IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34761-0.html
   My bibliography  Save this article

Dual roles and evolutionary implications of P26/poxin in antagonizing intracellular cGAS-STING and extracellular melanization immunity

Author

Listed:
  • Mengyi Yin

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Wenhua Kuang

    (Chinese Academy of Sciences)

  • Qianran Wang

    (Chinese Academy of Sciences)

  • Xi Wang

    (Chinese Academy of Sciences)

  • Chuanfei Yuan

    (Chinese Academy of Sciences)

  • Zhe Lin

    (Chinese Academy of Sciences)

  • Huanyu Zhang

    (Chinese Academy of Sciences)

  • Fei Deng

    (Chinese Academy of Sciences)

  • Haobo Jiang

    (Oklahoma State University)

  • Peng Gong

    (Chinese Academy of Sciences)

  • Zhen Zou

    (University of Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Zhihong Hu

    (Chinese Academy of Sciences)

  • Manli Wang

    (Chinese Academy of Sciences)

Abstract

P26, a homolog of the viral-encoded nuclease poxin that neutralizes the cGAS-STING innate immunity, is widely distributed in various invertebrate viruses, lepidopteran insects, and parasitoid wasps. P26/poxin from certain insect viruses also retains protease activity, though its biological role remains unknown. Given that many P26s contain a signal peptide, it is surmised that P26 may possess certain extracellular functions. Here, we report that a secretory baculoviral P26 suppresses melanization, a prominent insect innate immunity against pathogen invasion. P26 targets the cofactor of a prophenoloxidase-activating protease, and its inhibitory function is independent of nuclease activity. The analysis of P26/poxin homologs from different origins suggests that the ability to inhibit the extracellular melanization pathway is limited to P26s with a signal peptide and not shared by the homologs without it. These findings highlight the independent evolution of a single viral suppressor to perform dual roles in modulating immunity during virus-host adaptation.

