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2000
Volume 20, Issue 1
  • ISSN: 1574-8928
  • E-ISSN: 2212-3970

Abstract

Introduction

Ovarian Cancer (OC) is a heterogeneous malignancy with poor outcomes. Oxidative stress plays a crucial role in developing drug resistance. However, the relationships between Oxidative Stress-related Genes (OSRGs) and the prognosis of platinum-resistant OC remain unclear. This study aimed to develop an OSRGs-based prognostic risk model for platinum-resistant OC patients.

Methods

Gene Set Enrichment Analysis (GSEA) was performed to determine the expression difference of OSRGs between platinum-resistant and -sensitive OC patients. Cox regression analyses were used to identify the prognostic OSRGs and establish a risk score model. The model was validated by using an external dataset. Machine learning was used to determine the prognostic OSRGs associated with platinum resistance. Finally, the biological functions of selected OSRG were determined cellular experiments.

Results

Three gene sets associated with oxidative stress-related pathways were enriched ( < 0.05), and 105 OSRGs were found to be differentially expressed between platinum-resistant and -sensitive OC ( < 0.05). Twenty prognosis-associated OSRGs were identified (HR: 0:562-5.437; 95% CI: 0.319-20.148; < 0.005), and seven independent OSRGs were used to construct a prognostic risk score model, which accurately predicted the survival of OC patients (1-, 3-, and 5-year AUC=0.69, 0.75, and 0.67, respectively). The prognostic potential of this model was confirmed in the validation cohort. Machine learning showed five prognostic OSRGs (SPHK1, PXDNL, C1QA, WRN, and SETX) to be strongly correlated with platinum resistance in OC patients. Cellular experiments showed that WRN significantly promoted the malignancy and platinum resistance of OC cells.

Conclusion

The OSRGs-based risk score model can efficiently predict the prognosis and platinum resistance of OC patients. This model may improve the risk stratification of OC patients in the clinic.

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2024-05-09
2025-03-01
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References

  1. ZhengM. Oxidative stress response biomarkers of ovarian cancer based on single-cell and bulk RNA sequencing.Oxid Med Cell Longev20232023126103910.1155/2023/126103936743693
    [Google Scholar]
  2. ArmstrongD.K. AlvarezR.D. Bakkum-GamezJ.N. BarroilhetL. BehbakhtK. BerchuckA. ChenL. CristeaM. DeRosaM. EisenhauerE.L. GershensonD.M. GrayH.J. GrishamR. HakamA. JainA. KaramA. KonecnyG.E. LeathC.A. LiuJ. MahdiH. MartinL. MateiD. McHaleM. McLeanK. MillerD.S. O’MalleyD.M. Percac-LimaS. RatnerE. RemmengaS.W. VargasR. WernerT.L. ZsirosE. BurnsJ.L. EnghA.M. Ovarian cancer, version 2.2020, NCCN clinical practice guidelines in oncology.J. Natl. Compr. Canc. Netw.202119219122610.6004/jnccn.2021.000733545690
    [Google Scholar]
  3. LiuQ. Identifying the role of oxidative stress-related genes as prognostic biomarkers and predicting the response of immunotherapy and chemotherapy in ovarian cancer.Oxid Med Cell Longev20222022657553410.1155/2022/657553436561981
    [Google Scholar]
  4. StewartC. RalyeaC. LockwoodS. Ovarian cancer: An integrated review.Semin. Oncol. Nurs.201935215115610.1016/j.soncn.2019.02.00130867104
    [Google Scholar]
  5. YangL. XieH.J. LiY.Y. WangX. LiuX.X. MaiJ. Molecular mechanisms of platinum-based chemotherapy resistance in ovarian cancer (Review).Oncol. Rep.20224748210.3892/or.2022.829335211759
    [Google Scholar]
  6. CrijnsA.P.G. FehrmannR.S.N. de JongS. GerbensF. MeersmaG.J. KlipH.G. HollemaH. HofstraR.M.W. MeermanG.J. de VriesE.G.E. van der ZeeA.G.J. Survival-related profile, pathways, and transcription factors in ovarian cancer.PLoS Med.200962e100002410.1371/journal.pmed.100002419192944
    [Google Scholar]
  7. DvorakZ. StarhaP. TravnicekZ. New diiodo-platinum(+II) complexes with 7-azaindole, useful for treating breast cancer, osteosarcoma, ovarian cancer resistant against cisplatin, lung cancer, cervical cancer and malignant melanoma.Patent CZ201400275-A3.CZ305374-B6.2015
  8. BurnsN.M. Treating patient suffering from cancer e.g. platinum-resistant ovarian cancer and breast cancer, comprises administering a poly adenosine diphosphate ribose polymerase inhibitor, and a long-acting topoisomerase-I inhibitor to the patient.Patent WO2015108876-A1CA2934552-A1AU2015206667-A, 2015.
