Cited by 452Redox biology and oxidative stressCancer and biochemical researchAntioxidant Activity and Oxidative Stress

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The multifaceted role of reactive oxygen species in tumorigenesis

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Kirtonia, Anuradha, Sethi, Gautam, Garg, Manoj·2020·Cellular and Molecular Life Sciences

DOI 10.1007/s00018-020-03536-5PMC PMC11105050

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Abstract

Redox homeostasis is an essential requirement of the biological systems for performing various normal cellular functions including cellular growth, differentiation, senescence, survival and aging in humans. The changes in the basal levels of reactive oxygen species (ROS) are detrimental to cells and often lead to several disease conditions including cardiovascular, neurological, diabetes and cancer. During the last two decades, substantial research has been done which clearly suggests that ROS are essential for the initiation, progression, angiogenesis as well as metastasis of cancer in several ways. During the last two decades, the potential of dysregulated ROS to enhance tumor formation through the activation of various oncogenic signaling pathways, DNA mutations, immune escape, tumor microenvironment, metastasis, angiogenesis and extension of telomere has been discovered. At present, surgery followed by chemotherapy and/or radiotherapy is the major therapeutic modality for treating patients with either early or advanced stages of cancer. However, the majority of patients relapse or did not respond to initial treatment. One of the reasons for recurrence/relapse is the altered levels of ROS in tumor cells as well as in cancer-initiating stem cells. One of the critical issues is targeting the intracellular/extracellular ROS for significant antitumor response and relapse-free survival. Indeed, a large number of FDA-approved anticancer drugs are efficient to eliminate cancer cells and drug resistance by increasing ROS production. Thus, the modulation of oxidative stress response might represent a potential approach to eradicate cancer in combination with FDA-approved chemotherapies, radiotherapies as well as immunotherapies.

