DOI: http://dx.doi.org/10.18203/2320-6012.ijrms20170618

Role of oxidative stress in facilitating carcinogenesis

Venkateswaran Natarajan

Abstract


The carcinogenic role of ROS has been a great debate in the past and will be in the future. ROS is produced by both internal (inflammation) and external sources (UV). ROS is important for various important signalling mechanisms for the normal cellular survival. Even though literature exists to support the role of ROS in cancer, the magnitude of its expression and cell type it is expressed will determine whether it plays a positive (apoptosis) or negative role (genomic instability) in cancer. Apart from inducing DNA damage, ROS facilitates carcinogenesis by regulating cell cycle progression, gap junction, inflammation etc. The present review updates the recent discoveries of how ROS regulates these important cellular signalling mechanisms to facilitate carcinogenesis.


Keywords


Bystander effects, Cell cycle, DNA damage, Inflammation, ROS

Full Text:

PDF

References


Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA. Cancer J. Clin. 2016;66:7-30.

Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA. Cancer J. Clin. 2015;65:5-29.

Tyagi N, Arora S, Deshmukh SK, Singh S, Marimuthu S, Singh AP. Exploiting Nanotechnology for the Development of MicroRNA-Based Cancer Therapeutics. J. Biomed. Nanotechnol. 2016;12:28-42.

Deshmukh SK, Srivastava SK, Bhardwaj A, Singh AP, Tyagi N, Marimuthu S, et al. Resistin and interleukin-6 exhibit racially-disparate expression in breast cancer patients, display molecular association and promote growth and aggressiveness of tumor cells through STAT3 activation. Oncotarget. 2015;6:11231-41.

Tyagi N, Marimuthu S, Bhardwaj A, Deshmukh SK, Srivastava SK, Singh G, et al. Activated kinase 4 (PAK4) maintains stem cell-like phenotypes in pancreatic cancer cells through activation of STAT3 signaling. Cancer Lett. 2016;370:260-7.

Tyagi N, Bhardwaj A, Srivastava SK, Arora S, Marimuthu S, Deshmukh SK, et al. Development and Characterization of a Novel in vitro Progression Model for UVB-Induced Skin Carcinogenesis. Sci. Rep. 2015;5:13894.

Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57-70.

Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646-74.

Pelicano H, Carney D, Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist. Updat. Rev. Comment. Antimicrob. Anticancer Chemother. 2004;7:97-110.

Sabharwal SS, Schumacker PT. Mitochondrial ROS in cancer: initiators, amplifiers or an Achilles’ heel? Nat. Rev. Cancer. 2014;14:709-21.

Waris G, Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J. Carcinog. 2006;5:14.

Sullivan LB, Chandel NS. Mitochondrial reactive oxygen species and cancer. Cancer Metab. 2014;2:17.

Lu CY, Lee HC, Fahn HJ, Wei YH. Oxidative damage elicited by imbalance of free radical scavenging enzymes is associated with large-scale mtDNA deletions in aging human skin. Mutat. Res. 1999;423:11-21.

Halliwell B. Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am. J. Med. 1991;91:14S-22S.

Barzilai A, Rotman G, Shiloh Y. ATM deficiency and oxidative stress: a new dimension of defective response to DNA damage. DNA Repair. 2002;1:3-25.

Zimmerman R, Cerutti P. Active oxygen acts as a promoter of transformation in mouse embryo C3H/10T1/2/C18 fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 1984;81:2085-7.

Chinnadurai M, Chidambaram S, Ganesan V, Baraneedharan U, Sundaram L, Paul SFD, et al. Bleomycin, neocarzinostatin and ionising radiation-induced bystander effects in normal diploid human lung fibroblasts, bone marrow mesenchymal stem cells, lung adenocarcinoma cells and peripheral blood lymphocytes. Int. J. Radiat. Biol. 2011;87:673-82.

Chinnadurai M, Rao BS, Deepika R, Paul SF, Venkatachalam P. Role of reactive oxygen species and nitric oxide in mediating chemotherapeutic drug induced bystander response in human cancer cells exposed in-vitro. World J. Oncol. 2012;3:64-72.

Chinnadurai M, Paul SFD, Venkatachalam P. The effect of growth architecture on the induction and decay of bleomycin and X-ray-induced bystander response and genomic instability in lung adenocarcinoma cells and blood lymphocytes. Int. J. Radiat. Biol. 2013;89:69-78.

Basheerudeen SAS, Mani C, Kulkarni MAK, Pillai K, Rajan A, Venkatachalam P. Human brain glioblastoma cells do not induce but do respond to the bleomycin-induced bystander response from lung adenocarcinoma cells. Mutat. Res. 2013;757:114-9.

Szatrowski TP, Nathan CF. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991;51:794-8.

Zhou Y, Hileman EO, Plunkett W, Keating MJ, Huang P. Free radical stress in chronic lymphocytic leukemia cells and its role in cellular sensitivity to ROS-generating anticancer agents. Blood. 2003;101:4098-104.