    [Google Scholar]
  9. ReddyJ.A. LeamonC.P. NguyenB. Treating platinum-resistant ovarian cancer and endometrial or non-small cell lung cancers, comprises administering vintafolide, and paclitaxel having a mode of action of mitosis inhibition.Endocyte IncPatent US2014066383-A1, 2014.
    [Google Scholar]
  10. BraleyC. BradleyC. Treating platinum-resistant recurrent ovarian cancer in patient involves administering 4-iodo-3-nitrobenzamide or its metabolite or salt, gemcitabine and carboplatin to patient having platinum-resistant recurrent ovarian cancer.WO2011153383-A1, CA2725027-A1, AU2010249298-A12011
  11. BoseR.N. BoseR. New isolated monomeric platinum complex useful for treating cancer e.g. ovarian cancer, testicular cancer, small cell lung cancer and cancers that are resistant to anticancer agents e.g. cisplatin, carboplatin.WO2009021081-A2. US2009042838-A1. WO2009021081-A32009
  12. MenichincheriM. New 7-substd. 7-deoxy-taxol derivs. used as antitumour agents, e.g. for treating platinum-resistant ovarian cancer.WO9614309-A1. EP738266-A1. JP9507864-W1996
  13. BernasconiC. BollagD. Treating a patient diagnosed with a platinum-resistant   ovarian   cancer, comprises administering an anti-vascular endothelial growth factor antibody and a chemotherapeutic to the patient.WO2013135602-A2. WO2013135602-A3. EP2825558-A22013
  14. KelseyS.M. Treating cancer e.g. platinum-resistant ovarian cancer, involves administering human epidermal growth factor receptor 2 (HER2) antibody that inhibits HER dimerization more effectively than trastuzumab and gemcitabine.US2012107391-A1.2012
  15. LiJ. QiF. SuH. ZhangC. ZhangQ. ChenY. ChenP. SuL. ChenY. YangY. ChenZ. ZhangS. GRP75-faciliated Mitochondria-associated ER Membrane (MAM) integrity controls cisplatin-resistance in ovarian cancer patients.Int. J. Biol. Sci.20221872914293110.7150/ijbs.7157135541901
    [Google Scholar]
  16. SuL. SunZ. QiF. SuH. QianL. LiJ. ZuoL. HuangJ. YuZ. LiJ. ChenZ. ZhangS. GRP75-driven, cell-cycle-dependent macropinocytosis of Tat/pDNA-Ca2+ nanoparticles underlies distinct gene therapy effect in ovarian cancer.J. Nanobiotechnology202220134010.1186/s12951‑022‑01530‑635858873
    [Google Scholar]
  17. WuY. ZhangX. WangZ. ZhengW. CaoH. ShenW. Targeting oxidative phosphorylation as an approach for the treatment of ovarian cancer.Front. Oncol.20221297147910.3389/fonc.2022.97147936147929
    [Google Scholar]
  18. DattaA. BroshR.M.Jr WRN rescues replication forks compromised by a BRCA2 deficiency: Predictions for how inhibition of a helicase that suppresses premature aging tilts the balance to fork demise and chromosomal instability in cancer.BioEssays2022448220005710.1002/bies.20220005735751457
    [Google Scholar]
  19. BelotteJ. FletcherN.M. AwonugaA.O. AlexisM. Abu-SoudH.M. SaedM.G. DiamondM.P. SaedG.M. The role of oxidative stress in the development of cisplatin resistance in epithelial ovarian cancer.Reprod. Sci.201421450350810.1177/193371911350340324077440
    [Google Scholar]
  20. Fletcher-KingN.M. The role of oxidative stress in the pathogenesis of epithelial ovarian cancer.Wayne State University School of MedicineDetroit, MI, USA2013122
    [Google Scholar]
  21. WuC. HeL. WeiQ. LiQ. JiangL. ZhaoL. WangC. LiJ. WeiM. Bioinformatic profiling identifies a platinum-resistant–related risk signature for ovarian cancer.Cancer Med.2020931242125310.1002/cam4.269231856408
