Principles of cancer therapy: oncogene and non-oncogene addiction - PubMed (original) (raw)
Principles of cancer therapy: oncogene and non-oncogene addiction
Ji Luo et al. Cell. 2009.
Erratum in
- Cell. 2009 Aug 21;138(4):807
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.
Figures
Figure 1. The Hallmarks of Cancer
In addition to the six hallmarks originally proposed by Hanahan and Weinberg (top half, white symbols) and evasion of immune surveillance proposed by Kroemer and Pouyssegur, we propose a set of additional hallmarks that depict the stress phenotypes of cancer cells (lower half, colored symbols). These include metabolic stress, proteotoxic stress, mitotic stress, oxidative stress, and DNA damage stress. Functional interplays among these hallmarks promote the tumorigenic state and suppress oncogenic stress. For example, the utilization of glycolysis allows tumor cells to adapt to hypoxia and acidify its microenvironment to evade immune surveillance. Increased mitotic stress promotes aneuploidy, which leads to proteotoxic stress that requires compensation from the heat shock response pathway. Elevated levels of reactive oxygen species result in increased levels of DNA damage that normally elicits senescence or apoptosis but is overcome by tumor cells.
Figure 2. Examples of Non-oncogene Addictions in Cancer Cells
The tumorigenic state results in a variety of alterations (shown on top), which are related to the hallmarks described in Figure 1. These alterations give rise to a number of potentially deleterious circumstances or vulnerabilities (detailed in the bottom half) that could be lethal to the tumor cells if left unchecked. The existence of stress support pathways (shown in red) help suppress this lethality. Many of these pathways are examples of non-oncogene addiction (NOA), and therapeutics that interfere with their functions could display synthetic lethality with the tumor genotype/phenotype.
Figure 3. The Combinatorial Filter of Orthogonal Cancer Therapies
A tumor consists of genetically distinct subpopulations of cancer cells (represented by the different cell shapes), each with its own characteristic sensitivity profile to a given therapeutic agent. Each cancer therapy can be viewed as a filter that removes a subpopulation of cancer cells that are sensitive to this treatment while allowing other insensitive subpopulations to escape. This escape occurs as a result of suppressor mutations that occur at a given frequency (v) unique to each therapy and tumor type. By combining therapies with orthogonal modes of action, a combinatorial filter can be set up to minimize the recurrence index (RI) of the cancer. N represents the total number of cancer cells in the tumor. A combination of orthogonal therapies that result in RI < 1 would greatly enhance the likelihood of preventing tumor recurrence.
Similar articles
- Non-oncogene dependencies: Novel opportunities for cancer therapy.
Di Marco T, Mazzoni M, Greco A, Cassinelli G. Di Marco T, et al. Biochem Pharmacol. 2024 Oct;228:116254. doi: 10.1016/j.bcp.2024.116254. Epub 2024 May 3. Biochem Pharmacol. 2024. PMID: 38704100 Review. - Drugging the addict: non-oncogene addiction as a target for cancer therapy.
Nagel R, Semenova EA, Berns A. Nagel R, et al. EMBO Rep. 2016 Nov;17(11):1516-1531. doi: 10.15252/embr.201643030. Epub 2016 Oct 4. EMBO Rep. 2016. PMID: 27702988 Free PMC article. Review. - Oncogene addiction: pathways of therapeutic response, resistance, and road maps toward a cure.
Pagliarini R, Shao W, Sellers WR. Pagliarini R, et al. EMBO Rep. 2015 Mar;16(3):280-96. doi: 10.15252/embr.201439949. Epub 2015 Feb 13. EMBO Rep. 2015. PMID: 25680965 Free PMC article. Review. - How cancers escape their oncogene habit.
Giuriato S, Felsher DW. Giuriato S, et al. Cell Cycle. 2003 Jul-Aug;2(4):329-32. Cell Cycle. 2003. PMID: 12851484 Review. - Mechanisms of disease: Oncogene addiction--a rationale for molecular targeting in cancer therapy.
