Oxidative stress and gender disparity in cancer

References

• Yang HY, Huang JH, Hsu CY, et al. Gender differences and the trend in the acute myocardial infarction: a 10-year nationwide population-based analysis. Sci World J. 2012;2012:1–11.
   Google Scholar
• Benjamin EJ, Muntner P, Alonso A, et al. Heart disease and stroke statistics-2019 update: A report from the American Heart Association. Circulation. 2019;139(10):e56–e528.
   PubMed Web of Science ®Google Scholar
• Reczek CR, Birsoy K, Kong H, et al. A CRISPR screen identifies a pathway required for paraquat-induced cell death. Nat Chem Biol. 2017;13(12):1274–1279.
   PubMed Web of Science ®Google Scholar
• Dodson M, Castro-Portuguez R, Zhang DD. NRF2 plays a critical role in mitigating lipid peroxidation and ferroptosis. Redox Biol. 2019;23:101107.
   PubMed Web of Science ®Google Scholar
• Redza-Dutordoir M, Averill-Bates DA. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta. 2016;1863(12):2977–2992.
   PubMed Web of Science ®Google Scholar
• Austad SN, Fischer KE. Sex differences in lifespan. Cell Metab. 2016;23(6):1022–1033.
   PubMed Web of Science ®Google Scholar
• Zarulli V, Barthold Jones JA, Oksuzyan A, et al. Women live longer than men even during severe famines and epidemics. Proc Natl Acad Sci USA. 2018;115(4):E832–E840.
   PubMed Web of Science ®Google Scholar
• Lavoie JC, Tremblay A. Sex-specificity of oxidative stress in newborns leading to a personalized antioxidant nutritive strategy. Antioxidants. 2018;7(4):49.
   Web of Science ®Google Scholar
• Kander MC, Cui Y, Liu Z. Gender difference in oxidative stress: a new look at the mechanisms for cardiovascular diseases. J Cell Mol Med. 2017;21(5):1024–1032.
   PubMed Web of Science ®Google Scholar
• Borras C, Sastre J, Garcia-Sala D, et al. Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med. 2003;34(5):546–552.
   PubMed Web of Science ®Google Scholar
• Viña J, Sastre J, Pallardó FV, et al. Role of mitochondrial oxidative stress to explain the different longevity between genders: protective effect of estrogens. Free Radic Res. 2006;40(12):1359–1365.
   PubMed Web of Science ®Google Scholar
• Ide T, Tsutsui H, Ohashi N, et al. Greater oxidative stress in healthy young men compared with premenopausal women. ATVB. 2002;22(3):438–442.
   Google Scholar
• Dorak MT, Karpuzoglu E. Gender differences in cancer susceptibility: an inadequately addressed issue. Front Genet. 2012;3:268.
   PubMedGoogle Scholar
• Kim HI, Lim H, Moon A. Sex differences in cancer: epidemiology, genetics and therapy. Biomol Ther. 2018;26(4):335–342.
   PubMed Web of Science ®Google Scholar
• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA A Cancer J Clin. 2020;70(1):7–30.
   PubMed Web of Science ®Google Scholar
• Locker GY, Hamilton S, Harris J, et al. ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. J Clin Oncol. 2006;24(33):5313–5327.
   PubMed Web of Science ®Google Scholar
• Hayyan M, Hashim MA, AlNashef IM. Superoxide ion: generation and chemical implications. Chem Rev. 2016;116(5):3029–3085.
   PubMed Web of Science ®Google Scholar
• Niemann B, Rohrbach S, Miller MR, et al. Oxidative stress and cardiovascular risk: obesity, diabetes, smoking, and pollution: part 3 of a 3-part series. J Am Coll Cardiol. 2017;70(2):230–251.
   PubMed Web of Science ®Google Scholar
• Deavall DG, Martin EA, Horner JM, et al. Drug-induced oxidative stress and toxicity. J Toxicol. 2012;2012:645460.
   PubMedGoogle Scholar
• Yamamori T, Yasui H, Yamazumi M, et al. Ionizing radiation induces mitochondrial reactive oxygen species production accompanied by upregulation of mitochondrial electron transport chain function and mitochondrial content under control of the cell cycle checkpoint. Free Radic Biol Med. 2012;53(2):260–270.
   PubMed Web of Science ®Google Scholar
• Eriksson SE, Ceder S, Bykov VJN, et al. p53 as a hub in cellular redox regulation and therapeutic target in cancer. J Mol Cell Biol. 2019;11(4):330–341.
   PubMed Web of Science ®Google Scholar
• O'Flaherty C, Matsushita-Fournier D. Reactive oxygen species and protein modifications in spermatozoa. Biol Reprod. 2017;97(4):577–585.
   PubMed Web of Science ®Google Scholar
• Koppers AJ, Garg ML, Aitken RJ. Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa. Free Radic Biol Med. 2010;48(1):112–119.
   PubMed Web of Science ®Google Scholar
• Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. 5th ed. England: Oxford University Press; 2015.
   Google Scholar
• Sanchez-Alvarez M, Strippoli R, Donadelli M, et al. Sestrins as a therapeutic bridge between ROS and autophagy in cancer. Cancers. 2019;11(10):1415.