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Background
Nanotechnology-integrated ferroptosis inducers: a sharp sword against tumor drug resistance
Li, C., Wu, X., Zheng, C., Xu, S., Liu, Y., Qin, J., Fan, X., Ye, Y., & Fei, W. (2022) · Journal of Materials Chemistry B · doi:10.1039/d2tb01350a · Cited by 26
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Manica, D., da Silva, G. B., da Silva, A. P., Marafon, F., Maciel, S. F. V. D. O., Bagatini, M. D., & Moreno, M. (2023) · Cell Biochemistry and Function · doi:10.1002/cbf.3863 · Cited by 26
(-)-Asarinin alleviates gastric precancerous lesions by promoting mitochondrial ROS accumulation and inhibiting the STAT3 signaling pathway
Zhao, M., Wen, Y., Yang, Y., Pan, H., Xie, S., Shen, C., Liao, W., Chen, N., Zhang, G., Zhang, G., et al. (2024) · Phytomedicine · doi:10.1016/j.phymed.2024.155348 · Cited by 25
Nanoparticles (NPs)-mediated targeted regulation of redox homeostasis for effective cancer therapy
Zhao, Z., Cao, Y., Xu, R. F., Fang, J., Zhang, Y., Xu, X., Huang, L., & Li, R. (2024) · Smart Materials in Medicine · doi:10.1016/j.smaim.2024.03.003 · Cited by 27
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Zhang, Y., YAN, H. H., Wei, Y., & Wei, X. (2024) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2024.189107 · Cited by 30
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Tuli, H. S., Aggarwal, V., Tuorkey, M. J., Aggarwal, D., Parashar, N. C., Varol, M., Savla, R., Kaur, G., Mittal, S., & Sak, K. (2021) · Toxicology in Vitro · doi:10.1016/j.tiv.2021.105142 · Cited by 27
Multidirectional Strategies for Targeted Delivery of Oncolytic Viruses by Tumor Infiltrating Immune Cells
Osali, A., Zhiani, M., Ghaebi, M., Meymanat, M., & Esmaeilzadeh, A. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105094 · Cited by 25
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Kim, N. Y., Jung, Y. Y., Yang, M. H., Chinnathambi, A., Govindasamy, C., Narula, A. S., Namjoshi, O. A., Blough, B. E., & Ahn, K. S. (2022) · Biochimie · doi:10.1016/j.biochi.2022.05.018 · Cited by 24
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Basmadjian, O. M., Occhieppo, V. B., Marchese, N. A., Silvero, M. J., Becerra, M. C., Baiardi, G., & Bregonzio, C. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.647747 · Cited by 24
Cross‑link between ferroptosis and nasopharyngeal carcinoma: New approach to radiotherapy sensitization (Review)
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Pro-Oxidant Effect of Resveratrol on Human Breast Cancer MCF-7 Cells is Associated with CK2 Inhibition
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“These compounds can inhibit NF-κB, regulate MAPKs, deplete GPX, activate JNK and p38 pathways, and increase mitochondrial membrane potential by modulating reactive oxygen species in human cancers (32).”
Background
Black cardamom (Amomum subulatum Roxb.) fruit extracts exhibit apoptotic activity against lung cancer cells
Makhija, P., Handral, H. K., Mahadevan, G., Kathuria, H., Sethi, G., & Grobben, B. (2021) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2021.114953 · Cited by 23
Self-citation
Emerging roles of ferroptosis-related miRNAs in tumor metastasis
Jiang, Z., Zhou, J., Deng, J., Li, L., Wang, R., Han, Y., Zhou, J., Tao, R., Peng, L., Wang, D., et al. (2023) · Cell Death Discovery · doi:10.1038/s41420-023-01486-y · Cited by 23
Nanoparticles based on polymers modified with pH-sensitive molecular switch and low molecular weight heparin carrying Celastrol and ferrocene for breast cancer treatment
Qian, Y., Zhang, J., Xu, R., Li, Q., Shen, Q., & Zhu, G. (2021) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2021.05.204 · Cited by 23
Reprogramming of glycolysis by chemical carcinogens during tumor development
D’Souza, L. C., Shekher, A., Challagundla, K. B., Sharma, A., & Gupta, S. C. (2022) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2022.10.004 · Cited by 22
Protein nanoparticles as natural drugs carriers for cancer therapy
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“Normal cells are differentiated to restore their homeostatic environments to restore redox equilibrium by antioxidant enzymes or other intake antioxidant agents (Kirtonia et al. 2020).”
Background
Targeting cGAS/STING signaling-mediated myeloid immune cell dysfunction in TIME
Kumar, V., Bauer, C., & Stewart, J. H. (2023) · Journal of Biomedical Science · doi:10.1186/s12929-023-00942-2 · Cited by 23
20-Hydroxyecdysone Confers Antioxidant and Antineoplastic Properties in Human Non-Small Cell Lung Cancer Cells
Shuvalov, O., Kirdeeva, Y., Fefilova, E., Netsvetay, S., Zorin, M., Vlasova, Y., Fedorova, O., Daks, A., Parfenyev, S., & Barlev, N. (2023) · Metabolites · doi:10.3390/metabo13050656 · Cited by 21
“ROS are known to play a multifaced, opposing role in cancer, by favoring cancer onset at low doses on the one hand, and killing tumors at high doses on the other hand [29,55].”
Background
Antineoplastic with DNA fragmentation assay and anti-oxidant, anti-inflammatory with gene expression activity of Lactobacillus plantarum isolated from local Egyptian milk products
Elhalik, M. A., Mekky, A. E., Khedr, M., & Suleiman, W. B. (2024) · BMC Microbiology · doi:10.1186/s12866-024-03576-y · Cited by 21
“However, an overabundance of ROS can lead to a multitude of pathological conditions, including DNA damage, carcinogenesis, and cellular degeneration, potentially triggering diseases like cancer, inflammation, lung injury, and other disorders [14, 15].”
Background
Astaxanthin protects tilapia head kidney cells against polystyrene microplastics-induced inflammation through MAPK and NF-κB signaling pathways
Deng, W., Yang, T., Dong, R., Yan, Y., & Jiang, Q. (2023) · Aquaculture · doi:10.1016/j.aquaculture.2023.739686 · Cited by 22
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Sparstolonin B exerts beneficial effects on prostate cancer by acting on the reactive oxygen species‐mediated PI3K/AKT pathway
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“Cancer development and metastasis are both aided by the stimulation of nuclear factor-kB signaling (NF-kB) by reactive oxygen species (ROS) [9].”
