Principles of cancer therapy: oncogene and non-oncogene addiction

Luo, Ji; Solimini, Nicole L.; Elledge, Stephen J.

doi:10.1016/j.cell.2009.02.024

Cited by 1,765Cancer-related Molecular PathwaysCancer, Hypoxia, and MetabolismPI3K/AKT/mTOR signaling in cancer

Principles of cancer therapy: oncogene and non-oncogene addiction

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Luo, Ji, Solimini, Nicole L., Elledge, Stephen J.·2009·Cell

DOI 10.1016/j.cell.2009.02.024PMC PMC2894612

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Abstract

Cancer is a complex collection of distinct genetic diseases united by common hallmarks. Here, we expand upon the classic hallmarks to include the stress phenotypes of tumorigenesis. We describe a conceptual framework of how oncogene and non-oncogene addictions contribute to these hallmarks and how they can be exploited through stress sensitization and stress overload to selectively kill cancer cells. In particular, we present evidence for a large class of non-oncogenes that are essential for cancer cell survival and present attractive drug targets. Finally, we discuss the path ahead to therapeutic discovery and provide theoretical considerations for combining orthogonal cancer therapies.

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Synthetic lethal partners of KRAS often play critical roles in stress-response pathways such as DNA damage response, genomic stability, cell survival, metabolic adaptation, proteotoxic and oxidative stress.
“Second, synthetic lethal partners of KRAS often play a critical role in stress-response pathways – such as those involved in DNA damage response, genomic stability, cell survival, metabolic adaption, proteotoxic and oxidative stress – that serve to alleviate various forms of oncogenic stress associated with tumorigenesis (34).”
From KRAS mutation in pancreatic cancer (2021) · cites this paper as [34]

