IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40134-y.html
   My bibliography  Save this article

Highly specific and non-invasive imaging of Piezo1-dependent activity across scales using GenEPi

Author

Listed:
  • Sine Yaganoglu

    (Eidgenössische Technische Hochschule (ETH) Zurich)

  • Konstantinos Kalyviotis

    (Imperial College London)

  • Christina Vagena-Pantoula

    (Imperial College London)

  • Dörthe Jülich

    (Yale University)

  • Benjamin M. Gaub

    (Eidgenössische Technische Hochschule (ETH) Zurich)

  • Maaike Welling

    (Eidgenössische Technische Hochschule (ETH) Zurich
    Imperial College London)

  • Tatiana Lopes

    (Digestion, and Reproduction, Imperial College London)

  • Dariusz Lachowski

    (Imperial College London)

  • See Swee Tang

    (Imperial College London)

  • Armando Del Rio Hernandez

    (Imperial College London)

  • Victoria Salem

    (Imperial College London)

  • Daniel J. Müller

    (Eidgenössische Technische Hochschule (ETH) Zurich)

  • Scott A. Holley

    (Yale University)

  • Julien Vermot

    (Imperial College London)

  • Jian Shi

    (University of Leeds)

  • Nordine Helassa

    (St. George’s, University of London
    University of Liverpool)

  • Katalin Török

    (St. George’s, University of London)

  • Periklis Pantazis

    (Eidgenössische Technische Hochschule (ETH) Zurich
    Imperial College London)

Abstract

Mechanosensing is a ubiquitous process to translate external mechanical stimuli into biological responses. Piezo1 ion channels are directly gated by mechanical forces and play an essential role in cellular mechanotransduction. However, readouts of Piezo1 activity are mainly examined by invasive or indirect techniques, such as electrophysiological analyses and cytosolic calcium imaging. Here, we introduce GenEPi, a genetically-encoded fluorescent reporter for non-invasive optical monitoring of Piezo1-dependent activity. We demonstrate that GenEPi has high spatiotemporal resolution for Piezo1-dependent stimuli from the single-cell level to that of the entire organism. GenEPi reveals transient, local mechanical stimuli in the plasma membrane of single cells, resolves repetitive contraction-triggered stimulation of beating cardiomyocytes within microtissues, and allows for robust and reliable monitoring of Piezo1-dependent activity in vivo. GenEPi will enable non-invasive optical monitoring of Piezo1 activity in mechanochemical feedback loops during development, homeostatic regulation, and disease.

