721
Views
0
CrossRef citations to date
0
Altmetric
Pharmacology

Proteomic and metabolomic signatures of U87 glioblastoma cells treated with cisplatin and/or paclitaxel

ORCID Icon, , , , ORCID Icon, ORCID Icon, , ORCID Icon, , ORCID Icon & ORCID Icon show all
Article: 2305308 | Received 14 Sep 2023, Accepted 19 Dec 2023, Published online: 22 Jan 2024

References

  • Louis DN, Perry A, Wesseling P, et al. The 2021 WHO classification of tumors of the Central nervous system: a summary. Neuro Oncol. 2021;23(8):1–22. doi: 10.1093/neuonc/noab106.
  • Thakkar JP, Dolecek TA, Horbinski C, et al. Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol Biomarkers Prev. 2014;23(10):1985–1996. doi: 10.1158/1055-9965.EPI-14-0275.
  • Liu H, Liu B, Hou X, et al. Overexpression of NIMA-Related kinase 2 is associated with poor prognoses in malignant glioma. J Neurooncol. 2017;132(3):409–417. doi: 10.1007/s11060-017-2401-4.
  • Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–996. doi: 10.1056/NEJMoa043330.
  • Weller M, van den Bent M, Tonn JC, et al. European association for Neuro-Oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. The Lancet. Oncology. 2017;18(6):e315–e329. doi: 10.1016/S1470-2045(17)30194-8.
  • Zetterling M, Elf K, Semnic R, et al. Time course of neurological deficits after surgery for primary brain tumours. Acta Neurochir. 2020;162(12):3005–3018. doi: 10.1007/s00701-020-04425-3.
  • Lee SY. Temozolomide resistance in glioblastoma multiforme. Genes Dis. 2016;3(3):198–210. doi: 10.1016/j.gendis.2016.04.007.
  • Fetell MR, Grossman SA, Fisher JD, et al. Preirradiation paclitaxel in glioblastoma multiforme: efficacy, pharmacology, and drug interactions. New approaches to brain tumor therapy Central nervous system consortium. J Clin Oncol. 1997;15(9):3121–3128. doi: 10.1200/JCO.1997.15.9.3121.
  • Liu X, Sun K, Wang H, et al. Knockdown of retinoblastoma protein may sensitize glioma cells to cisplatin through inhibition of autophagy. Neurosci Lett. 2016;620:137–142. doi: 10.1016/j.neulet.2016.04.001.
  • Ozols RF, Bundy BN, Greer BE, et al. Phase III trial of carboplatin and paclitaxel compared with cisplatin and paclitaxel in patients with optimally resected stage III ovarian cancer: a gynecologic oncology group study. J Clin Oncol. 2003;21(17):3194–3200. doi: 10.1200/JCO.2003.02.153.
  • Kondagunta GV, Bacik J, Donadio A, et al. Combination of paclitaxel, ifosfamide, and cisplatin is an effective Second-Line therapy for patients with relapsed testicular germ cell tumors. J Clin Oncol. 2005;23(27):6549–6555. doi: 10.1200/JCO.2005.19.638.
  • Khan AB, D'Souza BJ, Wharam MD, et al. Cisplatin therapy in recurrent childhood brain tumors. Cancer Treat Rep. 1982;66(12):2013–2020.
  • Staff NP, Cavaletti G, Islam B, et al. Platinum-induced peripheral neurotoxicity: from pathogenesis to treatment. J Peripher Nerv Syst. 2019;24(Suppl 2):S26–S39. doi: 10.1111/jns.12335.
  • Jeremic B, Grujicic D, Jevremovic S, et al. Carboplatin and etoposide chemotherapy regimen for recurrent malignant glioma: a phase II study. J Clin Oncol. 1992;10(7):1074–1077. doi: 10.1200/JCO.1992.10.7.1074.
  • Launay-Vacher V, Rey J-B, Isnard-Bagnis C, et al. Prevention of cisplatin nephrotoxicity: state of the art and recommendations from the european society of clinical pharmacy special interest group on cancer care. Cancer Chemother Pharmacol. 2008;61(6):903–909. doi: 10.1007/s00280-008-0711-0.
  • Bouvier G, Penn RD, Kroin JS, et al. Stereotactic administration of intratumoral chronic chemotherapy of recurrent malignant gliomas. Appl Neurophysiol. 1987;50(1-6):223–226. doi: 10.1159/000100713.
  • Sheleg SV, Korotkevich EA, Zhavrid EA, et al. Local chemotherapy with cisplatin-Depot for glioblastoma multiforme. J Neurooncol. 2002;60(1):53–59. doi: 10.1023/A:1020288015457.
