Identification of chemoresistance targets in doxorubicin-resistant lung adenocarcinoma cells using LC-MS/MS-based proteomics

References

• Holohan C, Van Schaeybroeck S, Longley DB, et al. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer. 2013;13(10):714–726. doi: 10.1038/NRC3599.
   PubMed Web of Science ®Google Scholar
• Alfarouk KO, Stock C-M, Taylor S, et al. Resistance to cancer chemotherapy: failure in drug response from ADME to P-gp. Cancer Cell Int. 2015;15(1):71. doi: 10.1186/s12935-015-0221-1.
   PubMed Web of Science ®Google Scholar
• Kciuk M, Gielecińska A, Mujwar S, et al. Doxorubicin-An agent with multiple mechanisms of anticancer activity. Cells. 2023;12(4):659. doi: 10.3390/CELLS12040659.
   PubMed Web of Science ®Google Scholar
• Bray F, Laversanne M, Sung H, et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2024;74(3):229–263. doi: 10.3322/CAAC.21834.
   PubMed Web of Science ®Google Scholar
• Meschini S, Marra M, Calcabrini A, et al. Role of the lung resistance-related protein (LRP) in the drug sensitivity of cultured tumor cells. Toxicol In Vitro. 2002;16(4):389–398. doi: 10.1016/S0887-2333(02)00035-8.
   PubMed Web of Science ®Google Scholar
• Arafa E-SA, Zhu Q, Shah ZI, et al. Thymoquinone up-regulates PTEN expression and induces apoptosis in doxorubicin-resistant human breast cancer cells. Mutat Res. 2011;706(1–2):28–35. doi: 10.1016/J.MRFMMM.2010.10.007.
   PubMed Web of Science ®Google Scholar
• Mi J, Zhang X, Rabbani ZN, et al. RNA aptamer-targeted inhibition of NF-kappa B suppresses non-small cell lung cancer resistance to doxorubicin. Mol Ther. 2008;16(1):66–73. doi: 10.1038/SJ.MT.6300320.
   PubMed Web of Science ®Google Scholar
• Housman G, Byler S, Heerboth S, et al. Drug resistance in cancer: an overview. Cancers (Basel). 2014;6(3):1769–1792. doi: 10.3390/CANCERS6031769.
   PubMed Web of Science ®Google Scholar
• Berns K, Horlings HM, Hennessy BT, et al. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell. 2007;12(4):395–402. doi: 10.1016/J.CCR.2007.08.030.
   PubMed Web of Science ®Google Scholar
• Singhal A, Li BT, O'Reilly EM. Targeting KRAS in cancer. Nat Med. 2024;30(4):969–983. doi: 10.1038/S41591-024-02903-0.
   PubMed Web of Science ®Google Scholar
• Duan C, Yu M, Xu J, et al. Overcoming Cancer Multi-drug Resistance (MDR): reasons, mechanisms, nanotherapeutic solutions, and challenges. Biomed Pharmacother. 2023;162:114643. doi: 10.1016/J.BIOPHA.2023.114643.
   PubMed Web of Science ®Google Scholar
• Henry A, Mauperin M, Devy J, et al. The endocytic receptor protein LRP-1 modulate P-glycoprotein mediated drug resistance in MCF-7 cells. PLoS One. 2023;18(9):e0285834. doi: 10.1371/JOURNAL.PONE.0285834.
   PubMed Web of Science ®Google Scholar
• Ghasabi M, Mansoori B, Mohammadi A, et al. MicroRNAs in cancer drug resistance: basic evidence and clinical applications. J Cell Physiol. 2019;234(3):2152–2168. doi: 10.1002/JCP.26810.
   PubMed Web of Science ®Google Scholar
• Song Z, Jia G, Ma P, et al. Exosomal miR-4443 promotes cisplatin resistance in non-small cell lung carcinoma by regulating FSP1 m6A modification-mediated ferroptosis. Life Sci. 2021;276:119399. doi: 10.1016/J.LFS.2021.119399.
   PubMed Web of Science ®Google Scholar
• Gao H, Ma J, Cheng Y, et al. Exosomal transfer of macrophage-derived miR-223 confers doxorubicin resistance in gastric cancer. Onco Targets Ther. 2020;13:12169–12179. doi: 10.2147/OTT.S283542.
