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Chaperone-mediated autophagy promotes PCa survival during ARPI through selective proteome remodeling

Oncogene volume 42, pages 748–758 (2023)Cite this article

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Abstract

The androgen receptor (AR) plays an important role in PCa metabolism, with androgen receptor pathway inhibition (ARPI) subjecting PCa cells to acute metabolic stress caused by reduced biosynthesis and energy production. Defining acute stress response mechanisms that alleviate ARPI stress and therefore mediate prostate cancer (PCa) treatment resistance will help improve therapeutic outcomes of patients treated with ARPI. We identified the up-regulation of chaperone-mediated autophagy (CMA) in response to acute ARPI stress, which persisted in castration-resistant PCa (CRPC); previously undefined in PCa. CMA is a selective protein degradation pathway and a key stress response mechanism up-regulated under several stress stimuli, including metabolic stress. Through selective protein degradation, CMA orchestrates the cellular stress response by regulating cellular pathways through selective proteome remodeling. Through broad-spectrum proteomic analysis, CMA coordinates metabolic reprogramming of PCa cells to sustain PCa growth and survival during ARPI; through the upregulation of mTORC1 signaling and pathways associated with PCa biosynthesis and energetics. This not only promoted PCa growth during ARPI, but also promoted the emergence of CRPC in-vivo. During CMA inhibition, PCa metabolism is compromised, leading to ATP depletion, resulting in a profound anti-proliferative effect on PCa cells, and is enhanced when combined with ARPI. Furthermore, CMA inhibition prevented in-vivo tumour formation, and also re-sensitized enzalutamide-resistant cell lines in-vitro. The profound anti-proliferative effect of CMA inhibition was attributed to cell cycle arrest mediated through p53 transcriptional repression of E2F target genes. In summary, CMA is an acute ARPI stress response mechanism, essential in alleviating ARPI induced metabolic stress, essential for ensuring PCa growth and survival. CMA plays a critical role in the development of ARPI resistance in PCa.

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Fig. 1: ARPI induced stress upregulates CMA in AR driven PCa.
Fig. 2: CMA is essential for PCa growth and promotes ARPI treatment resistance.
Fig. 3: CMA coordinates the ARPI stress response in PCa cells through proteome remodeling.
Fig. 4: CMA sustains the metabolism of PCa cells and protects against ARPI induced metabolic stress.
Fig. 5: CMAi compromises PCa cell proliferation, promoting cell cycle arrest.
Fig. 6: Canonical CMA recognition motif shared between HK1 and HK2.

Data availability

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD036227”.

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Funding

MG acknowledge Terry Fox New Frontiers Program Project (1062) for supporting this research.

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Authors and Affiliations

  1. Vancouver Prostate Centre, University of British Columbia, Vancouver, BC, Canada

    Nicholas Nikesitch, Eliana Beraldi, Fan Zhang, Hans Adomat, Robert Bell, Kotaro Suzuki, Ladan Fazli, Sonia HY Kung, Christopher Wells, Nicholas Pinette, Neetu Saxena, Yuzhuo Wang & Martin Gleave

  2. Department of Urologic Sciences, University of British Columbia, Vancouver, BC, Canada

    Nicholas Nikesitch, Eliana Beraldi, Fan Zhang, Robert Bell, Kotaro Suzuki, Ladan Fazli, Nicholas Pinette, Neetu Saxena, Yuzhuo Wang & Martin Gleave

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  1. Nicholas Nikesitch
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Contributions

NN and MG conceived the idea and developed the project. NN designed and conducted the experiments, analyzed the data, discussed, and co-wrote the manuscript; NN, EB, FZ, HA, KS, LF, SK, CW, NP, and NS performed experiments; LF scored the TMAs; and MG led the research program, discussed the data, and co-wrote the manuscript.

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Correspondence to Martin Gleave.

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Nikesitch, N., Beraldi, E., Zhang, F. et al. Chaperone-mediated autophagy promotes PCa survival during ARPI through selective proteome remodeling. Oncogene 42, 748–758 (2023). https://doi.org/10.1038/s41388-022-02573-7

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