Weinstein IB, Joe AK. Weinstein IB, et al. Nat Clin Pract Oncol. 2006 Aug;3(8):448-57. doi: 10.1038/ncponc0558. Nat Clin Pract Oncol. 2006. PMID: 16894390 Review.
Cited by
- Targeting carbohydrate metabolism in colorectal cancer - synergy between DNA-damaging agents, cannabinoids, and intermittent serum starvation.
Cherkasova V, Kovalchuk O, Kovalchuk I. Cherkasova V, et al. Oncoscience. 2024 Nov 12;11:99-105. doi: 10.18632/oncoscience.611. eCollection 2024. Oncoscience. 2024. PMID: 39534512 Free PMC article. Review. - HSPD1 Supports Osteosarcoma Progression through Stabilizing ATP5A1 and thus Activation of AKT/mTOR Signaling.
Zhang Y, Pan R, Li K, Cheang LH, Zhao J, Zhong Z, Li S, Wang J, Zhang X, Cheng Y, Zheng X, He R, Wang H. Zhang Y, et al. Int J Biol Sci. 2024 Sep 23;20(13):5162-5190. doi: 10.7150/ijbs.100015. eCollection 2024. Int J Biol Sci. 2024. PMID: 39430254 Free PMC article. - Potential promising of synthetic lethality in cancer research and treatment.
Karami Fath M, Najafiyan B, Morovatshoar R, Khorsandi M, Dashtizadeh A, Kiani A, Farzam F, Kazemi KS, Nabi Afjadi M. Karami Fath M, et al. Naunyn Schmiedebergs Arch Pharmacol. 2024 Sep 21. doi: 10.1007/s00210-024-03444-6. Online ahead of print. Naunyn Schmiedebergs Arch Pharmacol. 2024. PMID: 39305329 Review. - Wee1 inhibitor PD0166285 sensitized TP53 mutant lung squamous cell carcinoma to cisplatin via STAT1.
Li Q, Yang W, Zhang Q, Zhang D, Deng J, Chen B, Li P, Zhang H, Jiang Y, Li Y, Zhang B, Lin N. Li Q, et al. Cancer Cell Int. 2024 Sep 13;24(1):315. doi: 10.1186/s12935-024-03489-w. Cancer Cell Int. 2024. PMID: 39272147 Free PMC article. - The stress response regulator HSF1 modulates natural killer cell anti-tumour immunity.
Hockemeyer K, Sakellaropoulos T, Chen X, Ivashkiv O, Sirenko M, Zhou H, Gambi G, Battistello E, Avrampou K, Sun Z, Guillamot M, Chiriboga L, Jour G, Dolgalev I, Corrigan K, Bhatt K, Osman I, Tsirigos A, Kourtis N, Aifantis I. Hockemeyer K, et al. Nat Cell Biol. 2024 Oct;26(10):1734-1744. doi: 10.1038/s41556-024-01490-z. Epub 2024 Sep 2. Nat Cell Biol. 2024. PMID: 39223375
References
- Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, Huang H, Porter D, Hu M, Chin L, Richardson A, et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell. 2004;6:17, 32. - PubMed
- Ashwell S, Zabludoff S. DNA damage detection and repair pathways-recent advances with inhibitors of checkpoint kinases in cancer therapy. Clin. Cancer Res. 2008;14:4032, 4037. - PubMed
- Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, Guldberg P, Sehested M, Nesland JM, Lukas C, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature. 2005;434:864, 870. - PubMed
- Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou LV, Kolettas E, Niforou K, Zoumpourlis VC, et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature. 2006;444:633, 637. - PubMed
- Bonnet S, Archer SL, Allalunis-Turner J, Haromy A, Beaulieu C, Thompson R, Lee CT, Lopaschuk GD, Puttagunta L, Harry G, et al. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell. 2007;11:37, 51. - PubMed
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Other Literature Sources