Metabolic impairment of non-small cell lung cancers by mitochondrial HSPD1 targeting
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Abstract
BACKGROUND: The identification of novel targets is of paramount importance to develop more effective drugs and improve the treatment of non-small cell lung cancer (NSCLC), the leading cause of cancer-related deaths worldwide. Since cells alter their metabolic rewiring during tumorigenesis and along cancer progression, targeting key metabolic players and metabolism-associated proteins represents a valuable approach with a high therapeutic potential. Metabolic fitness relies on the functionality of heat shock proteins (HSPs), molecular chaperones that facilitate the correct folding of metabolism enzymes and their assembly in macromolecular structures. METHODS: Gene fitness was determined by bioinformatics analysis from available datasets from genetic screenings. HSPD1 expression was evaluated by immunohistochemistry from formalin-fixed paraffin-embedded tissues from NSCLC patients. Real-time proliferation assays with and without cytotoxicity reagents, colony formation assays and cell cycle analyses were used to monitor growth and drug sensitivity of different NSCLC cells in vitro. In vivo growth was monitored with subcutaneous injections in immune-deficient mice. Cell metabolic activity was analyzed through extracellular metabolic flux analysis. Specific knockouts were introduced by CRISPR/Cas9. RESULTS: We show heat shock protein family D member 1 (HSPD1 or HSP60) as a survival gene ubiquitously expressed in NSCLC and associated with poor patients' prognosis. HSPD1 knockdown or its chemical disruption by the small molecule KHS101 induces a drastic breakdown of oxidative phosphorylation, and suppresses cell proliferation both in vitro and in vivo. By combining drug profiling with transcriptomics and through a whole-genome CRISPR/Cas9 screen, we demonstrate that HSPD1-targeted anti-cancer effects are dependent on oxidative phosphorylation and validated molecular determinants of KHS101 sensitivity, in particular, the creatine-transporter SLC6A8 and the subunit of the cytochrome c oxidase complex COX5B. CONCLUSIONS: These results highlight mitochondrial metabolism as an attractive target and HSPD1 as a potential theranostic marker for developing therapies to combat NSCLC.
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H460, A549, and H1299 cell lines are frequently used as widely accepted cell models in the context of the metabolic rewiring of NSCLC.
“H460, A549, and H1299 cell lines are frequently used as widely accepted cell models in the context of the metabolic rewiring of NSCLC [41,42,43].”
From 20-Hydroxyecdysone Confers Antioxidant and Antineoplastic Properties in Human Non-Small Cell Lung Cancer Cells (2023) · cites this paper as [41]
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- Authors
- Parma, B., Ramesh, V., Gollavilli, P. N., Siddiqui, A., Pinna, L., Schwab, A., Marschall, S., Zhang, S., Pilarsky, C., Napoli, F., Volante, M., Urbanczyk, S., Mielenz, D., Schrøder, H. D., Stemmler, M., Wurdak, H., & Ceppi, P.
- Affiliations
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- University of Southern Denmark (DK)
- University of Turin (IT)
- Odense University Hospital (DK)
- University of Leeds (GB)
- Corresponding author
- Wurdak, Heiko
- Ceppi, Paolo
- ORCID
- Venue
- Journal of Experimental & Clinical Cancer Research
- Published
- 2021-08-07
- Volume
- 40
- Issue
- 1
- Pages
- 248-248
- ISSN
- 0392-9078 (ISSN-L)
- 1756-9966
- PMC
- PMC8348813
- OpenAlex
- W3191219818
- Cited by
- 46
- References
- 61
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 7 · 2023: 10 · 2022: 9
- FWCI
- 2.58
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal of Experimental & Clinical Cancer Research (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- OPUS Repository (Kooperativer Bibliotheksverbund Berlin-Brandenburg) (submittedVersion, cc-by)
- Funders
- Deutsche Forschungsgemeinschaft (DFG-CE-281/5-1)
- H2020 European Research Council (MSCA-ITN-ETN PRECODE 861196)
- Friedrich-Alexander-Universität Erlangen-Nürnberg
- danmarks frie forskningsfond (0134-00012B)
- Universitätsklinikum Erlangen
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
- Keywords
- non-small cell lung cancer, HSPD1, HSP60, mitochondrial metabolism, oxidative phosphorylation, SLC6A8, creatine transporter, COX5B, cytochrome c oxidase, cancer metabolism, gene fitness, CRISPR-Cas9 screen, drug sensitivity, prognostic factors, cell proliferation
- MeSH terms
- Animals, Carcinoma, Non-Small-Cell Lung, Disease Models, Animal, Humans, Lung Neoplasms, Mitochondria, Survival Analysis, Chaperonin 60, Mitochondrial Proteins, Mice
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