   PubMed Web of Science ®Google Scholar
• Torki Z, Ghavi D, Hashemi S, et al. The related miRNAs involved in doxorubicin resistance or sensitivity of various cancers: an update. Cancer Chemother Pharmacol. 2021;88(5):771–793. doi: 10.1007/S00280-021-04337-8.
   PubMed Web of Science ®Google Scholar
• Proteomic profiling of MCF-7 breast cancer cells with chemoresistance to different types of anti-cancer drugs - PubMed; n.d. [accessed January 20, 2024]. https://pubmed.ncbi.nlm.nih.gov/17487377/.
   Google Scholar
• Lin Q, Shen S, Qian Z, et al. Comparative proteomic analysis identifies key metabolic regulators of gemcitabine resistance in pancreatic cancer. Mol Cell Proteomics. 2022;21(10):100409. doi: 10.1016/J.MCPRO.2022.100409.
   PubMed Web of Science ®Google Scholar
• Guney Eskiler G, Yanar S, Akpinar G, et al. Proteomic analysis of talazoparib resistance in triple-negative breast cancer cells. J Biochem & Molecular Tox. 2021;35(3):e22678. doi: 10.1002/jbt.22678.
   Web of Science ®Google Scholar
• Liu W, Chang J, Liu M, et al. Quantitative proteomics profiling reveals activation of mTOR pathway in trastuzumab resistance. Oncotarget. 2017;8(28):45793–45806. doi: 10.18632/ONCOTARGET.17415.
   PubMedGoogle Scholar
• Kuciauskas D, Dreize N, Ger M, et al. Proteomic analysis of breast cancer resistance to the anticancer drug RH1 reveals the importance of cancer stem cells. Cancers (Basel). 2019;11(7):972. doi: 10.3390/CANCERS11070972.
   PubMed Web of Science ®Google Scholar
• Zhang X, Maity TK, Ross KE, et al. Alterations in the global proteome and phosphoproteome in third generation EGFR TKI resistance reveal drug targets to circumvent resistance. Cancer Res. 2021;81(11):3051–3066. doi: 10.1158/0008-5472.CAN-20-2435.
   PubMed Web of Science ®Google Scholar
• Eriksson H, Lengqvist J, Hedlund J, et al. Quantitative membrane proteomics applying narrow range peptide isoelectric focusing for studies of small cell lung cancer resistance mechanisms. Proteomics. 2008;8(15):3008–3018. doi: 10.1002/PMIC.200800174.
   PubMed Web of Science ®Google Scholar
• Nakamura M, Nakatani K, Uzawa K, et al. Establishment and characterization of a cisplatin-resistant oral squamous cell carcinoma cell line, H-1R. Oncol Rep. 2005;14(5):1281–1286. doi: 10.3892/or.14.5.1281.
   PubMed Web of Science ®Google Scholar
• Busch M, Papior D, Stephan H, et al. Characterization of etoposide- and cisplatin-chemoresistant retinoblastoma cell lines. Oncol Rep. 2018;39(1):160–172. doi: 10.3892/OR.2017.6100.
   PubMed Web of Science ®Google Scholar
• Kainat KM, Ansari MI, Bano N, et al. Rifampicin-induced ER stress and excessive cytoplasmic vacuolization instigate hepatotoxicity via alternate programmed cell death paraptosis in vitro and in vivo. Life Sci. 2023;333:122164. doi: 10.1016/J.LFS.2023.122164.
   PubMed Web of Science ®Google Scholar
• Yadav SK, Pandey A, Sarkar S, et al. Identification of altered blood MicroRNAs and plasma proteins in a rat model of Parkinson’s disease. Mol Neurobiol. 2022;59(3):1781–1798. doi: 10.1007/S12035-021-02636-Y.
   PubMed Web of Science ®Google Scholar
• Rahman M, Hasan MR. Cancer metabolism and drug resistance. Metabolites. 2015;5(4):571–600. doi: 10.3390/METABO5040571.
   PubMed Web of Science ®Google Scholar
• Cell cycle-mediated drug resistance: an emerging concept in cancer therapy - PubMed; n.d. [accessed 2024 May 21]. https://pubmed.ncbi.nlm.nih.gov/11489790/.