   Web of Science ®Google Scholar
• Rhee SG, Bae SH. The antioxidant function of sestrins is mediated by promotion of autophagic degradation of Keap1 and Nrf2 activation and by inhibition of mTORC1. Free Radic Biol Med. 2015;88(Pt B):205–211.
   PubMed Web of Science ®Google Scholar
• Kuehne A, Emmert H, Soehle J, et al. Acute activation of oxidative pentose phosphate pathway as first-line response to oxidative stress in human skin cells. Mol Cell. 2015;59(3):359–371.
   PubMed Web of Science ®Google Scholar
• Cosentino C, Grieco D, Costanzo V. ATM activates the pentose phosphate pathway promoting anti-oxidant defence and DNA repair. EMBO J. 2011;30(3):546–555.
   PubMed Web of Science ®Google Scholar
• van der Reest J, Lilla S, Zheng L, et al. Proteome-wide analysis of cysteine oxidation reveals metabolic sensitivity to redox stress. Nat Commun. 2018;9(1):1581.
   PubMedGoogle Scholar
• Lee G, Won HS, Lee YM, et al. Oxidative dimerization of PHD2 is responsible for its inactivation and contributes to metabolic reprogramming via HIF-1α Activation. Sci Rep. 2016;6:18928.
   PubMed Web of Science ®Google Scholar
• Zheng L, Cardaci S, Jerby L, et al. Fumarate induces redox-dependent senescence by modifying glutathione metabolism. Nat Commun. 2015;6(5):6001.
   PubMedGoogle Scholar
• Liu D, Xu Y. p53, oxidative stress, and aging. Antioxid Redox Signal. 2011;15(6):1669–1678.
   PubMed Web of Science ®Google Scholar
• Chen D, Tavana O, Chu B, et al. NRF2 is a major target of ARF in p53-independent tumor suppression. Mol Cell. 2017;68(1):224–232.
   PubMed Web of Science ®Google Scholar
• Rose Li Y, Halliwill KD, Adams CJ, et al. Mutational signatures in tumours induced by high and low energy radiation in Trp53 deficient mice. Nat Commun. 2020;11(1):394.
   PubMed Web of Science ®Google Scholar
• Gill JG, Piskounova E, Morrison SJ. Cancer, oxidative stress, and metastasis. Cold Spring Harb Symp Quant Biol. 2016;81:163–175.
   PubMedGoogle Scholar
• Neumann CA, Krause DS, Carman CV, et al. Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature. 2003;424(6948):561–565.
   PubMed Web of Science ®Google Scholar
• Chong SJF, Lai JXH, Eu JQ, et al. Reactive oxygen species and oncoprotein signaling-a dangerous liaison. Antioxid Redox Signal. 2018;29(16):1553–1588.
   PubMed Web of Science ®Google Scholar
• Igelmann S, Neubauer HA, Ferbeyre G. STAT3 and STAT5 activation in solid cancers. Cancers. 2019;11(10):1428.
   Web of Science ®Google Scholar
• Liou GY, Doppler H, DelGiorno KE, et al. Mutant KRas-induced mitochondrial oxidative stress in acinar cells upregulates EGFR signaling to drive formation of pancreatic precancerous lesions. Cell Rep. 2016;14(10):2325–2336.
   PubMed Web of Science ®Google Scholar
• Marcar L, Bardhan K, Gheorghiu L, et al. Acquired resistance of EGFR-mutated lung cancer to tyrosine kinase inhibitor treatment promotes PARP inhibitor sensitivity. Cell Rep. 2019;27(12):3422–3432.e4.
   PubMed Web of Science ®Google Scholar
• Satoh K, Yachida S, Sugimoto M, et al. Global metabolic reprogramming of colorectal cancer occurs at adenoma stage and is induced by MYC. Proc Natl Acad Sci USA. 2017;114(37):E7697–E7706.
   PubMed Web of Science ®Google Scholar
• Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov. 2013;12(12):931–947.
   PubMed Web of Science ®Google Scholar
• He C, Danes JM, Hart PC, et al. SOD2 acetylation on lysine 68 promotes stem cell reprogramming in breast cancer. Proc Natl Acad Sci USA. 2019;116(47):23534–23541.
   PubMed Web of Science ®Google Scholar
• Moloney JN, Cotter TG. ROS signalling in the biology of cancer. Semin Cell Dev Biol. 2018;80:50–64.
   PubMed Web of Science ®Google Scholar
• Dongre A, Weinberg RA. New insights into the mechanisms of epithelial-mesenchymal transition and implications for cancer. Nat Rev Mol Cell Biol. 2019;20(2):69–84.
   PubMed Web of Science ®Google Scholar
• El-Kenawi A, Hänggi K, Ruffell B. The immune microenvironment and cancer metastasis. Cold Spring Harb Perspect Med. 2020;10(4):a037424.
   PubMed Web of Science ®Google Scholar
• Chaffer CL, San Juan BP, Lim E, et al. EMT, cell plasticity and metastasis. Cancer Metastasis Rev. 2016;35(4):645–654.
