IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49833-6.html
   My bibliography  Save this article

Microscale geometrical modulation of PIEZO1 mediated mechanosensing through cytoskeletal redistribution

Author

Listed:
  • Haoqing Jerry Wang

    (The University of Sydney
    The University of Sydney
    Camperdown)

  • Yao Wang

    (The University of Sydney)

  • Seyed Sajad Mirjavadi

    (The University of Sydney)

  • Tomas Andersen

    (The University of Sydney)

  • Laura Moldovan

    (The University of Sydney
    The University of Sydney
    Camperdown)

  • Parham Vatankhah

    (The University of Sydney)

  • Blake Russell

    (The University of Sydney)

  • Jasmine Jin

    (The University of Sydney)

  • Zijing Zhou

    (Victor Chang Cardiac Research Institute)

  • Qing Li

    (The University of Sydney)

  • Charles D. Cox

    (Victor Chang Cardiac Research Institute
    University of New South Wale)

  • Qian Peter Su

    (Camperdown
    University of Technology Sydney)

  • Lining Arnold Ju

    (The University of Sydney
    The University of Sydney
    Camperdown
    The University of Sydney)

Abstract

The microgeometry of the cellular microenvironment profoundly impacts cellular behaviors, yet the link between it and the ubiquitously expressed mechanosensitive ion channel PIEZO1 remains unclear. Herein, we describe a fluorescent micropipette aspiration assay that allows for simultaneous visualization of intracellular calcium dynamics and cytoskeletal architecture in real-time, under varied micropipette geometries. By integrating elastic shell finite element analysis with fluorescent lifetime imaging microscopy and employing PIEZO1-specific transgenic red blood cells and HEK cell lines, we demonstrate a direct correlation between the microscale geometry of aspiration and PIEZO1-mediated calcium signaling. We reveal that increased micropipette tip angles and physical constrictions lead to a significant reorganization of F-actin, accumulation at the aspirated cell neck, and subsequently amplify the tension stress at the dome of the cell to induce more PIEZO1’s activity. Disruption of the F-actin network or inhibition of its mobility leads to a notable decline in PIEZO1 mediated calcium influx, underscoring its critical role in cellular mechanosensing amidst geometrical constraints.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49833-6
    DOI: 10.1038/s41467-024-49833-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49833-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-49833-6?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. Hamza Atcha & Amit Jairaman & Jesse R. Holt & Vijaykumar S. Meli & Raji R. Nagalla & Praveen Krishna Veerasubramanian & Kyle T. Brumm & Huy E. Lim & Shivashankar Othy & Michael D. Cahalan & Medha M. P, 2021. "Mechanically activated ion channel Piezo1 modulates macrophage polarization and stiffness sensing," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. 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.
    3. M. Fritzsche & D. Li & H. Colin-York & V. T. Chang & E. Moeendarbary & J. H. Felce & E. Sezgin & G. Charras & E. Betzig & C. Eggeling, 2017. "Self-organizing actin patterns shape membrane architecture but not cell mechanics," Nature Communications, Nature, vol. 8(1), pages 1-14, April.
    4. Chih-Hao Lu & Kayvon Pedram & Ching-Ting Tsai & Taylor Jones & Xiao Li & Melissa L. Nakamoto & Carolyn R. Bertozzi & Bianxiao Cui, 2022. "Membrane curvature regulates the spatial distribution of bulky glycoproteins," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Anne Reversat & Florian Gaertner & Jack Merrin & Julian Stopp & Saren Tasciyan & Juan Aguilera & Ingrid Vries & Robert Hauschild & Miroslav Hons & Matthieu Piel & Andrew Callan-Jones & Raphael Voituri, 2020. "Cellular locomotion using environmental topography," Nature, Nature, vol. 582(7813), pages 582-585, June.
    6. 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.
    7. 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.
