IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47306-4.html
   My bibliography  Save this article

An Intricate Network Involving the Argonaute ALG-1 Modulates Organismal Resistance to Oxidative Stress

Author

Listed:
  • Carlos A. Vergani-Junior

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

  • Raíssa De P. Moro

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

  • Silas Pinto

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

  • Evandro A. De-Souza

    (Universidade Estadual de Campinas)

  • Henrique Camara

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas
    Joslin Diabetes Center)

  • Deisi L. Braga

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

  • Guilherme Tonon-da-Silva

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

  • Thiago L. Knittel

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

  • Gabriel P. Ruiz

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

  • Raissa G. Ludwig

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

  • Katlin B. Massirer

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

  • William B. Mair

    (Harvard University)

  • Marcelo A. Mori

    (Universidade Estadual de Campinas
    Universidade Estadual de Campinas
    Universidade Estadual de Campinas
    Universidade Estadual de Campinas)

Abstract

Cellular response to redox imbalance is crucial for organismal health. microRNAs are implicated in stress responses. ALG-1, the C. elegans ortholog of human AGO2, plays an essential role in microRNA processing and function. Here we investigated the mechanisms governing ALG-1 expression in C. elegans and the players controlling lifespan and stress resistance downstream of ALG-1. We show that upregulation of ALG-1 is a shared feature in conditions linked to increased longevity (e.g., germline-deficient glp-1 mutants). ALG-1 knockdown reduces lifespan and oxidative stress resistance, while overexpression enhances survival against pro-oxidant agents but not heat or reductive stress. R02D3.7 represses alg-1 expression, impacting oxidative stress resistance at least in part via ALG-1. microRNAs upregulated in glp-1 mutants (miR-87-3p, miR-230-3p, and miR-235-3p) can target genes in the protein disulfide isomerase pathway and protect against oxidative stress. This study unveils a tightly regulated network involving transcription factors and microRNAs which controls organisms’ ability to withstand oxidative stress.

