IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28205-y.html
   My bibliography  Save this article

Sonogenetic control of mammalian cells using exogenous Transient Receptor Potential A1 channels

Author

Listed:
  • Marc Duque

    (The Salk Institute for Biological Studies)

  • Corinne A. Lee-Kubli

    (The Salk Institute for Biological Studies)

  • Yusuf Tufail

    (The Salk Institute for Biological Studies)

  • Uri Magaram

    (The Salk Institute for Biological Studies
    University of California San Diego)

  • Janki Patel

    (The Salk Institute for Biological Studies)

  • Ahana Chakraborty

    (The Salk Institute for Biological Studies)

  • Jose Mendoza Lopez

    (The Salk Institute for Biological Studies)

  • Eric Edsinger

    (The Salk Institute for Biological Studies)

  • Aditya Vasan

    (University of California San Diego)

  • Rani Shiao

    (The Salk Institute for Biological Studies)

  • Connor Weiss

    (The Salk Institute for Biological Studies)

  • James Friend

    (University of California San Diego)

  • Sreekanth H. Chalasani

    (The Salk Institute for Biological Studies
    University of California San Diego)

Abstract

Ultrasound has been used to non-invasively manipulate neuronal functions in humans and other animals. However, this approach is limited as it has been challenging to target specific cells within the brain or body. Here, we identify human Transient Receptor Potential A1 (hsTRPA1) as a candidate that confers ultrasound sensitivity to mammalian cells. Ultrasound-evoked gating of hsTRPA1 specifically requires its N-terminal tip region and cholesterol interactions; and target cells with an intact actin cytoskeleton, revealing elements of the sonogenetic mechanism. Next, we use calcium imaging and electrophysiology to show that hsTRPA1 potentiates ultrasound-evoked responses in primary neurons. Furthermore, unilateral expression of hsTRPA1 in mouse layer V motor cortical neurons leads to c-fos expression and contralateral limb responses in response to ultrasound delivered through an intact skull. Collectively, we demonstrate that hsTRPA1-based sonogenetics can effectively manipulate neurons within the intact mammalian brain, a method that could be used across species.

Suggested Citation

  • Marc Duque & Corinne A. Lee-Kubli & Yusuf Tufail & Uri Magaram & Janki Patel & Ahana Chakraborty & Jose Mendoza Lopez & Eric Edsinger & Aditya Vasan & Rani Shiao & Connor Weiss & James Friend & Sreeka, 2022. "Sonogenetic control of mammalian cells using exogenous Transient Receptor Potential A1 channels," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28205-y
    DOI: 10.1038/s41467-022-28205-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28205-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28205-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. Mykhailo Y. Batiuk & Araks Martirosyan & Jérôme Wahis & Filip de Vin & Catherine Marneffe & Carola Kusserow & Jordan Koeppen & João Filipe Viana & João Filipe Oliveira & Thierry Voet & Chris P. Pontin, 2020. "Identification of region-specific astrocyte subtypes at single cell resolution," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. Stuart Ibsen & Ada Tong & Carolyn Schutt & Sadik Esener & Sreekanth H. Chalasani, 2015. "Sonogenetics is a non-invasive approach to activating neurons in Caenorhabditis elegans," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    3. David P. Corey & Jaime García-Añoveros & Jeffrey R. Holt & Kelvin Y. Kwan & Shuh-Yow Lin & Melissa A. Vollrath & Andrea Amalfitano & Eunice L.-M. Cheung & Bruce H. Derfler & Anne Duggan & Gwénaëlle S., 2004. "TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells," Nature, Nature, vol. 432(7018), pages 723-730, December.
    4. Jianhua Zhao & John V. Lin King & Candice E. Paulsen & Yifan Cheng & David Julius, 2020. "Irritant-evoked activation and calcium modulation of the TRPA1 receptor," Nature, Nature, vol. 585(7823), pages 141-145, September.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Joseph Rufo & Peiran Zhang & Ruoyu Zhong & Luke P. Lee & Tony Jun Huang, 2022. "A sound approach to advancing healthcare systems: the future of biomedical acoustics," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    2. Pei Liu & Josquin Foiret & Yinglin Situ & Nisi Zhang & Aris J. Kare & Bo Wu & Marina N. Raie & Katherine W. Ferrara & Lei S. Qi, 2023. "Sonogenetic control of multiplexed genome regulation and base editing," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