  • Bardal SK, Waechter JE, Martin DS. Applied pharmacology. St. Louis, MO: Elsevier/Saunders; 2011.
  • Joshi M, Liu X, Belani CP. Taxanes, past, present, and future impact on non-Small cell lung cancer. Anticancer Drugs. 2014;25(5):571–583. doi: 10.1097/CAD.0000000000000080.
  • Bookman MA. Optimal primary therapy of ovarian cancer. Ann Oncol. 2016;27(Suppl 1):i58–i62. doi: 10.1093/annonc/mdw088.
  • Bates D, Eastman A. Microtubule destabilising agents: far more than just antimitotic anticancer drugs. Br J Clin Pharmacol. 2017;83(2):255–268. doi: 10.1111/bcp.13126.
  • Yang C-PH, Horwitz SB. Taxol®: the first microtubule stabilizing agent. Int J Mol Sci. 2017;18(8):1733. doi: 10.3390/ijms18081733.
  • Tseng SH, Bobola MS, Berger MS, et al. Characterization of paclitaxel (taxol) sensitivity in human glioma- and Medulloblastoma-Derived cell lines. Neuro Oncol. 1999;1(2):101–108. doi: 10.1093/neuonc/1.2.101.
  • Zhang DY, Dmello C, Chen L, et al. Ultrasound-Mediated delivery of paclitaxel for glioma: a comparative study of distribution, toxicity, and efficacy of Albumin-Bound versus cremophor formulations. Clin Cancer Res. 2020;26(2):477–486. doi: 10.1158/1078-0432.CCR-19-2182.
  • Shi J, Mitchison TJ. Cell death response to anti-mitotic drug treatment in cell culture, mouse tumor model and the clinic. Endocr Relat Cancer. 2017;24(9):T83–T96. doi: 10.1530/ERC-17-0003.
  • Pei S, Wang X, Wang X, et al. Aberrant nuclear lamina contributes to the malignancy of human gliomas. J Genet Genomics. 2022;49(2):132–144. doi: 10.1016/j.jgg.2021.08.013.
  • Keener AB. Innovative therapies to tackle platinum-resistant ovarian cancer. Nature. 2021;600(7889):S45–S47. doi: 10.1038/d41586-021-03718-6.
  • Chamberlain MC, Kormanik P. Salvage chemotherapy with paclitaxel for recurrent primary brain tumors. J Clin Oncol. 1995;13(8):2066–2071. doi: 10.1200/JCO.1995.13.8.2066.
  • Chamberlain MC, Kormanik PA. Salvage chemotherapy with paclitaxel for recurrent oligodendrogliomas. J Clin Oncol. 1997;15(12):3427–3432. doi: 10.1200/JCO.1997.15.12.3427.
  • Roth AD, Maibach R, Martinelli G, et al. Docetaxel (taxotere)-cisplatin (TC): an effective drug combination in gastric carcinoma. Swiss group for clinical cancer research (SAKK), and the european institute of oncology (EIO). Ann Oncol. 2000;11(3):301–306. doi: 10.1023/a:1008342013224.
  • Muggia FM, Braly PS, Brady MF, et al. Phase III randomized study of cisplatin versus paclitaxel versus cisplatin and paclitaxel in patients with suboptimal stage III or IV ovarian cancer: a gynecologic oncology group study. J Clin Oncol. 2000;18(1):106–115. doi: 10.1200/JCO.2000.18.1.106.
  • Clark MJ, Homer N, O'Connor BD, et al. U87MG decoded: the genomic sequence of a cytogenetically aberrant human cancer cell line. PLoS Genet. 2010;6(1):e1000832. doi: 10.1371/journal.pgen.1000832.
  • Motaln H, Koren A, Gruden K, et al. Heterogeneous glioblastoma cell Cross-Talk promotes phenotype alterations and enhanced drug resistance. Oncotarget. 2015;6(38):40998–41017. doi: 10.18632/oncotarget.5701.
  • Liebmann JE, Cook JA, Lipschultz C, et al. Cytotoxic studies of paclitaxel (taxol) in human tumour cell lines. Br J Cancer. 1993;68(6):1104–1109. doi: 10.1038/bjc.1993.488.
  • Zenati RA, Giddey AD, Al-Hroub HM, et al. Evaluation of two simultaneous metabolomic and proteomic extraction protocols assessed by ultra-high-performance liquid chromatography tandem mass spectrometry. Int J Mol Sci. 2023;24(2):1354. doi: 10.3390/ijms24021354.