   Google Scholar
• Ngoka LCM. Sample prep for proteomics of breast cancer: proteomics and gene ontology reveal dramatic differences in protein solubilization preferences of radioimmunoprecipitation assay and urea lysis buffers. Proteome Sci. 2008;6(1):30. doi: 10.1186/1477-5956-6-30.
   PubMedGoogle Scholar
• Tran TO, Vo TH, Lam LHT, et al. ALDH2 as a potential stem cell-related biomarker in lung adenocarcinoma: comprehensive multi-omics analysis. Comput Struct Biotechnol J. 2023;21:1921–1929. doi: 10.1016/J.CSBJ.2023.02.045.
   PubMed Web of Science ®Google Scholar
• Wang W, Wang J, Liu S, et al. An EHMT2/NFYA-ALDH2 signaling axis modulates the RAF pathway to regulate paclitaxel resistance in lung cancer. Mol Cancer. 2022;21(1):106. doi: 10.1186/s12943-022-01579-9.
   Web of Science ®Google Scholar
• Harbottle A, Daly AK, Atherton K, et al. Role of glutathione S-transferase P1, P-glycoprotein and multidrug resistance-associated protein 1 in acquired doxorubicin resistance. Int J Cancer. 2001;92(6):777–783. doi: 10.1002/IJC.1283.
   PubMed Web of Science ®Google Scholar
• Lin C, Xie L, Lu Y, et al. miR-133b reverses cisplatin resistance by targeting GSTP1 in cisplatin-resistant lung cancer cells. Int J Mol Med. 2018;41(4):2050–2058. doi: 10.3892/IJMM.2018.3382.
   PubMed Web of Science ®Google Scholar
• Arsova-Sarafinovska Z, Matevska N, Eken A, et al. Glutathione peroxidase 1 (GPX1) genetic polymorphism, erythrocyte GPX activity, and prostate cancer risk. Int Urol Nephrol. 2009;41(1):63–70. doi: 10.1007/S11255-008-9407-Y.
   PubMed Web of Science ®Google Scholar
• Ravikumar B, Sarkar S, Davies JE, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev. 2010;90(4):1383–1435. doi: 10.1152/PHYSREV.00030.2009.
   PubMed Web of Science ®Google Scholar
• Bilodeau J-F, Patenaude A, Piedboeuf B, et al. Glutathione peroxidase-1 expression enhances recovery of human breast carcinoma cells from hyperoxic cell cycle arrest. Free Radic Biol Med. 2002;33(9):1279–1289. doi: 10.1016/S0891-5849(02)01013-4.
   PubMed Web of Science ®Google Scholar
• Chen B, Shen Z, Wu D, et al. Glutathione peroxidase 1 promotes NSCLC resistance to cisplatin via ROS-induced activation of PI3K/AKT pathway. Biomed Res Int. 2019;2019:7640547. doi: 10.1155/2019/7640547.
   PubMed Web of Science ®Google Scholar
• Alimbetov D, Askarova S, Umbayev B, et al. Pharmacological targeting of cell cycle, apoptotic and cell adhesion signaling pathways implicated in chemoresistance of cancer cells. Int J Mol Sci. 2018;19(6):1690. doi: 10.3390/IJMS19061690.
   PubMed Web of Science ®Google Scholar
• Wang SS, Esplin ED, Li JL, et al. Alterations of the PPP2R1B gene in human lung and colon cancer. Science. 1998;282(5387):284–287. doi: 10.1126/SCIENCE.282.5387.284.
   PubMed Web of Science ®Google Scholar
• Hamano R, Miyata H, Yamasaki M, et al. Overexpression of miR-200c induces chemoresistance in esophageal cancers mediated through activation of the Akt signaling pathway. Clin Cancer Res. 2011;17(9):3029–3038. doi: 10.1158/1078-0432.CCR-10-2532.
   PubMed Web of Science ®Google Scholar
• Song K-H, Choi CH, Lee H-J, et al. HDAC1 upregulation by NANOG promotes multidrug resistance and a stem-like phenotype in immune edited tumor cells. Cancer Res. 2017;77(18):5039–5053. doi: 10.1158/0008-5472.CAN-17-0072.
