Cited by 344Cancer Genomics and DiagnosticsGlioma Diagnosis and TreatmentCancer, Hypoxia, and Metabolism

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Passenger deletions generate therapeutic vulnerabilities in cancer

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Muller, Florian L., Colla, Simona, Aquilanti, Elisa, Manzo, Veronica E., Genovese, Giannicola, Lee, Jaclyn, Eisenson, Daniel, Narurkar, Rujuta, Deng, Pingna, Nezi, Luigi, Lee, Michelle A., Hu, Baoli, Hu, Jian, Sahin, Ergun, Ong, Derrick, Fletcher-Sananikone, Eliot, Ho, Dennis, Kwong, Lawrence, Brennan, Cameron, Wang, Y. Alan, Chin, Lynda, DePinho, Ronald A.·2012·Nature

DOI 10.1038/nature11331PMC PMC3712624

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Abstract

Inactivation of tumour-suppressor genes by homozygous deletion is a prototypic event in the cancer genome, yet such deletions often encompass neighbouring genes. We propose that homozygous deletions in such passenger genes can expose cancer-specific therapeutic vulnerabilities when the collaterally deleted gene is a member of a functionally redundant family of genes carrying out an essential function. The glycolytic gene enolase 1 (ENO1) in the 1p36 locus is deleted in glioblastoma (GBM), which is tolerated by the expression of ENO2. Here we show that short-hairpin-RNA-mediated silencing of ENO2 selectively inhibits growth, survival and the tumorigenic potential of ENO1-deleted GBM cells, and that the enolase inhibitor phosphonoacetohydroxamate is selectively toxic to ENO1-deleted GBM cells relative to ENO1-intact GBM cells or normal astrocytes. The principle of collateral vulnerability should be applicable to other passenger-deleted genes encoding functionally redundant essential activities and provide an effective treatment strategy for cancers containing such genomic events.

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Authors: Muller, F. L., Colla, S., Aquilanti, E., Manzo, V. E., Genovese, G., Lee, J., Eisenson, D., Narurkar, R., Deng, P., Nezi, L., Lee, M. A., Hu, B., Hu, J., Sahin, E., Ong, D., Fletcher-Sananikone, E., Ho, D., Kwong, L., Brennan, C., Wang, Y. A., Chin, L., & DePinho, R. A.
Affiliations: The University of Texas MD Anderson Cancer Center (US)
Dana-Farber Cancer Institute (US)
Harvard University (US)
Memorial Sloan Kettering Cancer Center (US)
Corresponding author: DePinho, Ronald A.
ORCID: Colla, Simona
Aquilanti, Elisa
Genovese, Giannicola
Lee, Jaclyn
Eisenson, Daniel
Deng, Pingna
Nezi, Luigi
Hu, Baoli
Hu, Jian
Ong, Derrick
Kwong, Lawrence
Brennan, Cameron
Wang, Y. Alan
DePinho, Ronald A.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-08-15
Volume: 488
Issue: 7411
Pages: 337-342
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature11331
PMC: PMC3712624
OpenAlex: W1982318323
Cited by: 339
References: 38
Citations by year: 2026: 12 · 2025: 20 · 2024: 20 · 2023: 20 · 2022: 32 · 2021: 34 · 2020: 32 · 2019: 32 · 2018: 20 · 2017: 27 · 2016: 18 · 2015: 19 · 2014: 33 · 2013: 14 · 2012: 6
FWCI: 7.62
Type: journal article
Language: en
Update notices: correction (2015-07-08)
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Howard Hughes Medical Institute (57006984)
National Eye Institute (R01EY020641)
National Cancer Institute (P01 CA 95616, T32CA009361, P01CA095616)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Health Sciences › Medicine › Oncology › Glioma Diagnosis and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Keywords: alpha-enolase, neuron-specific enolase, enolase, 1p36 deletion, glioblastoma, housekeeping genes, glycolysis, RNA interference, tumor suppressor, cancer therapy
MeSH terms: Animals, Antineoplastic Agents, Brain Neoplasms, Chromosomes, Human, Pair 1, DNA-Binding Proteins, Enzyme Inhibitors, Glioblastoma, Homozygote, Humans, Hydroxamic Acids, Neoplasm Transplantation, Phosphonoacetic Acid, Phosphopyruvate Hydratase, Biomarkers, Tumor, Gene Expression Regulation, Neoplastic, Genes, Tumor Suppressor, Sequence Deletion, Genes, Essential, Tumor Suppressor Proteins, RNA, Small Interfering, Cell Line, Tumor, Cell Proliferation, Mice, Gene Knockdown Techniques, Molecular Targeted Therapy

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Passenger deletions generate therapeutic vulnerabilities in cancer

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