IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0241122.html
   My bibliography  Save this article

Dichloroacetate-induced metabolic reprogramming improves lifespan in a Drosophila model of surviving sepsis

Author

Listed:
  • Veli Bakalov
  • Laura Reyes-Uribe
  • Rahul Deshpande
  • Abigail L Maloy
  • Steven D Shapiro
  • Derek C Angus
  • Chung-Chou H Chang
  • Laurence Le Moyec
  • Stacy Gelhaus Wendell
  • Ata Murat Kaynar

Abstract

Sepsis is the leading cause of death in hospitalized patients and beyond the hospital stay and these long-term sequelae are due in part to unresolved inflammation. Metabolic shift from oxidative phosphorylation to aerobic glycolysis links metabolism to inflammation and such a shift is commonly observed in sepsis under normoxic conditions. By shifting the metabolic state from aerobic glycolysis to oxidative phosphorylation, we hypothesized it would reverse unresolved inflammation and subsequently improve outcome. We propose a shift from aerobic glycolysis to oxidative phosphorylation as a sepsis therapy by targeting the pathways involved in the conversion of pyruvate into acetyl-CoA via pyruvate dehydrogenase (PDH). Chemical manipulation of PDH using dichloroacetic acid (DCA) will promote oxidative phosphorylation over glycolysis and decrease inflammation. We tested our hypothesis in a Drosophila melanogaster model of surviving sepsis infected with Staphylococcus aureus. Drosophila were divided into 3 groups: unmanipulated, sham and sepsis survivors, all treated with linezolid; each group was either treated or not with DCA for one week following sepsis. We followed lifespan, measured gene expression of Toll, defensin, cecropin A, and drosomycin, and levels of lactate, pyruvate, acetyl-CoA as well as TCA metabolites. In our model, metabolic effects of sepsis are modified by DCA with normalized lactate, TCA metabolites, and was associated with improved lifespan of sepsis survivors, yet had no lifespan effects on unmanipulated and sham flies. While Drosomycin and cecropin A expression increased in sepsis survivors, DCA treatment decreased both and selectively increased defensin.

Suggested Citation

  • Veli Bakalov & Laura Reyes-Uribe & Rahul Deshpande & Abigail L Maloy & Steven D Shapiro & Derek C Angus & Chung-Chou H Chang & Laurence Le Moyec & Stacy Gelhaus Wendell & Ata Murat Kaynar, 2020. "Dichloroacetate-induced metabolic reprogramming improves lifespan in a Drosophila model of surviving sepsis," PLOS ONE, Public Library of Science, vol. 15(11), pages 1-18, November.
  • Handle: RePEc:plo:pone00:0241122
    DOI: 10.1371/journal.pone.0241122
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0241122
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0241122&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0241122?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. Kazuhiko Yamane & Irene L Indalao & Junji Chida & Yoshikazu Yamamoto & Masaaki Hanawa & Hiroshi Kido, 2014. "Diisopropylamine Dichloroacetate, a Novel Pyruvate Dehydrogenase Kinase 4 Inhibitor, as a Potential Therapeutic Agent for Metabolic Disorders and Multiorgan Failure in Severe Influenza," PLOS ONE, Public Library of Science, vol. 9(5), pages 1-13, May.
    2. Oscar R. Colegio & Ngoc-Quynh Chu & Alison L. Szabo & Thach Chu & Anne Marie Rhebergen & Vikram Jairam & Nika Cyrus & Carolyn E. Brokowski & Stephanie C. Eisenbarth & Gillian M. Phillips & Gary W. Cli, 2014. "Functional polarization of tumour-associated macrophages by tumour-derived lactic acid," Nature, Nature, vol. 513(7519), pages 559-563, September.
    3. Liangchun Yang & Min Xie & Minghua Yang & Yan Yu & Shan Zhu & Wen Hou & Rui Kang & Michael T. Lotze & Timothy R. Billiar & Haichao Wang & Lizhi Cao & Daolin Tang, 2014. "PKM2 regulates the Warburg effect and promotes HMGB1 release in sepsis," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
    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. Tianshi Feng & Xuemei Zhao & Ping Gu & Wah Yang & Cunchuan Wang & Qingyu Guo & Qiaoyun Long & Qing Liu & Ying Cheng & Jin Li & Cynthia Kwan Yui Cheung & Donghai Wu & Xinyu Kong & Yong Xu & Dewei Ye & , 2022. "Adipocyte-derived lactate is a signalling metabolite that potentiates adipose macrophage inflammation via targeting PHD2," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Clément Adam & Léa Paolini & Naïg Gueguen & Guillaume Mabilleau & Laurence Preisser & Simon Blanchard & Pascale Pignon & Florence Manero & Morgane Mao & Alain Morel & Pascal Reynier & Céline Beauvilla, 2021. "Acetoacetate protects macrophages from lactic acidosis-induced mitochondrial dysfunction by metabolic reprograming," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Shuang Shang & Chen Yang & Fei Chen & Ren-shen Xiang & Huan Zhang & Shu-yuan Dai & Jing Liu & Xiao-xi Lv & Cheng Zhang & Xiao-tong Liu & Qi Zhang & Shuai-bing Lu & Jia-wei Song & Jiao-jiao Yu & Ji-cha, 2023. "ID1 expressing macrophages support cancer cell stemness and limit CD8+ T cell infiltration in colorectal cancer," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Fatima Khan & Yiyun Lin & Heba Ali & Lizhi Pang & Madeline Dunterman & Wen-Hao Hsu & Katie Frenis & R. Grant Rowe & Derek A. Wainwright & Kathleen McCortney & Leah K. Billingham & Jason Miska & Craig , 2024. "Lactate dehydrogenase A regulates tumor-macrophage symbiosis to promote glioblastoma progression," Nature Communications, Nature, vol. 15(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:plo:pone00:0241122. 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: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    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.