   PubMed Web of Science ®Google Scholar
• Jiang J, Wang K, Chen Y, et al. Redox regulation in tumor cell epithelial-mesenchymal transition: molecular basis and therapeutic strategy. Signal Transduct Target Ther. 2017;2:17036.
   PubMed Web of Science ®Google Scholar
• Haley JA, Ruiz CF, Montal ED, et al. Decoupling of Nrf2 expression promotes mesenchymal state maintenance in non-small cell lung cancer. Cancers. 2019;11(10):1488.
   Web of Science ®Google Scholar
• Muthuramalingam K, Cho M, Kim Y. Role of NAPDH oxidase and its therapeutic intervention in TGF-β-mediated EMT progression: an in vitro analysis on HeLa cervical cancer cells. Appl Biol Chem. 2020;63(1):4.
   Web of Science ®Google Scholar
• Ma M, Shi F, Zhai R, et al. TGF-β promote epithelial-mesenchymal transition via NF-κB/NOX4/ROS signal pathway in lung cancer cells. Mol Biol Rep. 2021;48(3):2365–2375.
   PubMed Web of Science ®Google Scholar
• Subramani R, Gonzalez E, Arumugam A, et al. Nimbolide inhibits pancreatic cancer growth and metastasis through ROS-mediated apoptosis and inhibition of epithelial-to-mesenchymal transition. Sci Rep. 2016;6(1):19819.
   PubMedGoogle Scholar
• Lu W, Kang Y. Epithelial-mesenchymal plasticity in cancer progression and metastasis. Dev Cell. 2019;49(3):361–374.
   PubMed Web of Science ®Google Scholar
• Cheung EC, DeNicola GM, Nixon C, et al. Dynamic ROS control by TIGAR regulates the initiation and progression of pancreatic cancer. Cancer Cell. 2020;37(2):168–182.e4.
   PubMed Web of Science ®Google Scholar
• Porporato PE, Payen VL, Perez-Escuredo J, et al. A mitochondrial switch promotes tumor metastasis. Cell Rep. 2014;8(3):754–766.
   PubMed Web of Science ®Google Scholar
• Goh J, Enns L, Fatemie S, et al. Mitochondrial targeted catalase suppresses invasive breast cancer in mice. BMC Cancer. 2011;11:191.
   PubMed Web of Science ®Google Scholar
• Bagati A, Moparthy S, Fink EE, et al. KLF9-dependent ROS regulate melanoma progression in stage-specific manner. Oncogene. 2019;38(19):3585–3597.
   PubMed Web of Science ®Google Scholar
• Wiel C, Le Gal K, Ibrahim MX, et al. BACH1 stabilization by antioxidants stimulates lung cancer metastasis. Cell. 2019;178(2):330–345.e22.
   PubMed Web of Science ®Google Scholar
• Hayes JD, Dinkova-Kostova AT, Tew KD. Oxidative stress in cancer. Cancer Cell. 2020;38(2):167–197.
   PubMed Web of Science ®Google Scholar
• Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249.
   PubMed Web of Science ®Google Scholar
• Mu L, Liu L, Niu R, et al. Indoor air pollution and risk of lung cancer among Chinese female non-smokers. Cancer Causes Control. 2013;24(3):439–450.
   PubMed Web of Science ®Google Scholar
• Turner MC, Andersen ZJ, Baccarelli A, et al. Outdoor air pollution and cancer: an overview of the current evidence and public health recommendations. CA Cancer J Clin. 2020;70(6):460–479.
   Web of Science ®Google Scholar
• Clinton SK, Giovannucci EL, Hursting SD. The world cancer research fund/american institute for cancer research third expert report on diet, nutrition, physical activity, and cancer: Impact and future directions. J Nutr. 2020;150(4):663–671.
   Google Scholar
• Infection with Helicobacter pylori. IARC Monogr Eval Carcinog Risks Hum. 1994;61:177–240.
   PubMedGoogle Scholar
• Herrera V, Parsonnet J. Helicobacter pylori and gastric adenocarcinoma. Clin Microbiol Infect. 2009;15(11):971–976.
   PubMed Web of Science ®Google Scholar
• Zhang X, Zhang P, Mourad AM. Aboul-Soud3 from inflammation to gastric cancer: role of Helicobacter pylori. Oncol Lett. 2017;13(2):543–548.
   PubMed Web of Science ®Google Scholar
• London TW, Petrick JL, McGlynn KA. Liver cancer. In: Thun M, Linet MS, Cerhan JR, Haiman CA, Schottenfeld D, editors. Cancer epidemiology and prevention. 4th ed. England: Oxford University Press; 2018. 635–660.
   Google Scholar
• Patel M, McSorley ST, Park JH, et al. The relationship between right-sided tumour location, tumour microenvironment, systemic inflammation, adjuvant therapy and survival in patients undergoing surgery for colon and rectal cancer. Br J Cancer. 2018;118(5):705–712.
   PubMed Web of Science ®Google Scholar
• Kim SE, Paik HY, Yoon H, et al. Sex-and gender-specific disparities in colorectal cancer risk. World J Gastroenterol. 2015;21(17):5167–5175.