Suggested Citation

  • Sine Yaganoglu & Konstantinos Kalyviotis & Christina Vagena-Pantoula & Dörthe Jülich & Benjamin M. Gaub & Maaike Welling & Tatiana Lopes & Dariusz Lachowski & See Swee Tang & Armando Del Rio Hernandez, 2023. "Highly specific and non-invasive imaging of Piezo1-dependent activity across scales using GenEPi," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40134-y
    DOI: 10.1038/s41467-023-40134-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40134-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-40134-y?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. Bertrand Coste & Bailong Xiao & Jose S. Santos & Ruhma Syeda & Jörg Grandl & Kathryn S. Spencer & Sung Eun Kim & Manuela Schmidt & Jayanti Mathur & Adrienne E. Dubin & Mauricio Montal & Ardem Patapout, 2012. "Piezo proteins are pore-forming subunits of mechanically activated channels," Nature, Nature, vol. 483(7388), pages 176-181, March.
    2. Xiaonan R. Sun & Aleksandra Badura & Diego A. Pacheco & Laura A. Lynch & Eve R. Schneider & Matthew P. Taylor & Ian B. Hogue & Lynn W. Enquist & Mala Murthy & Samuel S. -H. Wang, 2013. "Fast GCaMPs for improved tracking of neuronal activity," Nature Communications, Nature, vol. 4(1), pages 1-10, October.
    3. Joachim Goedhart, 2020. "PlotTwist: A web app for plotting and annotating continuous data," PLOS Biology, Public Library of Science, vol. 18(1), pages 1-10, January.
    4. Juliette Albuisson & Swetha E Murthy & Michael Bandell & Bertrand Coste & Hélène Louis-dit-Picard & Jayanti Mathur & Madeleine Fénéant-Thibault & Gérard Tertian & Jean-Pierre de Jaureguiberry & Pierre, 2013. "Dehydrated hereditary stomatocytosis linked to gain-of-function mutations in mechanically activated PIEZO1 ion channels," Nature Communications, Nature, vol. 4(1), pages 1-9, October.
    5. Elisavet Fotiou & Silvia Martin-Almedina & Michael A. Simpson & Shin Lin & Kristiana Gordon & Glen Brice & Giles Atton & Iona Jeffery & David C. Rees & Cyril Mignot & Julie Vogt & Tessa Homfray & Mich, 2015. "Novel mutations in PIEZO1 cause an autosomal recessive generalized lymphatic dysplasia with non-immune hydrops fetalis," Nature Communications, Nature, vol. 6(1), pages 1-6, November.
    6. Thomas Juan & Agatha Ribeiro da Silva & Bárbara Cardoso & SoEun Lim & Violette Charteau & Didier Y. R. Stainier, 2023. "Multiple pkd and piezo gene family members are required for atrioventricular valve formation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. S. A. Gudipaty & J. Lindblom & P. D. Loftus & M. J. Redd & K. Edes & C. F. Davey & V. Krishnegowda & J. Rosenblatt, 2017. "Mechanical stretch triggers rapid epithelial cell division through Piezo1," Nature, Nature, vol. 543(7643), pages 118-121, March.
    8. Jing Li & Bing Hou & Sarka Tumova & Katsuhiko Muraki & Alexander Bruns & Melanie J. Ludlow & Alicia Sedo & Adam J. Hyman & Lynn McKeown & Richard S. Young & Nadira Y. Yuldasheva & Yasser Majeed & Lesl, 2014. "Piezo1 integration of vascular architecture with physiological force," Nature, Nature, vol. 515(7526), pages 279-282, November.
    9. Fan Jiang & Kunlun Yin & Kun Wu & Mingmin Zhang & Shiqiang Wang & Heping Cheng & Zhou Zhou & Bailong Xiao, 2021. "The mechanosensitive Piezo1 channel mediates heart mechano-chemo transduction," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    10. George T. Eisenhoffer & Patrick D. Loftus & Masaaki Yoshigi & Hideo Otsuna & Chi-Bin Chien & Paul A. Morcos & Jody Rosenblatt, 2012. "Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia," Nature, Nature, vol. 484(7395), pages 546-549, April.
    11. Viktor Lukacs & Jayanti Mathur & Rong Mao & Pinar Bayrak-Toydemir & Melinda Procter & Stuart M. Cahalan & Helen J. Kim & Michael Bandell & Nicola Longo & Ronald W. Day & David A. Stevenson & Ardem Pat, 2015. "Impaired PIEZO1 function in patients with a novel autosomal recessive congenital lymphatic dysplasia," Nature Communications, Nature, vol. 6(1), pages 1-7, November.
    12. Mirko Moroni & M. Rocio Servin-Vences & Raluca Fleischer & Oscar Sánchez-Carranza & Gary R. Lewin, 2018. "Voltage gating of mechanosensitive PIEZO channels," Nature Communications, Nature, vol. 9(1), pages 1-15, 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. Nathalia G. Amado & Elena D. Nosyreva & David Thompson & Thomas J. Egeland & Osita W. Ogujiofor & Michelle Yang & Alexandria N. Fusco & Niccolo Passoni & Jeremy Mathews & Brandi Cantarel & Linda A. Ba, 2024. "PIEZO1 loss-of-function compound heterozygous mutations in the rare congenital human disorder Prune Belly Syndrome," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Xin Rui Lim & Mohammad M. Abd-Alhaseeb & Michael Ippolito & Masayo Koide & Amanda J. Senatore & Curtis Plante & Ashwini Hariharan & Nick Weir & Thomas A. Longden & Kathryn A. Laprade & James M. Staffo, 2024. "Endothelial Piezo1 channel mediates mechano-feedback control of brain blood flow," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Francisco Andrés Peralta & Mélaine Balcon & Adeline Martz & Deniza Biljali & Federico Cevoli & Benoit Arnould & Antoine Taly & Thierry Chataigneau & Thomas Grutter, 2023. "Optical control of PIEZO1 channels," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Haoqing Jerry Wang & Yao Wang & Seyed Sajad Mirjavadi & Tomas Andersen & Laura Moldovan & Parham Vatankhah & Blake Russell & Jasmine Jin & Zijing Zhou & Qing Li & Charles D. Cox & Qian Peter Su & Lini, 2024. "Microscale geometrical modulation of PIEZO1 mediated mechanosensing through cytoskeletal redistribution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Shilong Yang & Xinwen Miao & Steven Arnold & Boxuan Li & Alan T. Ly & Huan Wang & Matthew Wang & Xiangfu Guo & Medha M. Pathak & Wenting Zhao & Charles D. Cox & Zheng Shi, 2022. "Membrane curvature governs the distribution of Piezo1 in live cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Yingying Ye & Mohammad Barghouth & Haiqiang Dou & Cheng Luan & Yongzhi Wang & Alexandros Karagiannopoulos & Xiaoping Jiang & Ulrika Krus & Malin Fex & Quan Zhang & Lena Eliasson & Patrik Rorsman & Enm, 2022. "A critical role of the mechanosensor PIEZO1 in glucose-induced insulin secretion in pancreatic β-cells," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Carlos A. Z. Bassetto & Juergen Pfeffermann & Rohit Yadav & Simon Strassgschwandtner & Toma Glasnov & Francisco Bezanilla & Peter Pohl, 2024. "Photolipid excitation triggers depolarizing optocapacitive currents and action potentials," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Sara Baratchi & Habiba Danish & Chanly Chheang & Ying Zhou & Angela Huang & Austin Lai & Manijeh Khanmohammadi & Kylie M. Quinn & Khashayar Khoshmanesh & Karlheinz Peter, 2024. "Piezo1 expression in neutrophils regulates shear-induced NETosis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Timo N. Kohler & Joachim Jonghe & Anna L. Ellermann & Ayaka Yanagida & Michael Herger & Erin M. Slatery & Antonia Weberling & Clara Munger & Katrin Fischer & Carla Mulas & Alex Winkel & Connor Ross & , 2023. "Plakoglobin is a mechanoresponsive regulator of naive pluripotency," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    10. Mohammad Ikbal Choudhury & Yizeng Li & Panagiotis Mistriotis & Ana Carina N. Vasconcelos & Eryn E. Dixon & Jing Yang & Morgan Benson & Debonil Maity & Rebecca Walker & Leigha Martin & Fatima Koroma & , 2022. "Kidney epithelial cells are active mechano-biological fluid pumps," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    11. Omer Mano & Damon A Clark, 2017. "Graphics Processing Unit-Accelerated Code for Computing Second-Order Wiener Kernels and Spike-Triggered Covariance," PLOS ONE, Public Library of Science, vol. 12(1), pages 1-11, January.
    12. K. Sri-Ranjan & J. L. Sanchez-Alonso & P. Swiatlowska & S. Rothery & P. Novak & S. Gerlach & D. Koeninger & B. Hoffmann & R. Merkel & M. M. Stevens & S. X. Sun & J. Gorelik & Vania M. M. Braga, 2022. "Intrinsic cell rheology drives junction maturation," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    13. Yuqi Qin & Daqi Yu & Dan Wu & Jiangqing Dong & William Thomas Li & Chang Ye & Kai Chit Cheung & Yingyi Zhang & Yun Xu & YongQiang Wang & Yun Stone Shi & Shangyu Dang, 2023. "Cryo-EM structure of TMEM63C suggests it functions as a monomer," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    14. Jiayu Liu & Chuanrong Zhao & Xue Xiao & Aohan Li & Yueqi Liu & Jianan Zhao & Linwei Fan & Zhenhui Liang & Wei Pang & Weijuan Yao & Wei Li & Jing Zhou, 2023. "Endothelial discoidin domain receptor 1 senses flow to modulate YAP activation," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    15. Basila Moochickal Assainar & Kaushik Ragunathan & Ryan D. Baldridge, 2024. "Direct observation of autoubiquitination for an integral membrane ubiquitin ligase in ERAD," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    16. Nathan Ronceray & Massimo Spina & Vanessa Hui Yin Chou & Chwee Teck Lim & Andre K. Geim & Slaven Garaj, 2024. "Elastocapillarity-driven 2D nano-switches enable zeptoliter-scale liquid encapsulation," Nature Communications, Nature, vol. 15(1), pages 1-8, December.
    17. Manuela Völkner & Felix Wagner & Lisa Maria Steinheuer & Madalena Carido & Thomas Kurth & Ali Yazbeck & Jana Schor & Stephanie Wieneke & Lynn J. A. Ebner & Claudia Toro Runzer & David Taborsky & Katja, 2022. "HBEGF-TNF induce a complex outer retinal pathology with photoreceptor cell extrusion in human organoids," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    18. Remo Monti & Pia Rautenstrauch & Mahsa Ghanbari & Alva Rani James & Matthias Kirchler & Uwe Ohler & Stefan Konigorski & Christoph Lippert, 2022. "Identifying interpretable gene-biomarker associations with functionally informed kernel-based tests in 190,000 exomes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    19. Jonathan Madar & Namrata Tiwari & Cristina Smith & Divya Sharma & Shanwei Shen & Alsiddig Elmahdi & Liya Y. Qiao, 2023. "Piezo2 regulates colonic mechanical sensitivity in a sex specific manner in mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    20. Luis O. Romero & Rebeca Caires & A. Kaitlyn Victor & Juanma Ramirez & Francisco J. Sierra-Valdez & Patrick Walsh & Vincent Truong & Jungsoo Lee & Ugo Mayor & Lawrence T. Reiter & Valeria Vásquez & Jul, 2023. "Linoleic acid improves PIEZO2 dysfunction in a mouse model of Angelman Syndrome," Nature Communications, Nature, vol. 14(1), pages 1-20, 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:14:y:2023:i:1:d:10.1038_s41467-023-40134-y. 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.