IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33803-x.html
   My bibliography  Save this article

Optineurin links Hace1-dependent Rac ubiquitylation to integrin-mediated mechanotransduction to control bacterial invasion and cell division

Author

Listed:
  • Serena Petracchini

    (Université Paris Cité, CNRS UMR6047, INSERM U1306, Unité des Toxines Bactériennes)

  • Daniel Hamaoui

    (Université Côte d’Azur, INSERM, C3M, Team Microbial Toxins in Host-Pathogen Interactions
    Equipe Labellisée Ligue Contre le Cancer)

  • Anne Doye

    (Université Côte d’Azur, INSERM, C3M, Team Microbial Toxins in Host-Pathogen Interactions
    Equipe Labellisée Ligue Contre le Cancer)

  • Atef Asnacios

    (Université Paris Cité, CNRS, Laboratoire Matière et Systèmes Complexes, UMR7057)

  • Florian Fage

    (Université Paris Cité, CNRS, Laboratoire Matière et Systèmes Complexes, UMR7057)

  • Elisa Vitiello

    (Université Grenoble Alpes, CNRS, LiPhy)

  • Martial Balland

    (Université Grenoble Alpes, CNRS, LiPhy)

  • Sebastien Janel

    (Université de Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR9017, CIIL—Center for Infection and Immunity of Lille)

  • Frank Lafont

    (Université de Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR9017, CIIL—Center for Infection and Immunity of Lille)

  • Mukund Gupta

    (Université Paris Cité, CNRS, Institut Jacques Monod)

  • Benoit Ladoux

    (Université Paris Cité, CNRS, Institut Jacques Monod)

  • Jerôme Gilleron

    (Université Côte d’Azur, INSERM, C3M, Team Cellular and Molecular Pathophysiology of Obesity and Diabetes)

  • Teresa M. Maia

    (VIB-UGent Center for Medical Biotechnology, VIB
    Ghent University
    VIB Proteomics Core, VIB)

  • Francis Impens

    (VIB-UGent Center for Medical Biotechnology, VIB
    Ghent University
    VIB Proteomics Core, VIB)

  • Laurent Gagnoux-Palacios

    (Université Côte d’Azur, CNRS, INSERM, Institut de Biologie Valrose (iBV))

  • Mads Daugaard

    (Vancouver Prostate Centre
    Department of Urologic Sciences, University of British Columbia)

  • Poul H. Sorensen

    (University of British Columbia)

  • Emmanuel Lemichez

    (Université Paris Cité, CNRS UMR6047, INSERM U1306, Unité des Toxines Bactériennes
    Université Côte d’Azur, INSERM, C3M, Team Microbial Toxins in Host-Pathogen Interactions
    Equipe Labellisée Ligue Contre le Cancer)

  • Amel Mettouchi

    (Université Paris Cité, CNRS UMR6047, INSERM U1306, Unité des Toxines Bactériennes
    Université Côte d’Azur, INSERM, C3M, Team Microbial Toxins in Host-Pathogen Interactions
    Equipe Labellisée Ligue Contre le Cancer)

Abstract

Extracellular matrix (ECM) elasticity is perceived by cells via focal adhesion structures, which transduce mechanical cues into chemical signalling to conform cell behavior. Although the contribution of ECM compliance to the control of cell migration or division is extensively studied, little is reported regarding infectious processes. We study this phenomenon with the extraintestinal Escherichia coli pathogen UTI89. We show that UTI89 takes advantage, via its CNF1 toxin, of integrin mechanoactivation to trigger its invasion into cells. We identify the HACE1 E3 ligase-interacting protein Optineurin (OPTN) as a protein regulated by ECM stiffness. Functional analysis establishes a role of OPTN in bacterial invasion and integrin mechanical coupling and for stimulation of HACE1 E3 ligase activity towards the Rac1 GTPase. Consistent with a role of OPTN in cell mechanics, OPTN knockdown cells display defective integrin-mediated traction force buildup, associated with limited cellular invasion by UTI89. Nevertheless, OPTN knockdown cells display strong mechanochemical adhesion signalling, enhanced Rac1 activation and increased cyclin D1 translation, together with enhanced cell proliferation independent of ECM stiffness. Together, our data ascribe a new function to OPTN in mechanobiology.