    8. Xuzhong Yang & Chao Lin & Xudong Chen & Shouqin Li & Xueming Li & Bailong Xiao, 2022. "Structure deformation and curvature sensing of PIEZO1 in lipid membranes," Nature, Nature, vol. 604(7905), pages 377-383, April.
    9. Bo Shen & Alpaslan Tasdogan & Jessalyn M. Ubellacker & Jingzhu Zhang & Elena D. Nosyreva & Liming Du & Malea M. Murphy & Shuiqing Hu & Yating Yi & Nergis Kara & Xin Liu & Shay Guela & Yuemeng Jia & Vi, 2021. "A mechanosensitive peri-arteriolar niche for osteogenesis and lymphopoiesis," Nature, Nature, vol. 591(7850), pages 438-444, March.
    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. 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.
    2. 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.
    3. 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.
    4. 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.
    5. Chao Jiang & Hong-Yu Luo & Xinpeng Xu & Shuo-Xing Dou & Wei Li & Dongshi Guan & Fangfu Ye & Xiaosong Chen & Ming Guo & Peng-Ye Wang & Hui Li, 2023. "Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. Xianzhu Zhang & Wei Jiang & Chang Xie & Xinyu Wu & Qian Ren & Fei Wang & Xilin Shen & Yi Hong & Hongwei Wu & Youguo Liao & Yi Zhang & Renjie Liang & Wei Sun & Yuqing Gu & Tao Zhang & Yishan Chen & Wei, 2022. "Msx1+ stem cells recruited by bioactive tissue engineering graft for bone regeneration," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Matthias Pöhnl & Marius F. W. Trollmann & Rainer A. Böckmann, 2023. "Nonuniversal impact of cholesterol on membranes mobility, curvature sensing and elasticity," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. 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.
    9. Yang Li & Nan Li & Wei Liu & Aleksander Prominski & Seounghun Kang & Yahao Dai & Youdi Liu & Huawei Hu & Shinya Wai & Shilei Dai & Zhe Cheng & Qi Su & Ping Cheng & Chen Wei & Lihua Jin & Jeffrey A. Hu, 2023. "Achieving tissue-level softness on stretchable electronics through a generalizable soft interlayer design," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    10. Joann Chongsaritsinsuk & Alexandra D. Steigmeyer & Keira E. Mahoney & Mia A. Rosenfeld & Taryn M. Lucas & Courtney M. Smith & Alice Li & Deniz Ince & Fiona L. Kearns & Alexandria S. Battison & Marie A, 2023. "Glycoproteomic landscape and structural dynamics of TIM family immune checkpoints enabled by mucinase SmE," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. 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.
    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. Jonathan Mount & Grigory Maksaev & Brock T. Summers & James A. J. Fitzpatrick & Peng Yuan, 2022. "Structural basis for mechanotransduction in a potassium-dependent mechanosensitive ion channel," Nature Communications, Nature, vol. 13(1), pages 1-11, 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. Hyuek Jong Lee & Jueun Lee & Myung Jin Yang & Young-Chan Kim & Seon Pyo Hong & Jung Mo Kim & Geum-Sook Hwang & Gou Young Koh, 2023. "Endothelial cell-derived stem cell factor promotes lipid accumulation through c-Kit-mediated increase of lipogenic enzymes in brown adipocytes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    16. 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.
    17. Sergei Butenko & Raji R. Nagalla & Christian F. Guerrero-Juarez & Francesco Palomba & Li-Mor David & Ronald Q. Nguyen & Denise Gay & Axel A. Almet & Michelle A. Digman & Qing Nie & Philip O. Scumpia &, 2024. "Hydrogel crosslinking modulates macrophages, fibroblasts, and their communication, during wound healing," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    18. 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.
    19. 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.
    20. Adrienne Anginot & Julie Nguyen & Zeina Abou Nader & Vincent Rondeau & Amélie Bonaud & Maria Kalogeraki & Antoine Boutin & Julia P. Lemos & Valeria Bisio & Joyce Koenen & Lea Hanna Doumit Sakr & Amand, 2023. "WHIM Syndrome-linked CXCR4 mutations drive osteoporosis," 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:15:y:2024:i:1:d:10.1038_s41467-024-49833-6. 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.