   PubMed Web of Science ®Google Scholar
• Contreras-Sanzón E, Prado-Garcia H, Romero-Garcia S, et al. Histone deacetylases modulate resistance to the therapy in lung cancer. Front Genet. 2022;13:960263. doi: 10.3389/FGENE.2022.960263.
   PubMed Web of Science ®Google Scholar
• Mamdani H, Jalal SI. Histone deacetylase inhibition in non-small cell lung cancer: hype or hope? Front Cell Dev Biol. 2020;8:582370. doi: 10.3389/FCELL.2020.582370.
   PubMed Web of Science ®Google Scholar
• Min HY, Lee HY. Mechanisms of resistance to chemotherapy in non-small cell lung cancer. Arch Pharm Res. 2021;44(2):146–164. doi: 10.1007/S12272-021-01312-Y.
   PubMed Web of Science ®Google Scholar
• Christowitz C, Davis T, Isaacs A, et al. Mechanisms of doxorubicin-induced drug resistance and drug resistant tumour growth in a murine breast tumour model. BMC Cancer. 2019;19(1):757. doi: 10.1186/s12885-019-5939-z.
   PubMed Web of Science ®Google Scholar
• Yang C, Li Z, Bhatt T, et al. Acquired CDK6 amplification promotes breast cancer resistance to CDK4/6 inhibitors and loss of ER signaling and dependence. Oncogene. 2017;36(16):2255–2264. doi: 10.1038/ONC.2016.379.
   PubMed Web of Science ®Google Scholar
• Iwata S, Tatsumi Y, Yonemoto T, et al. CDK4 overexpression is a predictive biomarker for resistance to conventional chemotherapy in patients with osteosarcoma. Oncol Rep. 2021;46(1):135. doi: 10.3892/OR.2021.8086.
   PubMed Web of Science ®Google Scholar
• Ji ZP, Qiang L, Zhang JL. Transcription activated p73-modulated cyclin D1 expression leads to doxorubicin resistance in gastric cancer. Exp Ther Med. 2018;15(2):1831–1838. doi: 10.3892/ETM.2017.5642.
   PubMed Web of Science ®Google Scholar
• Biliran H, Wang Y, Banerjee S, et al. Overexpression of cyclin D1 promotes tumor cell growth and confers resistance to cisplatin-mediated apoptosis in an elastase-myc transgene-expressing pancreatic tumor cell line. Clin Cancer Res. 2005;11(16):6075–6086. doi: 10.1158/1078-0432.CCR-04-2419.
   PubMed Web of Science ®Google Scholar
• Zhang C, Elkahloun AG, Robertson M, et al. Loss of cytoplasmic CDK1 predicts poor survival in human lung cancer and confers chemotherapeutic resistance. PLoS One. 2011;6(8):e23849. doi: 10.1371/JOURNAL.PONE.0023849.
   PubMed Web of Science ®Google Scholar
• Fernald K, Kurokawa M. Evading apoptosis in cancer. Trends Cell Biol. 2013;23(12):620–633. doi: 10.1016/J.TCB.2013.07.006.
   PubMed Web of Science ®Google Scholar
• Campbell KJ, Leung HY. Evasion of cell death: a contributory factor in prostate cancer development and treatment resistance. Cancer Lett. 2021;520:213–221. doi: 10.1016/J.CANLET.2021.07.045.
   PubMed Web of Science ®Google Scholar
• Rathore R, McCallum JE, Varghese E, et al. Overcoming chemotherapy drug resistance by targeting inhibitors of apoptosis proteins (IAPs). Apoptosis. 2017;22(7):898–919. doi: 10.1007/S10495-017-1375-1.
   PubMed Web of Science ®Google Scholar
• Ozkan E, Bakar-Ates F. Ferroptosis: a trusted ally in combating drug resistance in cancer. Curr Med Chem. 2022;29(1):41–55. doi: 10.2174/0929867328666210810115812.
   PubMed Web of Science ®Google Scholar
• Janji B, Vallar L, Tanoury Z, et al. The actin filament cross-linker L-plastin confers resistance to TNF-alpha in MCF-7 breast cancer cells in a phosphorylation-dependent manner. J Cell Mol Med. 2010;14:1264–1275. doi: 10.1111/J.1582-4934.2009.00918.X.