   PubMed Web of Science ®Google Scholar
• Ayala A, Muñoz MF, Argüelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev. 2014;2014:360438.
   PubMed Web of Science ®Google Scholar
• Pizzimenti S, Ciamporcero E, Daga M, et al. Interaction of aldehydes derived from lipid peroxidation and membrane proteins. Front Physiol. 2013;4:242.
   PubMed Web of Science ®Google Scholar
• Tower J, Pomatto L, Davies K. Sex differences in the response to oxidative and proteolytic stress. Redox Biol. 2020;31:101488.
   PubMed Web of Science ®Google Scholar
• Huang S, Ye L, Chen H. Sex determination and maintenance: the role of DMRT1 and FOXL2. Asian J Androl. 2017;19(6):619–624.
   PubMed Web of Science ®Google Scholar
• Tower J. Sex-specific gene expression and life span regulation. Trends Endocrinol Metab. 2017;28(10):735–747.
   PubMed Web of Science ®Google Scholar
• Berletch JB, Ma W, Yang F, et al. Escape from X inactivation varies in mouse tissues. PLOS Genet. 2015;11(3):e1005079.
   PubMed Web of Science ®Google Scholar
• Cotton AM, Price EM, Jones MJ, et al. Landscape of DNA methylation on the X chromosome reflects CpG density, functional chromatin state and X-chromosome inactivation. Hum Mol Genet. 2015;24(6):1528–1539.
   PubMed Web of Science ®Google Scholar
• Tukiainen T, Villani AC, Yen A, et al. Landscape of X chromosome inactivation across human tissues. Nature. 2017;550(7675):244–248.
   PubMed Web of Science ®Google Scholar
• Tower J. Sex-specific regulation of aging and apoptosis. Mech Ageing Dev. 2006;127(9):705–718.
   PubMed Web of Science ®Google Scholar
• Poissant J, Wilson AJ, Coltman DW. Sex-specific genetic variance and the evolution of sexual dimorphism: a systematic review of cross-sex genetic correlations. Evolution. 2010;64(1):97–107.
   PubMed Web of Science ®Google Scholar
• Groß S, Immel U-D, Klintschar M, et al. Germline genetics of the p53 pathway affect longevity in a gender specific manner. CAS. 2014;7(2):91–100.
   Google Scholar
• Fang S, Krahe R, Bachinski LL, et al. Strong, sex-specific effect of the TP53 PIN3 polymorphism on cancer risk in a cohort study of TP53 germline mutation carriers. Hum Genet. 2011;130(6):789–794.
   PubMed Web of Science ®Google Scholar
• Fang S, Krahe R, Lozano G, et al. Effects of MDM2, MDM4 and TP53 codon 72 polymorphisms on cancer risk in a cohort study of carriers of TP53 germline mutations. PLOS One. 2010;5(5):e10813.
   PubMed Web of Science ®Google Scholar
• Tower J. Programmed cell death in aging. Ageing Res Rev. 2015;23(Pt A):90–100.
   PubMedGoogle Scholar
• Torrens-Mas M, Pons DG, Sastre-Serraa J, et al. Sexual hormones regulate the redox status and mitochondrial function in the brain. Pathological implications. Redox Biol. 2020;31:101505.
   PubMed Web of Science ®Google Scholar
• Wu J, Williams D, Walter GA, et al. Estrogen increases Nrf2 activity through activation of the PI3K pathway in MCF-7 breast cancer cells. Exp Cell Res. 2014;328(2):351–360.
   PubMed Web of Science ®Google Scholar
• Ruszkiewicz JA, Miranda-Vizuete A, Tinkov AA, et al. Sex-specific differences in redox homeostasis in brain norm and disease. J Mol Neurosci. 2019;67(2):312–342.
   PubMed Web of Science ®Google Scholar
• Fao L, Mota SI, Rego AC. Shaping the Nrf2-ARE-related pathways in Alzheimer's and Parkinson's diseases. Ageing Res Rev. 2019;54:100942.
   PubMed Web of Science ®Google Scholar
• Pajares M, Cuadrado A, Rojo AI. Modulation of proteostasis by transcription factor NRF2 and impact in neurodegenerative diseases. Redox Biol. 2017;11:543–553.
   PubMed Web of Science ®Google Scholar
• Pomatto LCD, Tower J, Davies KJA. Sexual dimorphism and aging differentially regulate adaptive homeostasis. J Gerontol A Biol Sci Med Sci. 2018;73(2):141–149.
   PubMed Web of Science ®Google Scholar
• Bota DA, Davies KJ. Mitochondrial Lon protease in human disease and aging: Including an etiologic classification of Lon-related diseases and disorders. Free Radic Biol Med. 2016;100:188–198.
   PubMed Web of Science ®Google Scholar
• Oh JY, Choi GE, Lee HJ, et al. 17β-Estradiol protects mesenchymal stem cells against high glucose-induced mitochondrial oxidants production via Nrf2/Sirt3/MnSOD signaling. Free Radic Biol Med. 2019;130:328–342.
