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Cryptococcal Hsf3 controls intramitochondrial ROS homeostasis by regulating the respiratory process

Author

Listed:
  • Xindi Gao

    (Northeastern University)

  • Yi Fu

    (Northeastern University)

  • Shengyi Sun

    (Northeastern University)

  • Tingyi Gu

    (Northeastern University)

  • Yanjian Li

    (Northeastern University)

  • Tianshu Sun

    (Beijing Key Laboratory for Mechanisms Research and Precision Diagnosis of Invasive Fungal Diseases
    Chinese Academy of Medical Science)

  • Hailong Li

    (The First Affiliated Hospital of China Medical University)

  • Wei Du

    (Northeastern University)

  • Chenhao Suo

    (Northeastern University)

  • Chao Li

    (Northeastern University)

  • Yiru Gao

    (Northeastern University)

  • Yang Meng

    (Northeastern University)

  • Yue Ni

    (Northeastern University)

  • Sheng Yang

    (Northeastern University)

  • Tian Lan

    (Northeastern University)

  • Sixiang Sai

    (Binzhou Medical University)

  • Jiayi Li

    (BMC A10)

  • Kun Yu

    (Northeastern University)

  • Ping Wang

    (Louisiana State University Health Sciences Center)

  • Chen Ding

    (Northeastern University)

Abstract

Mitochondrial quality control prevents accumulation of intramitochondrial-derived reactive oxygen species (mtROS), thereby protecting cells against DNA damage, genome instability, and programmed cell death. However, underlying mechanisms are incompletely understood, particularly in fungal species. Here, we show that Cryptococcus neoformans heat shock factor 3 (CnHsf3) exhibits an atypical function in regulating mtROS independent of the unfolded protein response. CnHsf3 acts in nuclei and mitochondria, and nuclear- and mitochondrial-targeting signals are required for its organelle-specific functions. It represses the expression of genes involved in the tricarboxylic acid cycle while promoting expression of genes involved in electron transfer chain. In addition, CnHsf3 responds to multiple intramitochondrial stresses; this response is mediated by oxidation of the cysteine residue on its DNA binding domain, which enhances DNA binding. Our results reveal a function of HSF proteins in regulating mtROS homeostasis that is independent of the unfolded protein response.

Suggested Citation

  • Xindi Gao & Yi Fu & Shengyi Sun & Tingyi Gu & Yanjian Li & Tianshu Sun & Hailong Li & Wei Du & Chenhao Suo & Chao Li & Yiru Gao & Yang Meng & Yue Ni & Sheng Yang & Tian Lan & Sixiang Sai & Jiayi Li & , 2022. "Cryptococcal Hsf3 controls intramitochondrial ROS homeostasis by regulating the respiratory process," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33168-1
    DOI: 10.1038/s41467-022-33168-1
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    References listed on IDEAS

    as
    1. Rocio Gomez-Pastor & Eileen T. Burchfiel & Daniel W. Neef & Alex M. Jaeger & Elisa Cabiscol & Spencer U. McKinstry & Argenia Doss & Alejandro Aballay & Donald C. Lo & Sergey S. Akimov & Christopher A., 2017. "Abnormal degradation of the neuronal stress-protective transcription factor HSF1 in Huntington’s disease," Nature Communications, Nature, vol. 8(1), pages 1-17, April.
    2. Ke Tan & Mitsuaki Fujimoto & Ryosuke Takii & Eiichi Takaki & Naoki Hayashida & Akira Nakai, 2015. "Erratum: Mitochondrial SSBP1 protects cells from proteotoxic stresses by potentiating stress-induced HSF1 transcriptional activity," Nature Communications, Nature, vol. 6(1), pages 1-1, November.
    3. Kwang-Woo Jung & Dong-Hoon Yang & Shinae Maeng & Kyung-Tae Lee & Yee-Seul So & Joohyeon Hong & Jaeyoung Choi & Hyo-Jeong Byun & Hyelim Kim & Soohyun Bang & Min-Hee Song & Jang-Won Lee & Min Su Kim & S, 2015. "Systematic functional profiling of transcription factor networks in Cryptococcus neoformans," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
    4. Ke Tan & Mitsuaki Fujimoto & Ryosuke Takii & Eiichi Takaki & Naoki Hayashida & Akira Nakai, 2015. "Mitochondrial SSBP1 protects cells from proteotoxic stresses by potentiating stress-induced HSF1 transcriptional activity," Nature Communications, Nature, vol. 6(1), pages 1-16, May.
    5. Camaron R. Hole & Chrissy M. Leopold Wager & Natalia Castro-Lopez & Althea Campuzano & Hong Cai & Karen L. Wozniak & Yufeng Wang & Floyd L. Wormley, 2019. "Induction of memory-like dendritic cell responses in vivo," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
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