   PubMed Web of Science ®Google Scholar
• [Reorganization of elements of the cytoskeletal and vacuolar systems in tumor cells in the early stage of developing multiple drug resistance]. PubMed; n.d. [accessed 2024 January 20]. https://pubmed.ncbi.nlm.nih.gov/9505346/.
   Google Scholar
• Zhao Y, Wang Z, Jiang Y, et al. Inactivation of Rac1 reduces Trastuzumab resistance in PTEN deficient and insulin-like growth factor I receptor overexpressing human breast cancer SKBR3 cells. Cancer Lett. 2011;313(1):54–63. doi: 10.1016/J.CANLET.2011.08.023.
   PubMed Web of Science ®Google Scholar
• Miao Z, Ali A, Hu L, et al. Microtubule actin cross-linking factor 1, a novel potential target in cancer. Cancer Sci. 2017;108(10):1953–1958. doi: 10.1111/CAS.13344.
   PubMed Web of Science ®Google Scholar
• Doostzadeh-Cizeron J, Yin S, Goodrich DW. Apoptosis induced by the nuclear death domain protein p84N5 is associated with caspase-6 and NF-kappa B activation. J Biol Chem. 2000;275(33):25336–25341. doi: 10.1074/JBC.M000793200.
   PubMed Web of Science ®Google Scholar
• Doostzadeh-Cizeron J, Terry NHA, Goodrich DW. The nuclear death domain protein p84N5 activates a G2/M cell cycle checkpoint prior to the onset of apoptosis. J Biol Chem. 2001;276(2):1127–1132. doi: 10.1074/JBC.M006944200.
   PubMed Web of Science ®Google Scholar
• Bonnal SC, López-Oreja I, Valcárcel J. Roles and mechanisms of alternative splicing in cancer - implications for care. Nat Rev Clin Oncol. 2020;17(8):457–474. doi: 10.1038/S41571-020-0350-X.
   PubMed Web of Science ®Google Scholar
• Wang E, Aifantis I. RNA splicing and cancer. Trends Cancer. 2020;6(8):631–644. doi: 10.1016/J.TRECAN.2020.04.011.
   PubMed Web of Science ®Google Scholar
• Montes M, Coiras M, Becerra S, et al. Functional consequences for apoptosis by transcription elongation regulator 1 (TCERG1)-mediated Bcl-x and Fas/CD95 alternative splicing. PLoS One. 2015;10(10):e0139812. doi: 10.1371/JOURNAL.PONE.0139812.
   PubMed Web of Science ®Google Scholar
• Liu Q, Sun Y, Long M, et al. DDX5 functions as a tumor suppressor in tongue cancer. Cancers (Basel). 2023;15(24):5882. doi: 10.3390/CANCERS15245882.
   PubMed Web of Science ®Google Scholar
• Kothandapani A, Dangeti VSMN, Brown AR, et al. Novel role of base excision repair in mediating cisplatin cytotoxicity. J Biol Chem. 2011;286(16):14564–14574. doi: 10.1074/JBC.M111.225375.
   PubMed Web of Science ®Google Scholar
• Kothandapani A, Sawant A, Dangeti VSMN, et al. Epistatic role of base excision repair and mismatch repair pathways in mediating cisplatin cytotoxicity. Nucleic Acids Res. 2013;41(15):7332–7343. doi: 10.1093/NAR/GKT479.
   PubMed Web of Science ®Google Scholar
• De Sousa VML, Carvalho L. Heterogeneity in lung cancer. Pathobiology. 2018;85(1–2):96–107. doi: 10.1159/000487440.
   PubMed Web of Science ®Google Scholar
• Goyal Y, Busch GT, Pillai M, et al. Diverse clonal fates emerge upon drug treatment of homogeneous cancer cells. Nature. 2023;620(7974):651–659. doi: 10.1038/S41586-023-06342-8.
   PubMed Web of Science ®Google Scholar
• Breen L, Keenan J, Clynes M. Generation of lung cancer cell line variants by drug selection or cloning. Methods Mol Biol. 2011;731:125–133. doi: 10.1007/978-1-61779-080-5_11.
   PubMedGoogle Scholar