   PubMed Web of Science ®Google Scholar
• Panza S, Santoro M, De Amicis F, et al. Estradiol via estrogen receptor beta influences ROS levels through the transcriptional regulation of SIRT3 in human seminoma TCam-2 cells. Tumour Biol. 2017;39(5):1010428317701642.
   Google Scholar
• Shi H, Deng HX, Gius D, et al. Sirt3 protects dopaminergic neurons from mitochondrial oxidative stress. Hum Mol Genet. 2017;26(10):1915–1926.
   PubMed Web of Science ®Google Scholar
• Torres MJ, Kew KA, Ryan TE, et al. 17β-Estradiol directly lowers mitochondrial membrane microviscosity and improves bioenergetic function in skeletal muscle. Cell Metab. 2018;27(1):167–179.e7.
   PubMed Web of Science ®Google Scholar
• Razmara A, Duckles SP, Krause DN, et al. Estrogen suppresses brain mitochondrial oxidative stress in female and male rats. Brain Res. 2007;1176:71–81.
   PubMed Web of Science ®Google Scholar
• Chen J-Q, Cammarata PR, Baines CP, et al. Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. Biochim Biophys Acta. 2009;1793(10):1540–1570.
   PubMed Web of Science ®Google Scholar
• Echtay KS, Bienengraeber M, Mayinger P, et al. Uncoupling proteins: martin Klingenberg's contributions for 40 years. Arch Biochem Biophys. 2018;657:41–55.
   PubMed Web of Science ®Google Scholar
• Sastre-Serra J, Valle A, Company MM, et al. Estrogen down-regulates uncoupling proteins and increases oxidative stress in breast cancer. Free Radic Biol Med. 2010;48(4):506–512.
   PubMed Web of Science ®Google Scholar
• Rodriguez AM, Monjo M, Roca P, et al. Opposite actions of testosterone and progesterone on UCP1 mRNA expression in cultured brown adipocytes. Cell Mol Life Sci. 2002;59(10):1714–1723.
   PubMed Web of Science ®Google Scholar
• Miro AM, Sastre-Serra J, Pons DG, et al. 17β-Estradiol regulates oxidative stress in prostate cancer cell lines according to ERalpha/ERbeta ratio. J Steroid Biochem Mol Biol. 2011;123(3–5):133–139.
   PubMed Web of Science ®Google Scholar
• Valle A, Oliver J, Roca P. Role of uncoupling proteins in cancer. Cancers. 2010;2(2):567–591.
   PubMedGoogle Scholar
• Ali I, Hogberg J, Hsieh JH, et al. Gender differences in cancer susceptibility: role of oxidative stress. Carcinogenesis. 2016;37(10):985–992.
   PubMed Web of Science ®Google Scholar
• Serra C, Sandor NL, Jang H, et al. The effects of testosterone deprivation and supplementation on proteasomal and autophagy activity in the skeletal muscle of the male mouse: differential effects on high-androgen responder and low-androgen responder muscle groups. Endocrinology. 2013;154(12):4594–4606.
   PubMed Web of Science ®Google Scholar
• Lucas-Herald AK, Alves-Lopes R, Montezano AC, et al. Genomic and non-genomic effects of androgens in the cardiovascular system: clinical implications. Clin Sci. 2017;131(13):1405–1418.
   Web of Science ®Google Scholar
• Vasconsuelo A, Pronsato L, Ronda AC, et al. Role of 17β-estradiol and testosterone in apoptosis. Steroids. 2011;76(12):1223–1231.
   PubMed Web of Science ®Google Scholar
• Foradori CD, Weiser MJ, Handa RJ. Non-genomic actions of androgens. Front Neuroendocrinol. 2008;29(2):169–181.
   PubMed Web of Science ®Google Scholar
• Roy AK, Tyagi PK, Song CS, et al. Androgen receptor: structural domains and functional dynamics after ligand-receptor interaction. Ann N Y Acad Sci. 2001;949:44–57.
   PubMed Web of Science ®Google Scholar
• Davey RA, Grossmann M. Androgen receptor structure, function and biology: from bench to bedside. Clin Biochem Rev. 2016;37(1):3–15.
   PubMedGoogle Scholar
• Pierdominici M, Ortona E, Franconi F, et al. Gender specific aspects of cell death in the cardiovascular system. Curr Pharm Des. 2011;17(11):1046–1055.
   PubMed Web of Science ®Google Scholar
• Pronsato L, Milanesi L, Vasconsuelo A, et al. Testosterone modulates FoxO3a and p53-related genes to protect C2C12 skeletal muscle cells against apoptosis. Steroids. 2017;124:35–45.
   PubMed Web of Science ®Google Scholar
• Er F, Michels G, Gassanov N, et al. Testosterone induces cytoprotection by activating ATP-sensitive K+ channels in the cardiac mitochondrial inner membrane. Circulation. 2004;110(19):3100–3107.
   PubMed Web of Science ®Google Scholar
• Zhang L, Wu S, Ruan Y, et al. Testosterone suppresses oxidative stress via androgen receptor-independent pathway in murine cardiomyocytes. Mol Med Rep. 2011;4(6):1183–1188.