  • Ramagli LS, Rodriguez LV. Quantitation of microgram amounts of protein in two-Dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis. 1985;6(11):559–563. doi: 10.1002/elps.1150061109.
  • Rappsilber J, Mann M, Ishihama Y. Protocol for Micro-Purification, enrichment, Pre-Fractionation and storage of peptides for proteomics using StageTips. Nat Protoc. 2007;2(8):1896–1906. doi: 10.1038/nprot.2007.261.
  • Pang Z, Zhou G, Ewald J, et al. Using MetaboAnalyst 5.0 for LC–HRMS spectra processing, multi-omics integration and covariate adjustment of global metabolomics data. Nat Protoc. 2022;17(8):1735–1761. doi: 10.1038/s41596-022-00710-w.
  • Fernández LP, Merino M, Colmenarejo G, et al. Metabolic enzyme ACSL3 is a prognostic biomarker and correlates with anticancer effectiveness of statins in non-Small cell lung cancer. Mol Oncol. 2020;14(12):3135–3152. doi: 10.1002/1878-0261.12816.
  • Bowen SL, Bloor BK, Leigh IM, et al. Adducin expression in cutaneous and oral lesions: alpha- and beta-adducin transcripts down-Regulate with keratinocyte differentiation in stratified epithelia. J Pathol. 2003;201(1):119–126. doi: 10.1002/path.1389.
  • Wang J, Pan W. The biological role of the collagen alpha-3 (VI) chain and its cleaved C5 domain fragment endotrophin in cancer. Onco Targets Ther. 2020;13:5779–5793. doi: 10.2147/OTT.S256654.
  • Zhang M, Zhou Z, Liu Z, et al. Exploring the potential biomarkers for prognosis of glioblastoma via weighted gene Co-expression network analysis. PeerJ. 2022;10:e12768. doi: 10.7717/peerj.12768.
  • Ghosh D, Ulasov IV, Chen L, et al. TGFβ-Responsive HMOX1 expression is associated with stemness and invasion in glioblastoma multiforme. Stem Cells. 2016;34(9):2276–2289. doi: 10.1002/stem.2411.
  • Zhang L-Y, Guo Q, Guan G-F, et al. Integrin beta 5 is a prognostic biomarker and potential therapeutic target in glioblastoma. Front Oncol. 2019;9:904. doi: 10.3389/fonc.2019.00904.
  • Pedersen H, Anne Adanma Obara E, Elbæk KJ, et al. Replication protein A (RPA) mediates Radio-Resistance of glioblastoma cancer stem-like cells. Int J Mol Sci. 2020;21(5):1588. doi: 10.3390/ijms21051588.
  • Vauléon E, Tony A, Hamlat A, et al. Immune genes are associated with human glioblastoma pathology and patient survival. BMC Med Genomics. 2012;5(1):41. doi: 10.1186/1755-8794-5-41.
  • Vastrad B, Vastrad C, Kotturshetti I. Identification of key genes and signaling pathways associated with the progression of glioblastoma multiform; preprint. Genetic and Genomic Medicine. 2020; doi: 10.1101/2020.12.21.20248616.
  • Ye S, Wu J, Wang Y, et al. Quantitative proteomics analysis of glioblastoma cell lines after lncRNA HULC silencing. Sci Rep. 2021;11(1):12587. doi: 10.1038/s41598-021-92089-z.
  • Karakaş N, Topcu O, Tüzün E, et al. Immunoreactivity against SLC3A2 in high grade gliomas displays positive correlation with glioblastoma patient survival: potential target for glioma diagnosis and therapy. Preprint; Immunology. 2023. doi: 10.1101/2023.01.26.525653.
  • Jiang X, Gillen S, Esposito I, et al. Reduced expression of the membrane skeleton protein Beta1-Spectrin (SPTBN1) is associated with worsened prognosis in pancreatic cancer. Histol Histopathol. 2010;25(12):1497–1506. doi: 10.14670/HH-25.1497.
  • Lieu EL, Nguyen T, Rhyne S, et al. Amino acids in cancer. Exp Mol Med. 2020;52(1):15–30. doi: 10.1038/s12276-020-0375-3.
  • Wu C, Wangpaichitr M, Feun L, et al. Overcoming cisplatin resistance by mTOR inhibitor in lung cancer. Mol Cancer. 2005;4(1):25. doi: 10.1186/1476-4598-4-25.
  • Byrne BM, Oakley GG. Replication protein A, the laxative that keeps DNA regular: the importance of RPA phosphorylation in maintaining genome stability. Semin Cell Dev Biol. 2019;86:112–120. doi: 10.1016/j.semcdb.2018.04.005.