Suggested Citation

  • Carlos A. Vergani-Junior & Raíssa De P. Moro & Silas Pinto & Evandro A. De-Souza & Henrique Camara & Deisi L. Braga & Guilherme Tonon-da-Silva & Thiago L. Knittel & Gabriel P. Ruiz & Raissa G. Ludwig , 2024. "An Intricate Network Involving the Argonaute ALG-1 Modulates Organismal Resistance to Oxidative Stress," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47306-4
    DOI: 10.1038/s41467-024-47306-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47306-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-47306-4?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. Cynthia J. Kenyon, 2010. "The genetics of ageing," Nature, Nature, vol. 464(7288), pages 504-512, March.
    2. Cynthia J. Kenyon, 2010. "Erratum: The genetics of ageing," Nature, Nature, vol. 467(7315), pages 622-622, September.
    3. Honor Hsin & Cynthia Kenyon, 1999. "Signals from the reproductive system regulate the lifespan of C. elegans," Nature, Nature, vol. 399(6734), pages 362-366, May.
    4. Davor Lessel & Daniela M. Zeitler & Margot R. F. Reijnders & Andriy Kazantsev & Fatemeh Hassani Nia & Alexander Bartholomäus & Victoria Martens & Astrid Bruckmann & Veronika Graus & Allyn McConkie-Ros, 2020. "Germline AGO2 mutations impair RNA interference and human neurological development," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    5. Calvin H. Jan & Robin C. Friedman & J. Graham Ruby & David P. Bartel, 2011. "Formation, regulation and evolution of Caenorhabditis elegans 3′UTRs," Nature, Nature, vol. 469(7328), pages 97-101, January.
    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. Xueqing Wang & Quanlong Jiang & Hongdao Zhang & Zhidong He & Yuanyuan Song & Yifan Chen & Na Tang & Yifei Zhou & Yiping Li & Adam Antebi & Ligang Wu & Jing-Dong J. Han & Yidong Shen, 2024. "Tissue-specific profiling of age-dependent miRNAomic changes in Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Yan-Ping Zhang & Wen-Hong Zhang & Pan Zhang & Qi Li & Yue Sun & Jia-Wen Wang & Shaobing O. Zhang & Tao Cai & Cheng Zhan & Meng-Qiu Dong, 2022. "Intestine-specific removal of DAF-2 nearly doubles lifespan in Caenorhabditis elegans with little fitness cost," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Eirini Lionaki & Ilias Gkikas & Ioanna Daskalaki & Maria-Konstantina Ioannidi & Maria I. Klapa & Nektarios Tavernarakis, 2022. "Mitochondrial protein import determines lifespan through metabolic reprogramming and de novo serine biosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Qucheng Deng & Yongping Wei & Lijuan Chen & Wei Liang & Jijun Du & Yuling Tan & Yinjun Zhao, 2019. "Relationship between Air Pollution and Regional Longevity in Guangxi, China," IJERPH, MDPI, vol. 16(19), pages 1-12, October.
    5. Jin-Hyuck Jeong & Jun-Seok Han & Youngae Jung & Seung-Min Lee & So-Hyun Park & Mooncheol Park & Min-Gi Shin & Nami Kim & Mi Sun Kang & Seokho Kim & Kwang-Pyo Lee & Ki-Sun Kwon & Chun-A. Kim & Yong Ryo, 2023. "A new AMPK isoform mediates glucose-restriction induced longevity non-cell autonomously by promoting membrane fluidity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Cyril Statzer & Jin Meng & Richard Venz & Monet Bland & Stacey Robida-Stubbs & Krina Patel & Dunja Petrovic & Raffaella Emsley & Pengpeng Liu & Ianessa Morantte & Cole Haynes & William B. Mair & Alban, 2022. "ATF-4 and hydrogen sulfide signalling mediate longevity in response to inhibition of translation or mTORC1," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Harper S. Kim & Danitra J. Parker & Madison M. Hardiman & Erin Munkácsy & Nisi Jiang & Aric N. Rogers & Yidong Bai & Colin Brent & James A. Mobley & Steven N. Austad & Andrew M. Pickering, 2023. "Early-adulthood spike in protein translation drives aging via juvenile hormone/germline signaling," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Caroline Beaudoin-Chabot & Lei Wang & Cenk Celik & Aishah Tul-Firdaus Abdul Khalid & Subhash Thalappilly & Shiyi Xu & Jhee Hong Koh & Venus Wen Xuan Lim & Ann Don Low & Guillaume Thibault, 2022. "The unfolded protein response reverses the effects of glucose on lifespan in chemically-sterilized C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    9. Edouard Debonneuil & Anne Eyraud-Loisel & Frédéric Planchet, 2018. "Can Pension Funds Partially Manage Longevity Risk by Investing in a Longevity Megafund?," Risks, MDPI, vol. 6(3), pages 1-27, July.
    10. Nan Wu & Yi-Cheng Ma & Xin-Qian Gong & Pei-Ji Zhao & Yong-Jian Jia & Qiu Zhao & Jia-Hong Duan & Cheng-Gang Zou, 2023. "The metabolite alpha-ketobutyrate extends lifespan by promoting peroxisomal function in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    11. Qucheng Deng & Lijuan Chen & Yongping Wei & Yonghua Li & Xuerong Han & Wei Liang & Yinjun Zhao & Xiaofei Wang & Juan Yin, 2018. "Understanding the Association between Environmental Factors and Longevity in Hechi, China: A Drinking Water and Soil Quality Perspective," IJERPH, MDPI, vol. 15(10), pages 1-17, October.
    12. Arles Urrutia & Víctor A García-Angulo & Andrés Fuentes & Mauricio Caneo & Marcela Legüe & Sebastián Urquiza & Scarlett E Delgado & Juan Ugalde & Paula Burdisso & Andrea Calixto, 2020. "Bacterially produced metabolites protect C. elegans neurons from degeneration," PLOS Biology, Public Library of Science, vol. 18(3), pages 1-31, March.
    13. Smith, Ken R. & Hanson, Heidi A. & Norton, Maria C. & Hollingshaus, Michael S. & Mineau, Geraldine P., 2014. "Survival of offspring who experience early parental death: Early life conditions and later-life mortality," Social Science & Medicine, Elsevier, vol. 119(C), pages 180-190.
    14. Daniele Campa & Francesco De Rango & Maura Carrai & Paolina Crocco & Alberto Montesanto & Federico Canzian & Giuseppina Rose & Cosmeri Rizzato & Giuseppe Passarino & Roberto Barale, 2012. "Bitter Taste Receptor Polymorphisms and Human Aging," PLOS ONE, Public Library of Science, vol. 7(11), pages 1-8, November.
    15. Seungjae Lee & Yen-Chung Chen & Austin E. Gillen & J. Matthew Taliaferro & Bart Deplancke & Hongjie Li & Eric C. Lai, 2022. "Diverse cell-specific patterns of alternative polyadenylation in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    16. Denisa Margină & Anca Ungurianu & Carmen Purdel & Dimitris Tsoukalas & Evangelia Sarandi & Maria Thanasoula & Fotios Tekos & Robin Mesnage & Demetrios Kouretas & Aristidis Tsatsakis, 2020. "Chronic Inflammation in the Context of Everyday Life: Dietary Changes as Mitigating Factors," IJERPH, MDPI, vol. 17(11), pages 1-27, June.
    17. Aditya Kshirsagar & Svetlana Maslov Doroshev & Anna Gorelik & Tsviya Olender & Tamar Sapir & Daisuke Tsuboi & Irit Rosenhek-Goldian & Sergey Malitsky & Maxim Itkin & Amir Argoetti & Yael Mandel-Gutfre, 2023. "LIS1 RNA-binding orchestrates the mechanosensitive properties of embryonic stem cells in AGO2-dependent and independent ways," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    18. Ádám Sturm & Éva Saskői & Bernadette Hotzi & Anna Tarnóci & János Barna & Ferenc Bodnár & Himani Sharma & Tibor Kovács & Eszter Ari & Nóra Weinhardt & Csaba Kerepesi & András Perczel & Zoltán Ivics & , 2023. "Downregulation of transposable elements extends lifespan in Caenorhabditis elegans," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    19. Debbie McLaggan & Maria R Amezaga & Eleni Petra & Andrew Frost & Elizabeth I Duff & Stewart M Rhind & Paul A Fowler & L Anne Glover & Cristina Lagido, 2012. "Impact of Sublethal Levels of Environmental Pollutants Found in Sewage Sludge on a Novel Caenorhabditis elegans Model Biosensor," PLOS ONE, Public Library of Science, vol. 7(10), pages 1-12, October.
    20. Zi Wang & Lina Zou & Yiyan Zhang & Mengnan Zhu & Shuxian Zhang & Di Wu & Jianfeng Lan & Xiao Zang & Qi Wang & Hanxin Zhang & Zixing Wu & Huanhu Zhu & Di Chen, 2023. "ACS-20/FATP4 mediates the anti-ageing effect of dietary restriction in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-13, 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_s41467-024-47306-4. 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.