Cerimele F, Battle T, Lynch R, Frank DA, Murad E, Cohen C, et al. Reactive oxygen signaling and MAPK activation distinguish Epstein-Barr Virus (EBV)-positive versus EBV-negative Burkitt’s lymphoma. Proc. Natl. Acad. Sci. U. S. A. 2005;102:175-9.

Flores-López LA, Martínez-Hernández MG, Viedma-Rodríguez R, Díaz-Flores M, Baiza-Gutman LA. High glucose and insulin enhance uPA expression, ROS formation and invasiveness in breast cancer-derived cells. Cell. Oncol. Dordr. 2016;39:365-78.

Ding S, Li C, Cheng N, Cui X, Xu X, Zhou G. Redox Regulation in Cancer Stem Cells. Oxid. Med. Cell. Longev. 2015;2015:750798.

Li JM, Brooks G. Cell cycle regulatory molecules (cyclins, cyclin-dependent kinases and cyclin-dependent kinase inhibitors) and the cardiovascular system; potential targets for therapy? Eur. Heart J. 1999;20:406-20.

Verbon EH, Post JA, Boonstra J. The influence of reactive oxygen species on cell cycle progression in mammalian cells. Gene. 2012;511:1-6.

Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, et al. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science. 1997;275:1649-52.

Bijur GN, Briggs B, Hitchcock CL, Williams MV. Ascorbic acid-dehydroascorbate induces cell cycle arrest at G2/M DNA damage checkpoint during oxidative stress. Environ. Mol. Mutagen. 1999;33:144-52.

Laparra JM, Vélez D, Barberá R, Farré R, Montoro R. As2O3-induced oxidative stress and cycle progression in a human intestinal epithelial cell line (Caco-2). Toxicol. Vitro Int. J. Publ. Assoc. BIBRA. 2008;22:444-9.

D’Angiolella V, Santarpia C, Grieco D. Oxidative stress overrides the spindle checkpoint. Cell Cycle Georget. Tex.l 2007;6:576-9.

Poehlmann A, Reissig K, Schönfeld P, Walluscheck D, Schinlauer A, Hartig, et al. Repeated H2 O2 exposure drives cell cycle progression in an in vitro model of ulcerative colitis. J. Cell. Mol. Med. 2013;17:1619-31.

Gamou S, Shimizu N. Hydrogen peroxide preferentially enhances the tyrosine phosphorylation of epidermal growth factor receptor. FEBS Lett. 1995;357:161-4.

de Wit R, Capello A, Boonstra J, Verkleij AJ, Post JA. Hydrogen peroxide inhibits epidermal growth factor receptor internalization in human fibroblasts. Free Radic. Biol. Med. 2000;28:28-38.

Mosher DF, Fogerty FJ, Chernousov MA, Barry EL. Assembly of fibronectin into extracellular matrix. Ann. N. Y. Acad. Sci. 1991;614:167-80.

Edwards GO, Botchway SW, Hirst G, Wharton CW, Chipman JK, Meldrum RA. Gap junction communication dynamics and bystander effects from ultrasoft X-rays. Br. J. Cancer. 2004;90:1450-6.

Azzam EI, de Toledo SM, Little JB. Direct evidence for the participation of gap junction-mediated intercellular communication in the transmission of damage signals from alpha -particle irradiated to nonirradiated cells. Proc. Natl. Acad. Sci. U. S. A. 2001;8:473-8.

Klaunig JE, Kamendulis LM. The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 2004;44:239-67.

Autsavapromporn N, de Toledo SM, Little JB, Jay-Gerin JP, Harris AL, Azzam EI. The role of gap junction communication and oxidative stress in the propagation of toxic effects among high-dose α-particle-irradiated human cells. Radiat. Res. 2011;175:347-57.

Choudhary M, Naczki C, Chen W, Barlow KD, Case LD, Metheny-Barlow LJ. Tumor-induced loss of mural Connexin 43 gap junction activity promotes endothelial proliferation. BMC Cancer. 2015;15:427.

Rakiman I, Chinnadurai M, Baraneedharan U, Paul SFD, Venkatachalam P. γ-H2AX assay: a technique to quantify DNA double strand breaks. Adv Biotech. 2008;39-41.

Tripathi K, Mani C, Clark DW, Palle K. Rad18 is required for functional interactions between FANCD2, BRCA2, and Rad51 to repair DNA topoisomerase 1-poisons induced lesions and promote fork recovery. Oncotarget. 2016;7:12537-53.

Tripathi K, Mani C, Somasagara RR, Clark DW, Ananthapur V, Vinaya K, et al. Detection and evaluation of estrogen DNA-adducts and their carcinogenic effects in cultured human cells using biotinylated estradiol. Mol. Carcinog. 2016.

Vartanian V, Lowell B, Minko IG, Wood TG, Ceci JD, George, et al. The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase. Proc. Natl. Acad. Sci. U. S. A. 2006;103:1864-9.

Mostoslavsky R, Chua KF, Lombard DB, Pang WW, Fischer MR, Gellon L, et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell. 2006;124:315-29.

Sato K, Ito K, Kohara H, Yamaguchi Y, Adachi K, Endo H. Negative regulation of catalase gene expression in hepatoma cells. Mol. Cell. Biol. 1992;12:2525-33.