    [Google Scholar]
  22. JelicM. MandicA. MaricicS. SrdjenovicB. Oxidative stress and its role in cancer.J. Cancer Res. Ther.2021171222810.4103/jcrt.JCRT_862_1633723127
    [Google Scholar]
  23. SaedG.M. DiamondM.P. FletcherN.M. Updates of the role of oxidative stress in the pathogenesis of ovarian cancer.Gynecol. Oncol.2017145359560210.1016/j.ygyno.2017.02.03328237618
    [Google Scholar]
  24. CruzI.N. ColeyH.M. KramerH.B. MadhuriT.K. SafuwanN.A.M. AngelinoA.R. YangM. Proteomics analysis of ovarian cancer cell lines and tissues reveals drug resistance-associated proteins.Cancer Genomics Proteomics2017141355210.21873/cgp.2001728031236
    [Google Scholar]
  25. ZhangJ. YangL. XiangX. LiZ. QuK. LiK. A panel of three oxidative stress-related genes predicts overall survival in ovarian cancer patients received platinum-based chemotherapy.Aging20181061366137910.18632/aging.10147329910195
    [Google Scholar]
  26. VerschoorM.L. SinghG. Ets-1 regulates intracellular glutathione levels: key target for resistant ovarian cancer.Mol. Cancer201312113810.1186/1476‑4598‑12‑13824238102
    [Google Scholar]
  27. WilsonL.A. YamamotoH. SinghG. Role of the transcription factor Ets-1 in cisplatin resistance.Mol. Cancer Ther.20043782383210.1158/1535‑7163.823.3.715252143
    [Google Scholar]
  28. TakedaY. HizukuriS. Actions of Aspergillus oryzae alpha-amylase, potato phosphorylase, and rabbit muscle phosphorylase a and b on phosphorylated (1→4)-α-d-glucan.Carbohydr. Res.1986153229530710.1016/S0008‑6215(00)90271‑43096568
    [Google Scholar]
  29. ReuterS. GuptaS.C. ChaturvediM.M. AggarwalB.B. Oxidative stress, inflammation, and cancer: How are they linked?Free Radic. Biol. Med.201049111603161610.1016/j.freeradbiomed.2010.09.00620840865
    [Google Scholar]
  30. Al-MurraniS. Al-MuraniS. Al MurraniS. Predicting resistance of chemotherapeutic drug to ovarian cancer, by detecting several expressed genes e.g. S100A10 in biological sample and control sample, comparing amount of expressed gene in biological sample with control sample.Patent WO2005066371-A2. US2005176669-A1. EP1704250-A2.2005
  31. WawrowiczK. Majkowska-PilipA. SzwedM. Żelechowska-MatysiakK. ChajdukE. BilewiczA. Oxidative status as an attribute for selective antitumor activity of platinum-containing nanoparticles against hepatocellular carcinoma.Int. J. Mol. Sci.202223231477310.3390/ijms23231477336499101
    [Google Scholar]
  32. QinZ. TongH. LiT. CaoH. ZhuJ. YinS. HeW. SPHK1 contributes to cisplatin resistance in bladder cancer cells via the NONO/STAT3 axis.Int. J. Mol. Med.202148520410.3892/ijmm.2021.503734549307
    [Google Scholar]
  33. HartP.C. ChiyodaT. LiuX. WeigertM. CurtisM. ChiangC.Y. LothR. LastraR. McGregorS.M. LocasaleJ.W. LengyelE. RomeroI.L. SPHK1 is a novel target of metformin in ovarian cancer.Mol. Cancer Res.201917487088110.1158/1541‑7786.MCR‑18‑040930655321
    [Google Scholar]
  34. ShidaD. TakabeK. KapitonovD. MilstienS. SpiegelS. Targeting SphK1 as a new strategy against cancer.Curr. Drug Targets20089866267310.2174/13894500878513240218691013
    [Google Scholar]
  35. RichardP. FengS. TsaiY.L. LiW. RinchettiP. MuhithU. Irizarry-ColeJ. StolzK. SanzL.A. HartonoS. HoqueM. TadesseS. SeitzH. LottiF. HiranoM. ChédinF. TianB. ManleyJ.L. SETX (senataxin), the helicase mutated in AOA2 and ALS4, functions in autophagy regulation.Autophagy20211781889190610.1080/15548627.2020.179629232686621