   PubMed Web of Science ®Google Scholar
• Szabo R, Borzsei D, Kupai K, et al. Spotlight on a new heme oxygenase pathway: testosterone-induced shifts in cardiac oxidant/antioxidant status. Antioxidants. 2019;8(8):288.
   Web of Science ®Google Scholar
• Lopes RA, Neves KB, Pestana CR, et al. Testosterone induces apoptosis in vascular smooth muscle cells via extrinsic apoptotic pathway with mitochondria-generated reactive oxygen species involvement. Am J Physiol Heart Circ Physiol. 2014;306(11):H1485–H1494.
   PubMed Web of Science ®Google Scholar
• Pavon N, Martinez-Abundis E, Hernandez L, et al. Sexual hormones: effects on cardiac and mitochondrial activity after ischemia-reperfusion in adult rats. Gender difference. J Steroid Biochem Mol Biol. 2012;132(1–2):135–146.
   PubMed Web of Science ®Google Scholar
• Okoh V, Deoraj A, Roy D. Estrogen-induced reactive oxygen species-mediated signalings contribute to breast cancer. Biochim Biophys Acta. 2011;1815(1):115–133.
   PubMed Web of Science ®Google Scholar
• Dos Santos EG, Dieudonne MN, Pecquery R, et al. Rapid nongenomic E2 effects on p42/p44 MAPK, activator protein-1, and cAMP response element binding protein in rat white adipocytes. Endocrinology. 2002;143(3):930–940.
   PubMed Web of Science ®Google Scholar
• Bozinovski S, Jones JE, Vlahos R, et al. Granulocyte/macrophage-colony-stimulating factor (GM-CSF) regulates lung innate immunity to lipopolysaccharide through Akt/Erk activation of NFkappa B and AP-1 in vivo. J Biol Chem. 2002;277(45):42808–42814.
   PubMed Web of Science ®Google Scholar
• Straface E, Malorni W, Pietraforte D. Sex differences in redox biology: a mandatory new point of view approaching human inflammatory diseases. Antioxid Redox Signal. 2017;26(1):44–45.
   PubMed Web of Science ®Google Scholar
• Hayes JD, Ebisine K, Sharma RS, et al. Regulation of the CNC-bZIP transcription factor Nrf2 by Keap1 and the axis between GSK-3 and b-TrCP. Curr Opin Toxicol. 2016;1:92–103.
   Google Scholar
• Sies H, Berndt C, Jones DP. Oxidative stress. Annu Rev Biochem. 2017;86:715–748.
   PubMed Web of Science ®Google Scholar
• Yamamoto M, Kensler TW, Motohashi H. The KEAP1-NRF2 system: a thiol-based sensor-effector apparatus for maintaining redox homeostasis. Physiol Rev. 2018;98(3):1169–1203.
   PubMed Web of Science ®Google Scholar
• Davoli T, Xu AW, Mengwasser KE, et al. Cumulative haploinsufficiency and triplosensitivity drive aneuploidy patterns and shape the cancer genome. Cell. 2013;155(4):948–962.
   PubMed Web of Science ®Google Scholar
• Khurana N, Sikka S. Targeting crosstalk between Nrf-2, NF-κB and androgen receptor signaling in prostate cancer. Cancers. 2018; 10(10):352.
   Web of Science ®Google Scholar
• Chhunchha B, Kubo E, Singh DP. Sulforaphane-induced Klf9/Prdx6 axis acts as a molecular switch to control redox signaling and determines fate of cells. Cells. 2019;8(10):1159.
   Web of Science ®Google Scholar
• Bieging KT, Mello SS, Attardi LD. Unravelling mechanisms of p53-mediated tumour suppression. Nat Rev Cancer. 2014;14(5):359–370.
   PubMed Web of Science ®Google Scholar
• Nguyen TT, Grimm SA, Bushel PR, et al. Revealing a human p53 universe. Nucleic Acids Res. 2018;46(16):8153–8167.
   PubMed Web of Science ®Google Scholar
• Haupt S, Caramia F, Herschtal A, et al. Identification of cancer sex-disparity in the functional integrity of p53 and its X chromosome network. Nat Commun. 2019;10(1):5385.
   PubMedGoogle Scholar
• Drolz A, Wewalka M, Horvatits T, et al. Gender-specific differences in energy metabolism during the initial phase of critical illness. Eur J Clin Nutr. 2014;68(6):707–711.
   PubMed Web of Science ®Google Scholar
• Lefaki M, Papaevgeniou N, Chondrogianni N. Redox regulation of proteasome function. Redox Biol. 2017;13:452–458.
   PubMed Web of Science ®Google Scholar
• Besse-Patin A, Léveillé M, Oropeza D, et al. Estrogen signals through peroxisome proliferator-activated receptor-γ coactivator 1α to reduce oxidative damage associated with diet-induced fatty liver disease. Gastroenterology. 2017;152(1):243–256.
   PubMed Web of Science ®Google Scholar
• Perkins ND. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol. 2007;8(1):49–62.
   PubMed Web of Science ®Google Scholar
• Morgan MJ, Liu ZG. Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res. 2011; 21(1):103–115.