Suggested Citation

  • Mengyi Yin & Wenhua Kuang & Qianran Wang & Xi Wang & Chuanfei Yuan & Zhe Lin & Huanyu Zhang & Fei Deng & Haobo Jiang & Peng Gong & Zhen Zou & Zhihong Hu & Manli Wang, 2022. "Dual roles and evolutionary implications of P26/poxin in antagonizing intracellular cGAS-STING and extracellular melanization immunity," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34761-0
    DOI: 10.1038/s41467-022-34761-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34761-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-34761-0?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. Björn Schwanhäusser & Dorothea Busse & Na Li & Gunnar Dittmar & Johannes Schuchhardt & Jana Wolf & Wei Chen & Matthias Selbach, 2011. "Global quantification of mammalian gene expression control," Nature, Nature, vol. 473(7347), pages 337-342, May.
    2. James B. Eaglesham & Youdong Pan & Thomas S. Kupper & Philip J. Kranzusch, 2019. "Publisher Correction: Viral and metazoan poxins are cGAMP-specific nucleases that restrict cGAS–STING signalling," Nature, Nature, vol. 569(7758), pages 12-12, May.
    3. James B. Eaglesham & Youdong Pan & Thomas S. Kupper & Philip J. Kranzusch, 2019. "Viral and metazoan poxins are cGAMP-specific nucleases that restrict cGAS–STING signalling," Nature, Nature, vol. 566(7743), pages 259-263, February.
    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. Nathan Meade & Helen K. Toreev & Ram P. Chakrabarty & Charles R. Hesser & Chorong Park & Navdeep S. Chandel & Derek Walsh, 2023. "The poxvirus F17 protein counteracts mitochondrially orchestrated antiviral responses," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Angel Rivera-Calzada & Raquel Arribas-Bosacoma & Alba Ruiz-Ramos & Paloma Escudero-Bravo & Jasminka Boskovic & Rafael Fernandez-Leiro & Antony W. Oliver & Laurence H. Pearl & Oscar Llorca, 2022. "Structural basis for the inactivation of cytosolic DNA sensing by the vaccinia virus," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Ning Yang & Yi Wang & Peihong Dai & Tuo Li & Christian Zierhut & Adrian Tan & Tuo Zhang & Jenny Zhaoying Xiang & Alban Ordureau & Hironori Funabiki & Zhijian Chen & Liang Deng, 2023. "Vaccinia E5 is a major inhibitor of the DNA sensor cGAS," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Ji Min Lee & Henrik M. Hammarén & Mikhail M. Savitski & Sung Hee Baek, 2023. "Control of protein stability by post-translational modifications," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Mohammad Soltani & Cesar A Vargas-Garcia & Duarte Antunes & Abhyudai Singh, 2016. "Intercellular Variability in Protein Levels from Stochastic Expression and Noisy Cell Cycle Processes," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-23, August.
    6. Jasjot Singh & Hadeer Elhabashy & Pathma Muthukottiappan & Markus Stepath & Martin Eisenacher & Oliver Kohlbacher & Volkmar Gieselmann & Dominic Winter, 2022. "Cross-linking of the endolysosomal system reveals potential flotillin structures and cargo," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Yuping Chen & Jo-Hsi Huang & Connie Phong & James E. Ferrell, 2024. "Viscosity-dependent control of protein synthesis and degradation," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    8. Gábor Csárdi & Alexander Franks & David S Choi & Edoardo M Airoldi & D Allan Drummond, 2015. "Accounting for Experimental Noise Reveals That mRNA Levels, Amplified by Post-Transcriptional Processes, Largely Determine Steady-State Protein Levels in Yeast," PLOS Genetics, Public Library of Science, vol. 11(5), pages 1-32, May.
    9. Yan Li & Chen Xu & Bing Wang & Fujiang Xu & Fahan Ma & Yuanyuan Qu & Dongxian Jiang & Kai Li & Jinwen Feng & Sha Tian & Xiaohui Wu & Yunzhi Wang & Yang Liu & Zhaoyu Qin & Yalan Liu & Jing Qin & Qi Son, 2022. "Proteomic characterization of gastric cancer response to chemotherapy and targeted therapy reveals potential therapeutic strategies," Nature Communications, Nature, vol. 13(1), pages 1-26, December.
    10. Kaslik, Eva & Rădulescu, Ileana Rodica, 2022. "Stability and bifurcations in fractional-order gene regulatory networks," Applied Mathematics and Computation, Elsevier, vol. 421(C).
    11. Suran Kim & Sungjin Min & Yi Sun Choi & Sung-Hyun Jo & Jae Hun Jung & Kyusun Han & Jin Kim & Soohwan An & Yong Woo Ji & Yun-Gon Kim & Seung-Woo Cho, 2022. "Tissue extracellular matrix hydrogels as alternatives to Matrigel for culturing gastrointestinal organoids," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    12. Jingbo Qie & Yang Liu & Yunzhi Wang & Fan Zhang & Zhaoyu Qin & Sha Tian & Mingwei Liu & Kai Li & Wenhao Shi & Lei Song & Mingjun Sun & Yexin Tong & Ping Hu & Tao Gong & Xiaqiong Wang & Yi Huang & Bolo, 2022. "Integrated proteomic and transcriptomic landscape of macrophages in mouse tissues," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    13. Lingling Li & Dongxian Jiang & Qiao Zhang & Hui Liu & Fujiang Xu & Chunmei Guo & Zhaoyu Qin & Haixing Wang & Jinwen Feng & Yang Liu & Weijie Chen & Xue Zhang & Lin Bai & Sha Tian & Subei Tan & Chen Xu, 2023. "Integrative proteogenomic characterization of early esophageal cancer," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    14. Thomas C. J. Tan & Van Kelly & Xiaoyan Zou & David Wright & Tony Ly & Rose Zamoyska, 2022. "Translation factor eIF5a is essential for IFNγ production and cell cycle regulation in primary CD8+ T lymphocytes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. Katharina Clemm von Hohenberg & Sandra Müller & Sibylle Schleich & Matthias Meister & Jonathan Bohlen & Thomas G. Hofmann & Aurelio A. Teleman, 2022. "Cyclin B/CDK1 and Cyclin A/CDK2 phosphorylate DENR to promote mitotic protein translation and faithful cell division," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    16. Jonathan J. Swietlik & Stefanie Bärthel & Chiara Falcomatà & Diana Fink & Ankit Sinha & Jingyuan Cheng & Stefan Ebner & Peter Landgraf & Daniela C. Dieterich & Henrik Daub & Dieter Saur & Felix Meissn, 2023. "Cell-selective proteomics segregates pancreatic cancer subtypes by extracellular proteins in tumors and circulation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    17. Ryosuke Ishimura & Afnan H. El-Gowily & Daisuke Noshiro & Satoko Komatsu-Hirota & Yasuko Ono & Mayumi Shindo & Tomohisa Hatta & Manabu Abe & Takefumi Uemura & Hyeon-Cheol Lee-Okada & Tarek M. Mohamed , 2022. "The UFM1 system regulates ER-phagy through the ufmylation of CYB5R3," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. Sajib Chakraborty & Hossain Uddin Shekhar, 2017. "Applications of Mass-Spectrometry Based Quantitative Proteomics to Understand Complex Cellular Functions and Cell Fate Decisions," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 1(1), pages 169-171, June.
    19. Marvin Hering & Alaa Madi & Roger Sandhoff & Sicong Ma & Jingxia Wu & Alessa Mieg & Karsten Richter & Kerstin Mohr & Nora Knabe & Diana Stichling & Gernot Poschet & Felix Bestvater & Larissa Frank & J, 2024. "Sphinganine recruits TLR4 adaptors in macrophages and promotes inflammation in murine models of sepsis and melanoma," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    20. Sébastien Durand & Marion Bruelle & Fleur Bourdelais & Bigitha Bennychen & Juliana Blin-Gonthier & Caroline Isaac & Aurélia Huyghe & Sylvie Martel & Antoine Seyve & Christophe Vanbelle & Annie Adrait , 2023. "RSL24D1 sustains steady-state ribosome biogenesis and pluripotency translational programs in embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-17, 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_s41467-022-34761-0. 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.