    [Google Scholar]
  36. LuM. LiuB. LiD. GaoZ. LiW. ZhouX. ZhanH. PXDNL activates the motility of urothelial bladder carcinoma cells through the Wnt/β-catenin pathway and has a prognostic value.Life Sci.202331212127010.1016/j.lfs.2022.12127036493879
    [Google Scholar]
  37. MengoliV. CeppiI. SanchezA. CannavoE. HalderS. ScaglioneS. GaillardP.H. McHughP.J. RiesenN. PettazzoniP. CejkaP. WRN helicase and mismatch repair complexes independently and synergistically disrupt cruciform DNA structures.EMBO J.2023423e11199810.15252/embj.202211199836541070
    [Google Scholar]
  38. DattaA. BiswasK. SommersJ.A. ThompsonH. AwateS. NicolaeC.M. ThakarT. MoldovanG.L. ShoemakerR.H. SharanS.K. BroshR.M.Jr WRN helicase safeguards deprotected replication forks in BRCA2-mutated cancer cells.Nat. Commun.2021121656110.1038/s41467‑021‑26811‑w34772932
    [Google Scholar]
  39. Iglesias-PedrazJ.M. Fossatti-JaraD.M. Valle-Riestra-FeliceV. Cruz-VisalayaS.R. Ayala FelixJ.A. ComaiL. WRN modulates translation by influencing nuclear mRNA export in HeLa cancer cells.BMC Mol. Cell Biol.20202117110.1186/s12860‑020‑00315‑933054770
    [Google Scholar]
  40. OrlovetskieN. SerruyaR. Abboud-JarrousG. JarrousN. Targeted inhibition of WRN helicase, replication stress and cancer.Biochim. Biophys. Acta Rev. Cancer201718671424810.1016/j.bbcan.2016.11.00427902925
    [Google Scholar]
  41. LeeS.Y. LeeH. KimE.S. ParkS. LeeJ. AhnB. WRN translocation from nucleolus to nucleoplasm is regulated by SIRT1 and required for DNA repair and the development of chemoresistance.Mutat. Res.2015774404810.1016/j.mrfmmm.2015.03.00125801465
    [Google Scholar]
  42. AraiA. ChanoT. FutamiK. FuruichiY. IkebuchiK. InuiT. TamenoH. OchiY. ShimadaT. HisaY. OkabeH. RECQL1 and WRN proteins are potential therapeutic targets in head and neck squamous cell carcinoma.Cancer Res.201171134598460710.1158/0008‑5472.CAN‑11‑032021571861
    [Google Scholar]
  43. MaoF.J. SidorovaJ.M. LauperJ.M. EmondM.J. MonnatR.J. The human WRN and BLM RecQ helicases differentially regulate cell proliferation and survival after chemotherapeutic DNA damage.Cancer Res.201070166548655510.1158/0008‑5472.CAN‑10‑047520663905
    [Google Scholar]
  44. LuoJ. WRN protein and Werner syndrome.N. Am. J. Med. Sci. 20103420520710.7156/v3i4p20522180828
    [Google Scholar]
  45. LebelM. MassipL. GarandC. ThorinE. Ascorbate improves metabolic abnormalities in Wrn mutant mice but not the free radical scavenger catechin.Ann. N. Y. Acad. Sci.201011971404410.1111/j.1749‑6632.2010.05189.x20536831
    [Google Scholar]
  46. MultaniA.S. ChangS. WRN at telomeres: implications for aging and cancer.J. Cell Sci.2007120571372110.1242/jcs.0339717314245
    [Google Scholar]
  47. WuX. HanL.Y. ZhangX.X. WangL. The Study of Nrf2 signaling pathway in ovarian cancer.Crit. Rev. Eukaryot. Gene Expr.201828432933610.1615/CritRevEukaryotGeneExpr.201802028630311581
    [Google Scholar]
  48. MaL. WangH. WangC. SuJ. XieQ. XuL. YuY. LiuS. LiS. XuY. LiZ. Failure of elevating calcium induces oxidative stress tolerance and imparts cisplatin resistance in ovarian cancer cells.Aging Dis.20167325426610.14336/AD.2016.011827330840
    [Google Scholar]