Background
Fangchinoline abrogates growth and survival of hepatocellular carcinoma by negative regulation of c‐met/HGF and its associated downstream signaling pathways
Jung, Y. Y., Um, J., Sethi, G., & Ahn, K. S. (2022) · Phytotherapy Research · doi:10.1002/ptr.7573 · Cited by 20
“(Dai et al., 2017; Ko et al., 2017).”
Self-citation
Reactive Oxygen Species Enlightened Therapeutic Strategy for Oral and Maxillofacial Diseases—Art of Destruction and Reconstruction
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“The imbalance between the elimination and generation of reactive oxygen species (ROS) is considered to be the main cause of various human diseases [1].”
Background
Porphyromonas gingivalis promotes malignancy and chemo-resistance via GSK3β-mediated mitochondrial oxidative phosphorylation in human esophageal squamous cell carcinoma
Liu, Y., Zhou, F., Yang, H., Zhang, Z., Zhang, J., He, K., Qian, M., Li, R., Sun, W., Dai, N., et al. (2023) · Translational Oncology · doi:10.1016/j.tranon.2023.101656 · Cited by 20
Blockage of the JAK/STAT3 signaling pathway in multiple myeloma by leelamine
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Self-citation
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Pharmacological Insights: Mitochondrial ROS Generation by FNC (Azvudine) in Dalton’s Lymphoma Cells Revealed by Super Resolution Imaging
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“The ability of nucleoside analogs to induce ROS has recently gained attention as an important mechanism underlying their anticancer effects [2, 3].”
Influential
Juglone triggers apoptosis of non-small cell lung cancer through the reactive oxygen species -mediated PI3K/Akt pathway
Zhong, J. Q., Hua, Y., Zou, S., & Wang, B. (2024) · PLoS ONE · doi:10.1371/journal.pone.0299921 · Cited by 19
“Collectively, these results indicate that the generation of ROS by juglone plays an important role in the apoptosis and acts as an upstream regulator of PI3K/Akt pathway in NSCLC cells, which is consistent with many FDA-approved anti-neoplastic drugs in clinical applications [44].”
Result
FeSA‐Ir/Metallene Nanozymes Induce Sequential Ferroptosis‐Pyroptosis for Multi‐Immunogenic Responses Against Lung Metastasis
Yang, B., Cao, L., Ge, K., Lv, C., Zhao, Z., Zheng, T., Gao, S., Zhang, J., Wang, T., Jiang, J., et al. (2024) · Small · doi:10.1002/smll.202401110 · Cited by 20
Amplifying glioblastoma immunotherapy: T cell shielding through Nitric oxide/reactive oxygen species scavenging nanoparticles Potentiates anti-PD-1
Lee, J., Kang, Y., Lee, H., Saravanakumar, G., Park, S. A., Ahn, S., & Kim, W. J. (2024) · Biomaterials · doi:10.1016/j.biomaterials.2024.122904 · Cited by 18
Regulation of apoptosis and autophagy by albendazole in human colon adenocarcinoma cells
Jung, Y. Y., Baek, S. H., Ha, I. J., & Ahn, K. S. (2022) · Biochimie · doi:10.1016/j.biochi.2022.04.014 · Cited by 20
The Emerging Roles of Human Gut Microbiota in Gastrointestinal Cancer
Guo, Q., Qin, H., Liu, X., Zhang, X., Chen, Z., Qin, T., Chang, L., & Zhang, W. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.915047 · Cited by 21
“A previous study has confirmed that LAB can induce the generation of reactive oxygen species (41) which initiates cancer angiogenesis, metastasis, and survival under individual concentrations (42).”
Background
Ferroptosis: opening up potential targets for gastric cancer treatment
Li, Y., Liu, J., Wu, S., Xiao, J., & Zhang, Z. (2023) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-023-04886-x · Cited by 18
“These pathways' abnormal activation is crucial for the development, growth, and progression of tumors [44].”
Loss of Myo19 increases metastasis by enhancing microenvironmental ROS gradient and chemotaxis
Ren, X., Shi, P., Su, J., Wei, T., Li, J., Hu, Y., & Wu, C. (2024) · EMBO Reports · doi:10.1038/s44319-023-00052-y · Cited by 18
“ROS, which are considered as double-edge swords, are involved in tumor initiation, proliferation, invasion and angiogenesis [9] .”
DHCR24 in Tumor Diagnosis and Treatment: A Comprehensive Review
Fu, X., & Wang, Z. (2024) · Technology in Cancer Research & Treatment · doi:10.1177/15330338241259780 · Cited by 18
“Interestingly, Ras is immobilized on lipid rafts and activated by multiple factors, such as ROS, 143,144 and activated Ras further affects Mdm2 phosphorylation through the PI3K-AKT pathway.”
Background
Nanoliposomes as nonviral vectors in cancer gene therapy
Yildiz, Ş., Entezari, M., Paskeh, M. D. A., Mirzaei, S., Kalbasi, A., Zabolian, A., Hashemi, F., Hushmandi, K., Hashemi, M., Raei, M., et al. (2024) · MedComm · doi:10.1002/mco2.583 · Cited by 18
“113,114 117 Various redox-responsive nanocarriers have been developed for cancer therapy to prolong their time in circulation and provide degradation after internalization, thus facilitating the drug and gene delivery.”
Background
Pyrimethamine Modulates Interplay between Apoptosis and Autophagy in Chronic Myelogenous Leukemia Cells
Jung, Y. Y., Kim, C., Ha, I. J., Lee, S., Lee, J., Um, J., & Ahn, K. S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158147 · Cited by 17
Ferroptosis: Iron-mediated cell death linked to disease pathogenesis
Zhang, X., Hu, Y., Wang, B., & Yang, S. (2024) · Journal of Biomedical Research · doi:10.7555/jbr.37.20230224 · Cited by 18
Mitochondrial targeting half-sandwich iridium(III) and ruthenium(II) dppf complexes and in vitro anticancer assay
Liu, J., Wu, Y., Yang, G. H., Liu, Z., & Liu, X. (2022) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2022.112069 · Cited by 17
In vivo optical imaging of reactive oxygen species (ROS)-related non-cancerous diseases
Gu, W., Li, S., Yang, Y., Wang, S., Li, K., Zhao, Y., Mu, J., & Chen, X. S. (2023) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2023.117360 · Cited by 17
Ferroptosis in head and neck squamous cell carcinoma: from pathogenesis to treatment
Yang, J., & Gu, Z. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1283465 · Cited by 19
“RT can damage DNA and inhibit GSH production, thereby promoting GPX4-mediated ferroptosis (Kirtonia et al., 2020).”
Background