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Non-Oncogene Addiction and the Stress Phenotype of Cancer Cells
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Nf1-Dependent Tumors Require a Microenvironment Containing Nf1+/−- and c-kit-Dependent Bone Marrow
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Bortezomib: Proteasome Inhibition as an Effective Anticancer Therapy
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The Challenge of Drugging Undruggable Targets in Cancer: Lessons Learned from Targeting BCL-2 Family Members
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Microenvironmental regulation of cancer development
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Profiling Essential Genes in Human Mammary Cells by Multiplex RNAi Screening
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Flying under the radar: the new wave of BCR–ABL inhibitors
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Anticancer Antifolates: Current Status and Future Directions
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No evidence of clonal somatic genetic alterations in cancer-associated fibroblasts from human breast and ovarian carcinomas
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Relationship of Gene Expression and Chromosomal Abnormalities in Colorectal Cancer
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In vivo Inhibition of Lung Cancer by GRN163L: A Novel Human Telomerase Inhibitor
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Cell intrinsic mechanisms of T‐cell inhibition and application to cancer therapy
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The human Ha-ras oncogene induces genomic instability in murine fibroblasts within one cell cycle.
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DNA Damage Detection and Repair Pathways—Recent Advances with Inhibitors of Checkpoint Kinases in Cancer Therapy
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Inhibition of the Bcr-Abl tyrosine kinase as a therapeutic strategy for CML
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Differentiation therapy
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Targeting Cyclins and Cyclin-Dependent Kinases in Cancer: Lessons from Mice, Hopes for Therapeutic Applications in Humans
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Bortezomib as an Antitumor Agent
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Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
The DNA Damage Response: Making It Safe to Play with Knives
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The extracellular matrix: A dynamic niche in cancer progression
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A comprehensive map of molecular drug targets
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Genomic instability — an evolving hallmark of cancer
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Drugging the undruggable RAS: Mission Possible?
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Immunological effects of conventional chemotherapy and targeted anticancer agents
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Genetic and pharmacological disruption of the TEAD–YAP complex suppresses the oncogenic activity of YAP
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Immunostimulation with chemotherapy in the era of immune checkpoint inhibitors
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Autophagy in malignant transformation and cancer progression
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Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis
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A Genome-wide RNAi Screen Identifies Multiple Synthetic Lethal Interactions with the Ras Oncogene
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Functional characterization of somatic mutations in cancer using network-based inference of protein activity
Alvarez, M. J., Shen, Y., Giorgi, F. M., Lachmann, A., Ding, B. B., Ye, B. H., & Califano, A. (2016) · Nature Genetics · doi:10.1038/ng.3593 · Cited by 966 · see citing works
Cumulative haploinsufficiency and triplosensitivity drive aneuploidy patterns and shape the cancer genome
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Signaling to p53: ribosomal proteins find their way
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Precision medicine for cancer with next-generation functional diagnostics
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APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p
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New frontiers in translational control of the cancer genome
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KRAS mutation in pancreatic cancer
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Exploiting cancer cell vulnerabilities to develop a combination therapy for ras-driven tumors
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A precision oncology approach to the pharmacological targeting of mechanistic dependencies in neuroendocrine tumors
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Functional Precision Medicine Provides Clinical Benefit in Advanced Aggressive Hematologic Cancers and Identifies Exceptional Responders
Kornauth, C., Pemovska, T., Vladimer, G. I., Bayer, G., Bergmann, M., Eder, S., Eichner, R., Erl, M., Esterbauer, H., Exner, R., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-0538 · Cited by 206 · see citing works
Identification of Causal Genetic Drivers of Human Disease through Systems-Level Analysis of Regulatory Networks
Chen, J. C., Alvarez, M. J., Talos, F., Dhruv, H., Rieckhof, G. E., Iyer, A., Diefes, K. L., Aldape, K., Berens, M., Shen, M. M., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.021 · Cited by 188 · see citing works
Small molecules regulating reactive oxygen species homeostasis for cancer therapy
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Protein Homeostasis and the Phenotypic Manifestation of Genetic Diversity: Principles and Mechanisms
Jarosz, D. F., Taipale, M., & Lindquist, S. (2010) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090412 · Cited by 179 · see citing works
Cisplatin Resistance Associated with PARP Hyperactivation
Michels, J., Vitale, I., Galluzzi, L., Adam, J., Olaussen, K. A., Kepp, O., Senovilla, L., Talhaoui, I., Guegan, J., Enot, D. P., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-3000 · Cited by 176 · see citing works
Systematic Identification of Molecular Subtype-Selective Vulnerabilities in Non-Small-Cell Lung Cancer
Kim, H. S., Mendiratta, S., Kim, J., Pecot, C. V., Larsen, J. E., Zubovych, I., Seo, B. Y., Kim, J., Eskiocak, B., Chung, H., et al. (2013) · Cell · doi:10.1016/j.cell.2013.09.041 · Cited by 172 · see citing works
Arsenic targets Pin1 and cooperates with retinoic acid to inhibit cancer-driving pathways and tumor-initiating cells