  49. DonadilleB. D’AnellaP. AuclairM. UhrhammerN. SorelM. GrigorescuR. OuzounianS. CambonieG. BoulotP. LaforêtP. CarbonneB. Christin-MaitreS. BignonY.J. VigourouxC. Partial lipodystrophy with severe insulin resistance and adult progeria Werner syndrome.Orphanet J. Rare Dis.20138110610.1186/1750‑1172‑8‑10623849162
    [Google Scholar]
  50. SteffensenK.D. WaldstrømM. BrandslundI. PetzoldM. JakobsenA. The prognostic and predictive value of combined HE4 and CA-125 in ovarian cancer patients.Int. J. Gynecol. Cancer20122291474148210.1097/IGC.0b013e3182681cfd23095772
    [Google Scholar]
  51. KanagarajR. ParasuramanP. MihaljevicB. van LoonB. BurdovaK. KönigC. FurrerA. BohrV.A. HübscherU. JanscakP. Involvement of Werner syndrome protein in MUTYH-mediated repair of oxidative DNA damage.Nucleic Acids Res.201240178449845910.1093/nar/gks64822753033
    [Google Scholar]
  52. SavvaC. SadiqM. SheikhO. KarimS. TrivediS. GreenA.R. RakhaE.A. MadhusudanS. AroraA. Werner syndrome protein expression in breast cancer.Clin. Breast Cancer20212115773.e710.1016/j.clbc.2020.07.01332919863
    [Google Scholar]
  53. RuszO. PálM. SzilágyiÉ. RovóL. VargaZ. TomisaB. FábiánG. KovácsL. NagyO. MózesP. ReiszZ. TiszlaviczL. DeákP. KahánZ. The expression of checkpoint and DNA repair genes in head and neck cancer as possible predictive factors.Pathol. Oncol. Res.201723225326410.1007/s12253‑016‑0088‑z27411922
    [Google Scholar]
  54. SakaoY. KatoA. TsujiT. YasudaH. TogawaA. FujigakiY. KahyoT. SetouM. HishidaA. Cisplatin induces Sirt1 in association with histone deacetylation and increased Werner syndrome protein in the kidney.Clin. Exp. Nephrol.201115336337210.1007/s10157‑011‑0421‑521416250
    [Google Scholar]
  55. DasA. BoldoghI. LeeJ.W. HarriganJ.A. HegdeM.L. PiotrowskiJ. de Souza PintoN. RamosW. GreenbergM.M. HazraT.K. MitraS. BohrV.A. The human Werner syndrome protein stimulates repair of oxidative DNA base damage by the DNA glycosylase NEIL1.J. Biol. Chem.200728236265912660210.1074/jbc.M70334320017611195
    [Google Scholar]
  56. PierceallW.E. SprottK.M. WeaverD.T. Determining the sensitivity or resistance of an ovarian cancer to a chemotherapeutic agent comprises identifying an alteration in at least one DNARMARKER e.g. PARP1 and XPF.Patent WO2012019000-A2. WO2012019000-A32012
  57. MunroeD ChanD W ZhangZ ChanD Panel for pre-operatively assessing subject's risk of having ovarian cancer comprises markers cancer antigen 125, prealbumin, transferrin and human epididymis protein 4.Patent WO2014182896-A1. CA2914918-A1. EP2994542-A12014
  58. EstellerM. Predicting the likelihood of successful treatment of cancer with topoisomerase, DNA methyltransferase, and/or histone deacetylases inhibitors, comprises determining the methylation status of a RecQ helicase family gene.Patent US2009047214-A12009
  59. CroceC.M. VecchioneA. CroceC. Diagnosing ovarian cancer resistant to chemotherapeutic intervention, preferably serous epithelial ovarian carcinoma, involves identifying e.g. microRNA-484 expression level in sample, and comparing expression levels with control.Patent WO2013056217-A1. US2013096022-A1. AU2012323924-A12013
  60. DingDN XieLZ ShenY LiJ GuoY FuY LiuFY HanFJ Insights into the role of oxidative stress in ovarian cancer.Oxid Med Cell Longev20212021838825810.1155/2021/838825834659640
    [Google Scholar]
  61. Katanić StankovićJ.S. SelakovićD. RosićG. Oxidative damage as a fundament of systemic toxicities induced by cisplatin—the crucial limitation or potential therapeutic target?Int. J. Mol. Sci.202324191457410.3390/ijms24191457437834021