Karihtala P, Soini Y. Reactive oxygen species and antioxidant mechanisms in human tissues and their relation to malignancies. APMIS Acta Pathol. Microbiol. Immunol. Scand. 2007;115:81-103.

Curtis CD, Thorngren DL, Nardulli AM. Immunohistochemical analysis of oxidative stress and DNA repair proteins in normal mammary and breast cancer tissues. BMC Cancer. 2010;10:9.

Zienolddiny S, Ryberg D, Haugen A. Induction of microsatellite mutations by oxidative agents in human lung cancer cell lines. Carcinogenesis. 2000;21:1521-6.

Stich HF, Anders F. The involvement of reactive oxygen species in oral cancers of betel quid/tobacco chewers. Mutat. Res. 1989;214:47-61.

Perrone S, Lotti F, Geronzi U, Guidoni E, Longini M, Buonocore G. Oxidative Stress in Cancer-Prone Genetic Diseases in Pediatric Age: The Role of Mitochondrial Dysfunction. Oxid. Med. Cell. Longev. 2016;4782426.

Lee CH, Yu HS. Role of mitochondria, ROS, and DNA damage in arsenic induced carcinogenesis. Front. Biosci. Sch. Ed. 2016;8:312-20.

Tripathi K, Mani C, Barnett R, Nalluri S, Bachaboina L, Rocconi RP, et al. Gli1 protein regulates the S-phase checkpoint in tumor cells via Bid protein, and its inhibition sensitizes to DNA topoisomerase 1 inhibitors. J. Biol. Chem. 2014;289:31513-25.

Palle K, Mani C, Tripathi K, Athar M. Aberrant GLI1 Activation in DNA Damage Response, Carcinogenesis and Chemoresistance. Cancers. 2015;7:2330-1.

Kohchi C, Inagawa H, Nishizawa T, Soma GI. ROS and innate immunity. Anticancer Res. 2009;29:817–21.

Theys J, Lambin P. Clostridium to treat cancer: dream or reality? Ann. Transl. Med. 2015;3:S21.

Rossow HA, Calvert CC. Computer modeling of obesity links theoretical energetic measures with experimental measures of fuel use for lean and obese men. J. Nutr. 2014;144:1650-7.

Chhabra G, Sharma P, Anant A, Deshmukh S, Kaushik H, Gopal K, et al. Identification and modeling of a drug target for Clostridium perfringens SM101. Bioinformation. 2010;4:278–89.

Mathur DD, Deshmukh S, Kaushik H, Garg LC. Functional and structural characterization of soluble recombinant epsilon toxin of Clostridium perfringens D, causative agent of enterotoxaemia. Appl. Microbiol. Biotechnol. 2010;88:877-84.

Kaushik H, Deshmukh S, Mathur DD, Tiwari A, Garg LC. Recombinant expression of in silico identified Bcell epitope of epsilon toxin of Clostridium perfringens in translational fusion with a carrier protein. Bioinformation. 2013;9:617-21.

Spooner R, Yilmaz O. The role of reactive-oxygen-species in microbial persistence and inflammation. Int. J. Mol. Sci. 2011;12:334-52.

Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic. Res. 2010;44:479-96.

Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic. Biol. Med. 2010;49:1603-16.

Grivennikov SI, Karin M. Inflammation and oncogenesis: a vicious connection. Curr. Opin. Genet. Dev. 2010;20:65-71.

Roque AT, Gambeloni RZ, Felitti S, Ribeiro ML, Santos JC. Inflammation-induced oxidative stress in breast cancer patients. Med. Oncol. Northwood Lond. Engl. 2015;32:263.

Charlton BM, Rich-Edwards JW, Colditz GA, Missmer SA, Rosner BA, Hankinson, et al. Oral contraceptive use and mortality after 36 years of follow-up in the Nurses’ Health Study: prospective cohort study. BMJ. 2014;349:6356.

Perše M. Oxidative stress in the pathogenesis of colorectal cancer: cause or consequence? BioMed Res. Int. 2013:725710.

Hardikar S, Onstad L, Song X, Wilson AM, Montine TJ, et al. Inflammation and oxidative stress markers and esophageal adenocarcinoma incidence in a Barrett’s esophagus cohort. Cancer Epidemiol. Biomark. Prev. Publ. Am. Assoc. Cancer Res. Cosponsored Am. Soc. Prev. Oncol. 2014;23:2393-403.

Jackson JR, Seed MP, Kircher CH, Willoughby DA, Winkler JD. The codependence of angiogenesis and chronic inflammation. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 1997;11:457-65.

Ishibashi T. Molecular hydrogen: new antioxidant and anti-inflammatory therapy for rheumatoid arthritis and related diseases. Curr. Pharm. Des. 2013;19:6375-81.

Li Z, Geng YN, Jiang JD, Kong WJ. Antioxidant and anti-inflammatory activities of berberine in the treatment of diabetes mellitus. Evid.-Based Complement. Altern. Med. ECAM. 2014:289264.