   PubMed Web of Science ®Google Scholar
• Perkins ND. The diverse and complex roles of NF-κB subunits in cancer. Nat Rev Cancer. 2012;12(2):121–132.
   PubMed Web of Science ®Google Scholar
• Frasor J, Weaver A, Pradhan M, et al. Positive cross-talk between estrogen receptor and NF-kappaB in breast cancer. Cancer Res. 2009; 69(23):8918–8925.
   PubMed Web of Science ®Google Scholar
• Hielscher A, Gerecht S. Hypoxia and free radicals: role in tumor progression and the use of engineering-based platforms to address these relationships. Free Radic Biol Med. 2015;79:281–291.
   PubMed Web of Science ®Google Scholar
• T, McGarry T, Biniecka M, Veale DJ, et al. Hypoxia, oxidative stress and inflammation. Free Radic Biol Med. 2018;125:15–24.
   PubMed Web of Science ®Google Scholar
• Chandel NS, McClintock DS, Feliciano CE, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000;275(33):25130–25138.
   PubMed Web of Science ®Google Scholar
• Masson N, Willam C, Maxwell PH, et al. Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation. EMBO J. 2001;20(18):5197–5206.
   PubMed Web of Science ®Google Scholar
• Chandel NS, Maltepe E, Goldwasser E, et al. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA. 1998;95(20):11715–11720.
   PubMed Web of Science ®Google Scholar
• Campos ACE, Molognoni F, Melo FHM, et al. Oxidative stress modulates DNA methylation during melanocyte anchorage blockade associated with malignant transformation. Neoplasia. 2007;9(12):1111–1121.
   PubMed Web of Science ®Google Scholar
• Lim SO, Gu JM, Kim MS, et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology. 2008;135(6):2128–2140.
   PubMed Web of Science ®Google Scholar
• Mahalingaiah PK, Ponnusamy L, Singh KP. Oxidative stress-induced epigenetic changes associated with malignant transformation of human kidney epithelial cells. Oncotarget. 2017;8(7):11127–11143.
   PubMedGoogle Scholar
• Nanduri J, Makarenko V, Reddy VD, et al. Epigenetic regulation of hypoxic sensing disrupts cardiorespiratory homeostasis. Proc Natl Acad Sci USA. 2012;109(7):2515–2520.
   PubMed Web of Science ®Google Scholar
• Chan SY, Zhang YY, Hemann C, et al. MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab. 2009;10(4):273–284.
   PubMed Web of Science ®Google Scholar
• Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell. 2012;148(3):399–408.
   PubMed Web of Science ®Google Scholar
• Stegen S, van Gastel N, Eelen G, et al. HIF-1α promotes glutamine-mediated redox homeostasis and glycogen-dependent bioenergetics to support postimplantation bone cell survival. Cell Metab. 2016;23(2):265–279.
   PubMed Web of Science ®Google Scholar
• Samanta D, Semenza GL. Maintenance of redox homeostasis by hypoxia-inducible factors. Redox Biol. 2017;13:331–335.
   PubMed Web of Science ®Google Scholar
• Parker CS, Topol J. A drosophila RNA polymerase II transcription factor contains a promoter-region-specific DNA-binding activity. Cell. 1984;36(2):357–369.
   PubMed Web of Science ®Google Scholar
• Topol J, Ruden DM, Parker CS. Sequences required for in vitro transcriptional activation of a drosophila hsp 70 gene. Cell. 1985;42(2):527–537.
   PubMed Web of Science ®Google Scholar
• Hoang AT, Huang J, Rudra-Ganguly N, et al. A novel association between the human heat shock transcription factor 1 (HSF1) and prostate adenocarcinoma. Am J Pathol. 2000;156(3):857–864.
   PubMed Web of Science ®Google Scholar
• Fang F, Chang R, Yang L. Heat shock factor 1 promotes invasion and metastasis of hepatocellular carcinoma in vitro and in vivo. Cancer. 2012;118(7):1782–1794.
   PubMed Web of Science ®Google Scholar
• Kourtis N, Moubarak RS, Aranda-Orgilles B, et al. FBXW7 modulates cellular stress response and metastatic potential through HSF1 post-translational modification. Nat Cell Biol. 2015;17(3):322–332.
   PubMed Web of Science ®Google Scholar
• Chen K, Qian W, Li J, et al. Loss of AMPK activation promotes the invasion and metastasis of pancreatic cancer through an HSF1-dependent pathway. Mol Oncol. 2017;11(10):1475–1492.
   PubMed Web of Science ®Google Scholar
• Li Y, Xu D, Bao C, et al. MicroRNA-135b, a HSF1 target, promotes tumor invasion and metastasis by regulating RECK and EVI5 in hepatocellular carcinoma. Oncotarget. 2015;6(4):2421–2433.
   PubMedGoogle Scholar
• Khaleque MA, Bharti A, Gong J, et al. Heat shock factor 1 represses estrogen-dependent transcription through association with MTA1. Oncogene. 2008;27(13):1886–1893.
   PubMed Web of Science ®Google Scholar
• Dai C, Whitesell L, Rogers AB, et al. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell. 2007;130(6):1005–1018.