Suggested Citation

  • Serena Petracchini & Daniel Hamaoui & Anne Doye & Atef Asnacios & Florian Fage & Elisa Vitiello & Martial Balland & Sebastien Janel & Frank Lafont & Mukund Gupta & Benoit Ladoux & Jerôme Gilleron & Te, 2022. "Optineurin links Hace1-dependent Rac ubiquitylation to integrin-mediated mechanotransduction to control bacterial invasion and cell division," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33803-x
    DOI: 10.1038/s41467-022-33803-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33803-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-33803-x?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. A. J. Ehrlicher & F. Nakamura & J. H. Hartwig & D. A. Weitz & T. P. Stossel, 2011. "Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A," Nature, Nature, vol. 478(7368), pages 260-263, October.
    2. Maximilian M. Sauer & Roman P. Jakob & Jonathan Eras & Sefer Baday & Deniz Eriş & Giulio Navarra & Simon Bernèche & Beat Ernst & Timm Maier & Rudi Glockshuber, 2016. "Catch-bond mechanism of the bacterial adhesin FimH," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
    3. Sandrine Etienne-Manneville & Alan Hall, 2002. "Rho GTPases in cell biology," Nature, Nature, vol. 420(6916), pages 629-635, December.
    4. Gilles Flatau & Emmanuel Lemichez & Michel Gauthier & Pierre Chardin & Sonia Paris & Carla Fiorentini & Patrice Boquet, 1997. "Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine," Nature, Nature, vol. 387(6634), pages 729-733, June.
    5. Caitlin N. Spaulding & Roger D. Klein & Ségolène Ruer & Andrew L. Kau & Henry L. Schreiber & Zachary T. Cusumano & Karen W. Dodson & Jerome S. Pinkner & Daved H. Fremont & James W. Janetka & Han Remau, 2017. "Selective depletion of uropathogenic E. coli from the gut by a FimH antagonist," Nature, Nature, vol. 546(7659), pages 528-532, June.
    6. Zhucheng Chen & Dominika Borek & Shae B. Padrick & Timothy S. Gomez & Zoltan Metlagel & Ayman M. Ismail & Junko Umetani & Daniel D. Billadeau & Zbyszek Otwinowski & Michael K. Rosen, 2010. "Structure and control of the actin regulatory WAVE complex," Nature, Nature, vol. 468(7323), pages 533-538, November.
    7. Kalpana Mandal & Irène Wang & Elisa Vitiello & Laura Andreina Chacòn Orellana & Martial Balland, 2014. "Cell dipole behaviour revealed by ECM sub-cellular geometry," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    8. Matthew J. Paszek & Christopher C. DuFort & Olivier Rossier & Russell Bainer & Janna K. Mouw & Kamil Godula & Jason E. Hudak & Jonathon N. Lakins & Amanda C. Wijekoon & Luke Cassereau & Matthew G. Rub, 2014. "The cancer glycocalyx mechanically primes integrin-mediated growth and survival," Nature, Nature, vol. 511(7509), pages 319-325, July.
    9. Carsten Grashoff & Brenton D. Hoffman & Michael D. Brenner & Ruobo Zhou & Maddy Parsons & Michael T. Yang & Mark A. McLean & Stephen G. Sligar & Christopher S. Chen & Taekjip Ha & Martin A. Schwartz, 2010. "Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics," Nature, Nature, vol. 466(7303), pages 263-266, July.
    10. Mads Daugaard & Roberto Nitsch & Babak Razaghi & Lindsay McDonald & Ameer Jarrar & Stéphanie Torrino & Sonia Castillo-Lluva & Barak Rotblat & Liheng Li & Angeliki Malliri & Emmanuel Lemichez & Amel Me, 2013. "Hace1 controls ROS generation of vertebrate Rac1-dependent NADPH oxidase complexes," Nature Communications, Nature, vol. 4(1), pages 1-13, October.
    11. A. Marijke Keestra & Maria G. Winter & Josef J. Auburger & Simon P. Fräßle & Mariana N. Xavier & Sebastian E. Winter & Anita Kim & Victor Poon & Mariëtta M. Ravesloot & Julian F. T. Waldenmaier & René, 2013. "Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1," Nature, Nature, vol. 496(7444), pages 233-237, April.
    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. Yuting Feng & Shuyi Wang & Xiaoye Liu & Yiming Han & Hongwei Xu & Xiaocen Duan & Wenyue Xie & Zhuoling Tian & Zuoying Yuan & Zhuo Wan & Liang Xu & Siying Qin & Kangmin He & Jianyong Huang, 2023. "Geometric constraint-triggered collagen expression mediates bacterial-host adhesion," Nature Communications, Nature, vol. 14(1), pages 1-13, 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. Matthew R. Pawlak & Adam T. Smiley & Maria Paz Ramirez & Marcus D. Kelly & Ghaidan A. Shamsan & Sarah M. Anderson & Branden A. Smeester & David A. Largaespada & David J. Odde & Wendy R. Gordon, 2023. "RAD-TGTs: high-throughput measurement of cellular mechanotype via rupture and delivery of DNA tension probes," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Sorosh Amiri & Camelia Muresan & Xingbo Shang & Clotilde Huet-Calderwood & Martin A. Schwartz & David A. Calderwood & Michael Murrell, 2023. "Intracellular tension sensor reveals mechanical anisotropy of the actin cytoskeleton," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Paul A Roberts & Ryan M Huebinger & Emma Keen & Anne-Marie Krachler & Sara Jabbari, 2018. "Predictive modelling of a novel anti-adhesion therapy to combat bacterial colonisation of burn wounds," PLOS Computational Biology, Public Library of Science, vol. 14(5), pages 1-28, May.