    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. Samuel S. Kim & Buu Truong & Karthik Jagadeesh & Kushal K. Dey & Amber Z. Shen & Soumya Raychaudhuri & Manolis Kellis & Alkes L. Price, 2024. "Leveraging single-cell ATAC-seq and RNA-seq to identify disease-critical fetal and adult brain cell types," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Junjun Jing & Jifan Feng & Yuan Yuan & Tingwei Guo & Jie Lei & Fei Pei & Thach-Vu Ho & Yang Chai, 2022. "Spatiotemporal single-cell regulatory atlas reveals neural crest lineage diversification and cellular function during tooth morphogenesis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Irene Serra & Julio Esparza & Laura Delgado & Cristina Martín-Monteagudo & Margalida Puigròs & Petar Podlesniy & Ramón Trullás & Marta Navarrete, 2022. "Ca2+-modulated photoactivatable imaging reveals neuron-astrocyte glutamatergic circuitries within the nucleus accumbens," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Hidenori Tabata & Megumi Sasaki & Masakazu Agetsuma & Hitomi Sano & Yuki Hirota & Michio Miyajima & Kanehiro Hayashi & Takao Honda & Masashi Nishikawa & Yutaka Inaguma & Hidenori Ito & Hirohide Takeba, 2022. "Erratic and blood vessel-guided migration of astrocyte progenitors in the cerebral cortex," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    5. Jingyang Qian & Jie Liao & Ziqi Liu & Ying Chi & Yin Fang & Yanrong Zheng & Xin Shao & Bingqi Liu & Yongjin Cui & Wenbo Guo & Yining Hu & Hudong Bao & Penghui Yang & Qian Chen & Mingxiao Li & Bing Zha, 2023. "Reconstruction of the cell pseudo-space from single-cell RNA sequencing data with scSpace," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Lavanya Moparthi & Viktor Sinica & Vamsi K. Moparthi & Mohamed Kreir & Thibaut Vignane & Milos R. Filipovic & Viktorie Vlachova & Peter M. Zygmunt, 2022. "The human TRPA1 intrinsic cold and heat sensitivity involves separate channel structures beyond the N-ARD domain," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Chengyu Yin & Boyu Liu & Zishan Dong & Sai Shi & Chenxing Peng & Yushuang Pan & Xiaochen Bi & Huimin Nie & Yunwen Zhang & Yan Tai & Qimiao Hu & Xuan Wang & Xiaomei Shao & Hailong An & Jianqiao Fang & , 2024. "CXCL5 activates CXCR2 in nociceptive sensory neurons to drive joint pain and inflammation in experimental gouty arthritis," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    8. Pei Liu & Josquin Foiret & Yinglin Situ & Nisi Zhang & Aris J. Kare & Bo Wu & Marina N. Raie & Katherine W. Ferrara & Lei S. Qi, 2023. "Sonogenetic control of multiplexed genome regulation and base editing," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    9. Ryota Nomura, 2013. "Listening to the Ensemble of Story-Telling Performance and Audience Reactions," Academic Journal of Interdisciplinary Studies, Richtmann Publishing Ltd, vol. 2, October.
    10. Enrica Boda & Martina Lorenzati & Roberta Parolisi & Brian Harding & Gianmarco Pallavicini & Luca Bonfanti & Amanda Moccia & Stephanie Bielas & Ferdinando Di Cunto & Annalisa Buffo, 2022. "Molecular and functional heterogeneity in dorsal and ventral oligodendrocyte progenitor cells of the mouse forebrain in response to DNA damage," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    11. Ravneet Jaura & Ssu-Yu Yeh & Kaitlin N. Montanera & Alyssa Ialongo & Zobia Anwar & Yiming Lu & Kavindu Puwakdandawa & Ho Sung Rhee, 2022. "Extended intergenic DNA contributes to neuron-specific expression of neighboring genes in the mammalian nervous system," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    12. Jongdae Won & Jinsung Kim & Hyeongseop Jeong & Jinhyeong Kim & Shasha Feng & Byeongseok Jeong & Misun Kwak & Juyeon Ko & Wonpil Im & Insuk So & Hyung Ho Lee, 2023. "Molecular architecture of the Gαi-bound TRPC5 ion channel," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Juan F. Quintana & Praveena Chandrasegaran & Matthew C. Sinton & Emma M. Briggs & Thomas D. Otto & Rhiannon Heslop & Calum Bentley-Abbot & Colin Loney & Luis de Lecea & Neil A. Mabbott & Annette MacLe, 2022. "Single cell and spatial transcriptomic analyses reveal microglia-plasma cell crosstalk in the brain during Trypanosoma brucei infection," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    14. Tuo Ji & Lihua Zheng & Jiale Wu & Mei Duan & Qianwen Liu & Peng Liu & Chen Shen & Jinling Liu & Qinyi Ye & Jiangqi Wen & Jiangli Dong & Tao Wang, 2023. "The thioesterase APT1 is a bidirectional-adjustment redox sensor," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. A. Catalina Vélez-Ortega & Ruben Stepanyan & Stephanie E. Edelmann & Sara Torres-Gallego & Channy Park & Desislava A. Marinkova & Joshua S. Nowacki & Ghanshyam P. Sinha & Gregory I. Frolenkov, 2023. "TRPA1 activation in non-sensory supporting cells contributes to regulation of cochlear sensitivity after acoustic trauma," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    16. Avnika Bali & Samantha P. Schaefer & Isabelle Trier & Alice L. Zhang & Lilian Kabeche & Candice E. Paulsen, 2023. "Molecular mechanism of hyperactivation conferred by a truncation of TRPA1," Nature Communications, Nature, vol. 14(1), pages 1-15, 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:13:y:2022:i:1:d:10.1038_s41467-022-28205-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.