    [Google Scholar]
  62. PodratzJ.L. KnightA.M. TaL.E. StaffN.P. GassJ.M. GenelinK. SchlattauA. LathroumL. WindebankA.J. Cisplatin induced mitochondrial DNA damage in dorsal root ganglion neurons.Neurobiol. Dis.201141366166810.1016/j.nbd.2010.11.01721145397
    [Google Scholar]
  63. GaladariS. RahmanA. PallichankandyS. ThayyullathilF. Reactive oxygen species and cancer paradox: To promote or to suppress?Free Radic. Biol. Med.201710414416410.1016/j.freeradbiomed.2017.01.00428088622
    [Google Scholar]
  64. CaiX. LiY. ZhengJ. LiuL. JiaoZ. LinJ. JiangS. LinX. SunY. Modeling of senescence-related chemoresistance in ovarian cancer using data analysis and patient-derived organoids.Front. Oncol.202413129155910.3389/fonc.2023.129155938370348
    [Google Scholar]
  65. OpreskoP.L. CalvoJ.P. von KobbeC. Role for the Werner syndrome protein in the promotion of tumor cell growth.Mech. Ageing Dev.20071287-842343610.1016/j.mad.2007.05.00917624410
    [Google Scholar]
  66. WirtenbergerM. FrankB. HemminkiK. KlaesR. SchmutzlerR.K. WappenschmidtB. MeindlA. KiechleM. ArnoldN. WeberB.H. NiederacherD. BartramC.R. BurwinkelB. Interaction of Werner and Bloom syndrome genes with p53 in familial breast cancer.Carcinogenesis20052781655166010.1093/carcin/bgi37416501249
    [Google Scholar]
  67. MajT. WangW. CrespoJ. ZhangH. WangW. WeiS. ZhaoL. VatanL. ShaoI. SzeligaW. LyssiotisC. LiuJ.R. KryczekI. ZouW. Oxidative stress controls regulatory T cell apoptosis and suppressor activity and PD-L1-blockade resistance in tumor.Nat. Immunol.201718121332134110.1038/ni.386829083399
    [Google Scholar]
  68. WangX. XuY. DaiL. YuZ. WangM. ChanS. SunR. HanQ. ChenJ. ZuoX. WangZ. HuX. YangY. ZhaoH. HuK. ZhangH. ChenW. A novel oxidative stress- and ferroptosis-related gene prognostic signature for distinguishing cold and hot tumors in colorectal cancer.Front. Immunol.202213104373810.3389/fimmu.2022.104373836389694
    [Google Scholar]
  69. TanY. LiJ. ZhaoG. HuangK.C. CardenasH. WangY. MateiD. ChengJ.X. Metabolic reprogramming from glycolysis to fatty acid uptake and beta-oxidation in platinum-resistant cancer cells.Nat. Commun.2022131455410.1038/s41467‑022‑32101‑w35931676
    [Google Scholar]
  70. LiuQ. YuM. ZhangT. Construction of oxidative stress-related genes risk model predicts the prognosis of uterine corpus endometrial cancer patients.Cancers20221422557210.3390/cancers1422557236428665
    [Google Scholar]
  71. WuX. ZhuZ. GaiM. Prognostic modelling of colorectal cancer based on oxidative stress-related genes.J. Cancer Res. Clin. Oncol.202314912106231063110.1007/s00432‑023‑04914‑937300722
    [Google Scholar]
  72. GuayD. GaudreaultI. MassipL. LebelM. Formation of a nuclear complex containing the p53 tumor suppressor, YB-1, and the Werner syndrome gene product in cells treated with UV light.Int. J. Biochem. Cell Biol.20063881300131310.1016/j.biocel.2006.01.00816584908
    [Google Scholar]
  73. SzekelyA.M. BleichertF. NümannA. Van KomenS. ManasanchE. Ben NasrA. CanaanA. WeissmanS.M. Werner protein protects nonproliferating cells from oxidative DNA damage.Mol. Cell. Biol.20052523104921050610.1128/MCB.25.23.10492‑10506.200516287861
    [Google Scholar]