   PubMed Web of Science ®Google Scholar
• Antonietti P, Linder B, Hehlgans S, et al. Interference with the HSF1/HSP70/BAG3 pathway primes glioma cells to matrix detachment and BH3 mimetic-induced apoptosis. Mol Cancer Ther. 2017;16(1):156–168.
   PubMed Web of Science ®Google Scholar
• Jacobs AT, Marnett LJ. Heat shock factor 1 attenuates 4-hydroxynonenal-mediated apoptosis: critical role for heat shock protein 70 induction and stabilization of Bcl-XL. J Biol Chem. 2007;282(46):33412–33420.
   PubMed Web of Science ®Google Scholar
• Jacobs AT, Marnett LJ. HSF1-mediated BAG3 expression attenuates apoptosis in 4-hydroxynonenal-treated colon cancer cells via stabilization of anti-apoptotic bcl-2 proteins. J Biol Chem. 2009;284(14):9176–9183.
   PubMed Web of Science ®Google Scholar
• Wang J, He H, Yu L, et al. HSF1 down-regulates XAF1 through transcriptional regulation. J Biol Chem. 2006;281(5):2451–2459.
   PubMed Web of Science ®Google Scholar
• Liang W, Liao Y, Zhang J, et al. Heat shock factor 1 inhibits the mitochondrial apoptosis pathway by regulating second mitochondria-derived activator of caspase to promote pancreatic tumorigenesis. J Exp Clin Cancer Res. 2017;36(1):64.
   PubMedGoogle Scholar
• Dong B, Jaeger AM, Thiele DJ. Inhibiting heat shock factor 1 in cancer: a unique therapeutic opportunity. Trends Pharmacol Sci. 2019; 40(12):986–1005.
   PubMed Web of Science ®Google Scholar
• Kovács D, Sigmond T, Hotzi B, et al. HSF1Base: a comprehensive database of HSF1 (heat shock factor 1) target genes. Int J Mol Sci. 2019;20(20):5815.
   Google Scholar
• Gökmen-Polar Y, Badve S. Upregulation of HSF1 in estrogen receptor positive breast cancer. Oncotarget. 2016;7(51):84239–84245.
   PubMedGoogle Scholar
• Klotz LO, Sanchez-Ramos C, Prieto-Arroyo I, et al. Redox regulation of FoxO transcription factors. Redox Biol. 2015;6:51–72.
   PubMed Web of Science ®Google Scholar
• Putker M, Madl T, Vos HR, et al. Redox-dependent control of FOXO/DAF-16 by transportin-1. Mol Cell. 2013;49(4):730–742.
   PubMed Web of Science ®Google Scholar
• Carpenter R, Gökmen-Polar Y. HSF1 as a cancer biomarker and therapeutic target. Curr Cancer Drug Targets. 2019;19(7):515–524.
   PubMed Web of Science ®Google Scholar
• Eijkelenboom A, Burgering BM. FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol. 2013;14(2):83–97.
   PubMed Web of Science ®Google Scholar
• Lin CY, Jan YJ, Kuo LK, et al. Elevation of androgen receptor promotes prostate cancer metastasis by induction of epithelial-mesenchymal transition and reduction of KAT5. Cancer Sci. 2018;109(11):3564–3574.
   PubMed Web of Science ®Google Scholar
• Huang Q, Sun Y, Ma X, et al. Androgen receptor increases hematogenous metastasis yet decreases lymphatic metastasis of renal cell carcinoma. Nat Commun. 2017;8(1):918.
   PubMedGoogle Scholar
• Li P, Lee H, Guo S, et al. AKT-independent protection of prostate cancer cells from apoptosis mediated through complex formation between the androgen receptor and FKHR. Mol Cell Biol. 2003;23(1):104–118.
   PubMed Web of Science ®Google Scholar
• Deroo BJ, Korach KS. Estrogen receptors and human disease. J Clin Invest. 2006;116(3):561–570.
   PubMed Web of Science ®Google Scholar
• Lei JT, Gou X, Seker S, et al. ESR1 alterations and metastasis in estrogen receptor positive breast cancer. JCMT. 2019;2019:38.
   Google Scholar
• Bejjani F, Evanno E, Zibara K, et al. The AP-1 transcriptional complex: local switch or remote command? Biochim Biophys Acta Rev Cancer. 2019;1872(1):11–23.
   PubMed Web of Science ®Google Scholar
• Glorieux C, Sandoval JM, Fattaccioli A, et al. Chromatin remodeling regulates catalase expression during cancer cells adaptation to chronic oxidative stress. Free Radic Biol Med. 2016;99:436–450.
   PubMed Web of Science ®Google Scholar
• Soriano FX, Baxter P, Murray LM, et al. Transcriptional regulation of the AP-1 and Nrf2 target gene sulfiredoxin. Mol Cells. 2009;27(3):279–282.
   PubMed Web of Science ®Google Scholar
• Eferl R, Wagner EF. AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer. 2003;3(11):859–868.
   PubMed Web of Science ®Google Scholar
• Shaulian E, Karin M. AP-1 in cell proliferation and survival. Oncogene. 2001;20(19):2390–2400.
   PubMed Web of Science ®Google Scholar