol dysregulates autophagy and phospholipid metabolism via PPP2R2D," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    19. Joshua J. Rennick & Cameron J. Nowell & Colin W. Pouton & Angus P. R. Johnston, 2022. "Resolving subcellular pH with a quantitative fluorescent lifetime biosensor," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    20. Denisa Margină & Anca Ungurianu & Carmen Purdel & Dimitris Tsoukalas & Evangelia Sarandi & Maria Thanasoula & Fotios Tekos & Robin Mesnage & Demetrios Kouretas & Aristidis Tsatsakis, 2020. "Chronic Inflammation in the Context of Everyday Life: Dietary Changes as Mitigating Factors," IJERPH, MDPI, vol. 17(11), pages 1-27, June.

    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:13:y:2022:i:1:d:10.1038_s41467-022-30153-6. 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.