Kozono, S., Lin, Y.-M., Seo, H.-S., Pinch, B., Lian, X., Qiu, C., Herbert, M. K., Chen, C.-H., Tan, L., Gao, Z. J., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05402-2 · Cited by 168 · see citing works
Targeted degradation of the enhancer lysine acetyltransferases CBP and p300
Vannam, R., Sayilgan, J., Ojeda, S., Karakyriakou, B., Hu, E., Kreuzer, J., Morris, R., Herrera Lopez, X. I., Rai, S., Haas, W., et al. (2021) · Cell Chemical Biology · doi:10.1016/j.chembiol.2020.12.004 · Cited by 177 · see citing works
Poly(Ethylene Glycol)–Polylactide Micelles for Cancer Therapy
Wang, J., Li, S., Han, Y., Guan, J., Chung, S., Wang, C., & Li, D. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00202 · Cited by 155 · see citing works
Identification of small molecule proliferating cell nuclear antigen (PCNA) inhibitor that disrupts interactions with PIP-box proteins and inhibits DNA replication
Punchihewa, C., Inoue, A., Hishiki, A., Fujikawa, Y., Connelly, M., Evison, B., Shao, Y., Heath, R., Kuraoka, I., Rodrigues, P., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.353201 · Cited by 135 · see citing works
MAP kinase and autophagy pathways cooperate to maintain RAS mutant cancer cell survival
Lee, C.-S., Lee, L. C., Yuan, T. L., Chakka, S., Fellmann, C., Lowe, S. W., Caplen, N. J., McCormick, F., & Luo, J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1817494116 · Cited by 126 · see citing works
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Histone H2B ubiquitin ligase RNF20 is required for MLL -rearranged leukemia
Wang, E., Kawaoka, S., Yu, M., Shi, J., Ni, T., Yang, W., Zhu, J., Roeder, R. G., & Vakoc, C. R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301045110 · Cited by 121 · see citing works
Targeting EGFR in Lung Cancer: Current Standards and Developments
Díaz-Serrano, A., Gella, P., Jiménez, E., Zugazagoitia, J., & Paz-Ares Rodríguez, L. (2018) · Drugs · doi:10.1007/s40265-018-0916-4 · Cited by 108 · see citing works
Integrating the DNA damage and protein stress responses during cancer development and treatment
Gorgoulis, V. G., Pefani, D., Pateras, I. S., & Trougakos, I. P. (2018) · The Journal of Pathology · doi:10.1002/path.5097 · Cited by 108 · see citing works
Meta-analysis of the global gene expression profile of triple-negative breast cancer identifies genes for the prognostication and treatment of aggressive breast cancer
Al-Ejeh, F., Simpson, P. T., Sanus, J. M., Klein, K., Kalimutho, M., Shi, W., Miranda, M., Kutasovic, J., Raghavendra, A., Madore, J., et al. (2014) · Oncogenesis · doi:10.1038/oncsis.2014.14 · Cited by 107 · see citing works
DDIT4 promotes gastric cancer proliferation and tumorigenesis through the p53 and MAPK pathways
Du, F., Sun, L., Chu, Y., Li, T., Lei, C., Wang, X., Jiang, M., Min, Y., Lu, Y., Zhao, X., et al. (2018) · Cancer Communications · doi:10.1186/s40880-018-0315-y · Cited by 103 · see citing works
Synthetic Lethal Vulnerabilities in KRAS-Mutant Cancers
Aguirre, A. J., & Hahn, W. C. (2018) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a031518 · Cited by 90 · see citing works
The Oxygen Paradox, the French Paradox, and age-related diseases
Davies, J. M. S., Cillard, J., Friguet, B., Cadenas, E., Cadet, J., Cayce, R., Fishmann, A., Liao, D., Bulteau, A.-L., Derbré, F., et al. (2017) · GeroScience · doi:10.1007/s11357-017-0002-y · Cited by 82 · see citing works
“̂ Among these are DNA damage, mitotic stress, metabolic stress, and oxidative stress, which are all sensitive to reactive oxygen species-mediated signaling (Luo et al. 2009).”
Background
Inactivation of the CRL4-CDT2-SET8/p21 ubiquitylation and degradation axis underlies the therapeutic efficacy of pevonedistat in melanoma
Benamar, M., Guessous, F., Du, K., Corbett, P., Obeid, J., Gioeli, D., Slingluff, C. L., & Abbas, T. (2016) · eBioMedicine · doi:10.1016/j.ebiom.2016.06.023 · Cited by 77 · see citing works
Targeting Nrf2 with wogonin overcomes cisplatin resistance in head and neck cancer
Kim, E. H., Jang, H., Shin, D., Baek, S. H., & Roh, J.-L. (2016) · APOPTOSIS · doi:10.1007/s10495-016-1284-8 · Cited by 77 · see citing works
Mutational signatures reveal the role of RAD52 in p53-independent p21-driven genomic instability
Galanos, P., Pappas, G., Polyzos, A., Kotsinas, A., Svolaki, I., Giakoumakis, N. N., Glytsou, C., Pateras, I. S., Swain, U., Souliotis, V. L., et al. (2018) · Genome Biology · doi:10.1186/s13059-018-1401-9 · Cited by 67 · see citing works
MDM2 antagonists synergize broadly and robustly with compounds targeting fundamental oncogenic signaling pathways
Saiki, A. Y., Caenepeel, S., Yu, D., Lofgren, J. A., Osgood, T., Robertson, R., Canon, J., Su, C., Jones, A., Zhao, X., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.1918 · Cited by 55 · see citing works
The mTOR pathway negatively controls ATM by up-regulating miRNAs
Shen, C., & Houghton, P. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220898110 · Cited by 50 · see citing works
Evolving toward a human-cell based and multiscale approach to drug discovery for CNS disorders
Schadt, E. E., Buchanan, S., Brennand, K. J., & Merchant, K. M. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00252 · Cited by 39 · see citing works
Karyotypic Aberrations in Oncogenesis and Cancer Therapy
Vitale, I., Manic, G., Senovilla, L., Kroemer, G., & Galluzzi, L. (2015) · Trends in Cancer · doi:10.1016/j.trecan.2015.08.001 · Cited by 34 · see citing works
Cellular Redox Imbalance and Changes of Protein S-glutathionylation Patterns Are Associated with Senescence Induced by Oncogenic H-Ras
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Authors: Luo, J., Solimini, N. L., & Elledge, S. J.
Affiliations: Brigham and Women's Hospital (US)
Corresponding author: Elledge, Stephen J.
ORCID: Luo, Ji
Solimini, Nicole L.
Elledge, Stephen J.
Venue: Cell
Publisher: Elsevier BV
Published: 2009-03
Volume: 136
Issue: 5
Pages: 823-837
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2009.02.024
PMC: PMC2894612
OpenAlex: W2077813812
Cited by: 1,765
References: 124
Citations by year: 2026: 48 · 2025: 66 · 2024: 64 · 2023: 72 · 2022: 92 · 2021: 96 · 2020: 102 · 2019: 93 · 2018: 87 · 2017: 107 · 2016: 108 · 2015: 132 · 2014: 153 · 2013: 131 · 2012: 143
FWCI: 68.26
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1635 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (R33CA140039)
Topics: Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › PI3K/AKT/mTOR signaling in cancer
Keywords: cancer hallmarks, oncogene addiction, non-oncogene addiction, stress sensitization, stress overload, tumor cell survival, therapeutic target, combination cancer therapy, cancer therapy
MeSH terms: Animals, Hypoxia, Humans, Neoplasms, Oncogenes, Genes, Tumor Suppressor

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Principles of cancer therapy: oncogene and non-oncogene addiction

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