    4. Jocelyn E. Chau & Kimberly J. Vish & Titus J. Boggon & Amy L. Stiegler, 2022. "SH3 domain regulation of RhoGAP activity: Crosstalk between p120RasGAP and DLC1 RhoGAP," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Jiankai Wei & Wei Zhang & An Jiang & Hongzhe Peng & Quanyong Zhang & Yuting Li & Jianqing Bi & Linting Wang & Penghui Liu & Jing Wang & Yonghang Ge & Liya Zhang & Haiyan Yu & Lei Li & Shi Wang & Liang, 2024. "Temporospatial hierarchy and allele-specific expression of zygotic genome activation revealed by distant interspecific urochordate hybrids," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    6. Xiaoyi Cheng & Radwa Barakat & Giulia Pavani & Masuma Khatun Usha & Rodolfo Calderon & Elizabeth Snella & Abigail Gorden & Yudi Zhang & Paul Gadue & Deborah L. French & Karin S. Dorman & Antonella Fid, 2023. "Nod1-dependent NF-kB activation initiates hematopoietic stem cell specification in response to small Rho GTPases," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    7. Navish Wadhwa & Alberto Sassi & Howard C. Berg & Yuhai Tu, 2022. "A multi-state dynamic process confers mechano-adaptation to a biological nanomachine," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    8. April Schweinhart & Janine Austin Clayton, 2018. "Reversing the Trends toward Shorter Lives and Poorer Health for U.S. Women: A Call for Innovative Interdisciplinary Research," IJERPH, MDPI, vol. 15(9), pages 1-14, August.
    9. Limei Wu & Srinivas Chatla & Qiqi Lin & Fabliha Ahmed Chowdhury & Werner Geldenhuys & Wei Du, 2021. "Quinacrine-CASIN combination overcomes chemoresistance in human acute lymphoid leukemia," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    10. Gabriela Casanova-Sepúlveda & Joel A. Sexton & Benjamin E. Turk & Titus J. Boggon, 2023. "Autoregulation of the LIM kinases by their PDZ domain," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    11. Cummings, F.W, 2004. "A model of morphogenesis," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 339(3), pages 531-547.
    12. Steffen Nørgaard & Shuer Deng & Wei Cao & Roger Pocock, 2018. "Distinct CED-10/Rac1 domains confer context-specific functions in development," PLOS Genetics, Public Library of Science, vol. 14(9), pages 1-24, September.
    13. Huilong Luo & Yanmei Chen & Xiao Kuang & Xinyue Wang & Fengmin Yang & Zhenping Cao & Lu Wang & Sisi Lin & Feng Wu & Jinyao Liu, 2022. "Chemical reaction-mediated covalent localization of bacteria," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    14. Yanan Wang & Giovanni Chiappetta & Raphaël Guérois & Yijun Liu & Stéphane Romero & Daniel J. Boesch & Matthias Krause & Claire A. Dessalles & Avin Babataheri & Abdul I. Barakat & Baoyu Chen & Joelle V, 2023. "PPP2R1A regulates migration persistence through the NHSL1-containing WAVE Shell Complex," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    15. Zhaowei Liu & Haipei Liu & Andrés M. Vera & Byeongseon Yang & Philip Tinnefeld & Michael A. Nash, 2024. "Engineering an artificial catch bond using mechanical anisotropy," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    16. Rashmi Priya & Guillermo A Gomez & Srikanth Budnar & Bipul R Acharya & Andras Czirok & Alpha S Yap & Zoltan Neufeld, 2017. "Bistable front dynamics in a contractile medium: Travelling wave fronts and cortical advection define stable zones of RhoA signaling at epithelial adherens junctions," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-19, March.
    17. Yasuo Takashima & Atsushi Kawaguchi & Junya Fukai & Yasuo Iwadate & Koji Kajiwara & Hiroaki Hondoh & Ryuya Yamanaka, 2021. "Survival prediction based on the gene expression associated with cancer morphology and microenvironment in primary central nervous system lymphoma," PLOS ONE, Public Library of Science, vol. 16(6), pages 1-14, June.
    18. Yuhang Zhang & Jingyi Du & Xian Liu & Fei Shang & Yunxin Deng & Jiaqing Ye & Yukai Wang & Jie Yan & Hu Chen & Miao Yu & Shimin Le, 2024. "Multi-domain interaction mediated strength-building in human α-actinin dimers unveiled by direct single-molecule quantification," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    19. Juan Manuel Ortiz-Sanchez & Sara E Nichols & Jacqueline Sayyah & Joan Heller Brown & J Andrew McCammon & Barry J Grant, 2012. "Identification of Potential Small Molecule Binding Pockets on Rho Family GTPases," PLOS ONE, Public Library of Science, vol. 7(7), pages 1-13, July.
    20. Venkat R. Chirasani & Mohammad Ashhar I. Khan & Juilee N. Malavade & Nikolay V. Dokholyan & Brenton D. Hoffman & Sharon L. Campbell, 2023. "Molecular basis and cellular functions of vinculin-actin directional catch bonding," 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:13:y:2022:i:1:d:10.1038_s41467-022-33803-x. 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.