  74. ZhuY. TangQ. CaoW. ZhouN. JinX. SongZ. ZuL. XuS. Identification of a novel oxidative stress-related prognostic model in lung adenocarcinoma.Front. Pharmacol.202213103006210.3389/fphar.2022.103006236467027
    [Google Scholar]
  75. HuangX. LuZ. HeM. FengY. YuS. ShenB. LuJ. WuP. PanB. DingH. ChenC. SunY. A prognostic risk model of a novel oxidative stress-related signature predicts clinical prognosis and demonstrates immune relevancy in lung adenocarcinoma.Oxid. Med. Cell. Longev.2022202214310.1155/2022/226201436439693
    [Google Scholar]
  76. PaganoG. ZatteraleA. DeganP. d’IschiaM. KellyF.J. PallardóF.V. KodamaS. Multiple involvement of oxidative stress in Werner syndrome phenotype.Biogerontology20056423324310.1007/s10522‑005‑2624‑116333757
    [Google Scholar]
  77. NguyenD.T. RoviraI.I. FinkelT. Regulation of the Werner helicase through a direct interaction with a subunit of protein kinase A.FEBS Lett.20025211-317017410.1016/S0014‑5793(02)02868‑512067711
    [Google Scholar]
  78. LinD. HuB. ZhuS. WuY. Exploring a ferroptosis and oxidative stress-based prognostic model for clear cell renal cell carcinoma.Front. Oncol.202313113147310.3389/fonc.2023.113147337064095
    [Google Scholar]
  79. WangD. DengZ. LuM. DengK. LiZ. ZhouF. Integrated analysis of the roles of oxidative stress related genes and prognostic value in clear cell renal cell carcinoma.J. Cancer Res. Clin. Oncol.202314913110571107110.1007/s00432‑023‑04983‑w37340189
    [Google Scholar]
  80. TongS. XiaM. XuY. SunQ. YeL. YuanF. WangY. CaiJ. YeZ. TianD. Identification and validation of a novel prognostic signature based on mitochondria and oxidative stress related genes for glioblastoma.J. Transl. Med.202321113610.1186/s12967‑023‑03970‑636814293
    [Google Scholar]
  81. ZengS. LiW. OuyangH. XieY. FengX. HuangL. A novel prognostic pyroptosis-related gene signature correlates to oxidative stress and immune-related features in gliomas.Oxid. Med. Cell. Longev.2023202312810.1155/2023/425611636778205
    [Google Scholar]
  82. LiJ. WangS. ChiX. HeQ. TaoC. DingY. WangJ. ZhaoJ. WangW. Identification of heterogeneous subtypes and a prognostic model for gliomas based on mitochondrial dysfunction and oxidative stress-related genes.Front. Immunol.202314118347510.3389/fimmu.2023.118347537334354
    [Google Scholar]
  83. RenZ. ZhangJ. ZhengD. LuoY. SongZ. ChenF. LiA. LiuX. Identification of prognosis-related oxidative stress model with immunosuppression in HCC.Biomedicines202311369510.3390/biomedicines1103069536979675
    [Google Scholar]
  84. HongJ. CaiX. Construction of a novel oxidative stress response-related gene signature for predicting the prognosis and therapeutic responses in hepatocellular carcinoma.Dis. Markers2022202212010.1155/2022/620198736133439
    [Google Scholar]
  85. LiS. CaoT. WuT. XuJ. ShenC. HouS. WuY. Identification of a ferroptosis and oxidative stress-associated gene signature for prognostic stratification of ovarian cancer.Am. J. Transl. Res.20231542645265537193145
    [Google Scholar]
  86. HuX. QinW. LiS. HeM. WangY. GuanS. ZhaoH. YaoW. WeiM. LiuM. WuH. Polymorphisms in DNA repair pathway genes and ABCG2 gene in advanced colorectal cancer: correlation with tumor characteristics and clinical outcome in oxaliplatin-based chemotherapy.Cancer Manag. Res.20181128529710.2147/CMAR.S18192230643454
    [Google Scholar]
/content/journals/pra/10.2174/0115748928311077240424065832
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