Authors: Kirtonia, A., Sethi, G., & Garg, M.
Affiliations: Amity University (IN)
National University of Singapore (SG)
Corresponding author: Sethi, Gautam
Garg, Manoj
ORCID: Kirtonia, Anuradha
Sethi, Gautam
Garg, Manoj
Venue: Cellular and Molecular Life Sciences
Publisher: Springer Science and Business Media LLC
Published: 2020-05-01
Volume: 77
Issue: 22
Pages: 4459-4483
ISSN: 1420-682X (ISSN-L)
1420-9071
DOI: 10.1007/s00018-020-03536-5
PMC: PMC11105050
OpenAlex: W3022746266
Cited by: 452
References: 257
Citations by year: 2026: 33 · 2025: 45 · 2024: 90 · 2023: 72 · 2022: 106 · 2021: 80 · 2020: 26
FWCI: 6.79
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Cellular and Molecular Life Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Department of Biotechnology , Ministry of Science and Technology
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cancer and biochemical research
Health Sciences › Medicine › Biochemistry (medical) › Antioxidant Activity and Oxidative Stress
Keywords: reactive oxygen species, carcinogenesis, redox homeostasis, oxidative stress, metastasis, angiogenesis, oncogenic signaling, DNA mutations, tumor microenvironment, cancer stem cells, drug resistance, anticancer agents, immunotherapy, radiotherapy, chemotherapy
MeSH terms: Animals, Humans, Neoplasm Recurrence, Local, Neoplasms, Oxidation-Reduction, Signal Transduction, Reactive Oxygen Species, Oxidative Stress, Carcinogenesis

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The multifaceted role of reactive oxygen species in tumorigenesis

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