  • Giddey AD, de Kock E, Nakedi KC, et al. A temporal proteome dynamics study reveals the molecular basis of induced phenotypic resistance in Mycobacterium Smegmatis at Sub-Lethal rifampicin concentrations. Sci Rep. 2017;7(1):43858. doi: 10.1038/srep43858.
  • Pietras P, Aulas A, Fay MM, et al. Translation inhibition and suppression of stress granules formation by cisplatin. Biomed Pharmacother. 2022;145:112382. doi: 10.1016/j.biopha.2021.112382.
  • Melnikov SV, Söll D, Steitz TA, et al. Insights into RNA binding by the anticancer drug cisplatin from the crystal structure of cisplatin-modified ribosome. Nucleic Acids Res. 2016;44(10):4978–4987. doi: 10.1093/nar/gkw246.
  • Lewis-Tuffin LJ, Rodriguez F, Giannini C, et al. Misregulated E-Cadherin expression associated with an aggressive brain tumor phenotype. PLoS One. 2010;5(10):e13665. doi: 10.1371/journal.pone.0013665.
  • Alvarado AG, Turaga SM, Sathyan P, et al. Coordination of Self-Renewal in glioblastoma by integration of adhesion and microRNA signaling. Neuro Oncol. 2016;18(5):656–666. doi: 10.1093/neuonc/nov196.
  • Milanese C, Mastroberardino PG. A perspective on DNA damage-induced potentiation of the pentose phosphate shunt and reductive stress in chemoresistance. Mol Cell Oncol. 2020;7(3):1733383. doi: 10.1080/23723556.2020.1733383.
  • Jiang P, Du W, Wu M. Regulation of the pentose phosphate pathway in cancer. Protein Cell. 2014;5(8):592–602. doi: 10.1007/s13238-014-0082-8.
  • Catanzaro D, Gaude E, Orso G, et al. Inhibition of glucose-6-phosphate dehydrogenase sensitizes cisplatin-resistant cells to death. Oncotarget. 2015;6(30):30102–30114. doi: 10.18632/oncotarget.4945.
  • Muhammad N, Lee HM, Kim J. Oncology therapeutics targeting the metabolism of amino acids. Cells. 2020;9(8):1904. doi: 10.3390/cells9081904.
  • Palmer BF, Alpern RJ. Metabolic acidosis. In Comprehensive clinical nephrology. United States: Elsevier, 2010; pp 155–166. doi: 10.1016/B978-0-323-05876-6.00012-5.
  • Ai Z, Lu Y, Qiu S, et al. Overcoming cisplatin resistance of ovarian cancer cells by targeting HIF-1-regulated cancer metabolism. Cancer Lett. 2016;373(1):36–44. doi: 10.1016/j.canlet.2016.01.009.
  • Yi G-Z, Huang G, Guo M, et al. Acquired temozolomide resistance in MGMT-Deficient glioblastoma cells is associated with regulation of DNA repair by DHC2. Brain. 2019;142(8):2352–2366. doi: 10.1093/brain/awz202.
  • Li S, Topatana W, Juengpanich S, et al. Development of synthetic lethality in cancer: molecular and cellular classification. Sig Transduct Target Ther. 2020;5(1):241. doi: 10.1038/s41392-020-00358-6.
  • Bhutia YD, Babu E, Prasad PD, et al. The amino acid transporter SLC6A14 in cancer and its potential use in chemotherapy. Asian J Pharm Sci. 2014;9(6):293–303. doi: 10.1016/j.ajps.2014.04.004.
  • Honore S, Pasquier E, Braguer D. Understanding microtubule dynamics for improved cancer therapy. Cell Mol Life Sci. 2005;62(24):3039–3056. doi: 10.1007/s00018-005-5330-x.
  • Alexandre J, Batteux F, Nicco C, et al. Accumulation of hydrogen peroxide is an early and crucial step for paclitaxel-induced cancer cell death both in vitro and in vivo. Int J Cancer. 2006;119(1):41–48. doi: 10.1002/ijc.21685.
  • Digomann D, Linge A, Dubrovska A. SLC3A2/CD98hc, autophagy and tumor radioresistance: a link confirmed. Autophagy. 2019;15(10):1850–1851. doi: 10.1080/15548627.2019.1639302.
  • Goubert E, Mircheva Y, Lasorsa FM, et al. Inhibition of the mitochondrial glutamate carrier SLC25A22 in astrocytes leads to intracellular glutamate accumulation. Front Cell Neurosci. 2017;11:149. doi: 10.3389/fncel.2017.00149.
  • Kumari A. Beta oxidation of fatty acids. In Sweet biochemistry. Elsevier, 2018; pp 17–19. doi: 10.1016/B978-0-12-814453-4.00004-2.
  • Gerner EW, Meyskens FL. Polyamines and cancer: old molecules, new understanding. Nat Rev Cancer. 2004;4(10):781–792. doi: 10.1038/nrc1454.
  • Pless M, Belhadj K, Menssen HD, et al. Clinical efficacy, tolerability, and safety of SAM486A, a novel polyamine biosynthesis inhibitor, in patients with relapsed or refractory non-Hodgkin’s lymphoma: results from a phase II multicenter study. Clin Cancer Res. 2004;10(4):1299–1305. doi: 10.1158/1078-0432.ccr-0977-03.
  • Nowotarski SL, Woster PM, Casero RA. Polyamines and cancer: implications for chemotherapy and chemoprevention. Expert Rev Mol Med. 2013;15:e3. doi: 10.1017/erm.2013.3.
  • Pegg AE. Functions of polyamines in mammals. J Biol Chem. 2016;291(29):14904–14912. doi: 10.1074/jbc.R116.731661.
  • Bensaad K, Favaro E, Lewis CA, et al. Fatty acid uptake and lipid storage induced by HIF-1α contribute to cell growth and survival after Hypoxia-Reoxygenation. Cell Rep. 2014;9(1):349–365. doi: 10.1016/j.celrep.2014.08.056.
  • Park JK, Coffey NJ, Limoges A, et al. The heterogeneity of lipid metabolism in cancer. In The heterogeneity of cancer metabolism. In Le, A., Ed.; Advances in Experimental Medicine and Biology. Cham: Springer International Publishing; 2021; Vol. 1311, pp 39–56. doi: 10.1007/978-3-030-65768-0_3.
  • Yang WS, Moon H-G, Kim HS, et al. Proteomic approach reveals FKBP4 and S100A9 as potential prediction markers of therapeutic response to neoadjuvant chemotherapy in patients with breast cancer. J Proteome Res. 2012;11(2):1078–1088. doi: 10.1021/pr2008187.
  • Lee PJ, Jiang B-H, Chin BY, et al. Hypoxia-Inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J Biol Chem. 1997;272(9):5375–5381. doi: 10.1074/jbc.272.9.5375.
  • Yang Z-Z, Zou A-P. Transcriptional regulation of heme oxygenases by HIF-1α in renal medullary interstitial cells. Am J Physiol Renal Physiol. 2001;281(5):F900–F908. doi: 10.1152/ajprenal.2001.281.5.F900.
  • Yang L, Lin K, Zhu L, et al. Long non-coding RNA DARS-AS1 promotes tumor progression by directly suppressing PACT-Mediated cellular stress. Commun Biol. 2022;5(1):822. doi: 10.1038/s42003-022-03778-y.
  • Chan P-C, Hsu RYC, Liu C-W, et al. Adducin-1 is essential for mitotic spindle assembly through its interaction with Myosin-X. J Cell Biol. 2014;204(1):19–28. doi: 10.1083/jcb.201306083.
  • Poon M-W, Zhuang JTF, Wong STS, et al. Co-expression of cytoskeletal protein adducin 3 and CD133 in neurospheres and a Temozolomide-Resistant subclone of glioblastoma. Anticancer Res. 2015;35(12):6487–6495.
  • Ipata PL. Origin, utilization, and recycling of nucleosides in the Central nervous system. Adv Physiol Educ. 2011;35(4):342–346. doi: 10.1152/advan.00068.2011.
  • Purohit A, Singh A, Ghilchik MW, et al. Inhibition of tumor necrosis factor Alpha-Stimulated aromatase activity by microtubule-Stabilizing agents, paclitaxel and 2-Methoxyestradiol. Biochem Biophys Res Commun. 1999;261(1):214–217. doi: 10.1006/bbrc.1999.1010.
  • Mondragón JA, Serrano Y, Torres A, et al. Glioblastoma cells express crucial enzymes involved in androgen synthesis: 3β-Hydroxysteroid dehydrogenase, 17–20α-Hydroxylase, 17β-Hydroxysteroid dehydrogenase and 5α-Reductase. Endocrinol Diabetes Metab. 2021;4(4):e00289. doi: 10.1002/edm2.289.
  • Contreras-Zárate MJ, Cittelly DM. Sex steroid hormone function in the brain niche: implications for brain metastatic colonization and progression. Cancer Rep. 2022;5(4):e1241. doi: 10.1002/cnr2.1241.