The rediscovery of platinum-based cancer therapy.
Journal
Nature reviews. Cancer
ISSN: 1474-1768
Titre abrégé: Nat Rev Cancer
Pays: England
ID NLM: 101124168
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
accepted:
22
09
2020
pubmed:
1
11
2020
medline:
2
2
2021
entrez:
31
10
2020
Statut:
ppublish
Résumé
Platinum (Pt) compounds entered the clinic as anticancer agents when cisplatin was approved in 1978. More than 40 years later, even in the era of precision medicine and immunotherapy, Pt drugs remain among the most widely used anticancer drugs. As Pt drugs mainly target DNA, it is not surprising that recent insights into alterations of DNA repair mechanisms provide a useful explanation for their success. Many cancers have defective DNA repair, a feature that also sheds new light on the mechanisms of secondary drug resistance, such as the restoration of DNA repair pathways. In addition, genome-wide functional screening approaches have revealed interesting insights into Pt drug uptake. About half of cisplatin and carboplatin but not oxaliplatin may enter cells through the widely expressed volume-regulated anion channel (VRAC). The analysis of this heteromeric channel in tumour biopsies may therefore be a useful biomarker to stratify patients for initial Pt treatments. Moreover, Pt-based approaches may be improved in the future by the optimization of combinations with immunotherapy, management of side effects and use of nanodelivery devices. Hence, Pt drugs may still be part of the standard of care for several cancers in the coming years.
Identifiants
pubmed: 33128031
doi: 10.1038/s41568-020-00308-y
pii: 10.1038/s41568-020-00308-y
doi:
Substances chimiques
Antineoplastic Agents
0
Organoplatinum Compounds
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
37-50Références
US Food and Drug Administration. Drugs@FDA: FDA-approved drugs. New drug application (NDA): 018057 (FDA, 2019).
Kelland, L. The resurgence of platinum-based cancer chemotherapy. Nat. Rev. Cancer 7, 573–584 (2007).
pubmed: 17625587
doi: 10.1038/nrc2167
Kauffman, G. B., Pentimalli, R., Doldi, S. & Hall, M. D. Michele Peyrone (1813–1883), discoverer of cisplatin. Platin Met. Rev. 54, 250–256 (2010).
doi: 10.1595/147106710X534326
Rosenberg, B., van Camp, L. & Krigas, T. Inhibition of cell division in Escherichia coli by electrolysis products from a platinum electrode. Nature 205, 698–699 (1965).
pubmed: 14287410
doi: 10.1038/205698a0
Wiltshaw, E. Cisplatin in the treatment of cancer. Platin Met. Rev. 23, 90–98 (1979).
US Food and Drug Administration. Drugs@FDA: FDA-approved drugs. Abbreviated new drug application (ANDA): 077139 (FDA, 2012).
Perego, P. & Robert, J. Oxaliplatin in the era of personalized medicine: from mechanistic studies to clinical efficacy. Cancer Chemother. Pharmacol. 77, 5–18 (2016).
pubmed: 26589793
doi: 10.1007/s00280-015-2901-x
Dilruba, S. & Kalayda, G. V. Platinum-based drugs: past, present and future. Cancer Chemother. Pharmacol. 77, 1103–1124 (2016).
pubmed: 26886018
doi: 10.1007/s00280-016-2976-z
Lippard, S. J. New chemistry of an old molecule: cis-[Pt(NH
pubmed: 6890712
doi: 10.1126/science.6890712
Wang, D. & Lippard, S. J. Cellular processing of platinum anticancer drugs. Nat. Rev. Drug Discov. 4, 307–320 (2005).
pubmed: 15789122
doi: 10.1038/nrd1691
Burger, H. et al. Drug transporters of platinum-based anticancer agents and their clinical significance. Drug Resist. Updat. 14, 22–34 (2011).
pubmed: 21251871
doi: 10.1016/j.drup.2010.12.002
Borst, P., Rottenberg, S. & Jonkers, J. How do real tumors become resistant to cisplatin? Cell Cycle 7, 1353–1359 (2008).
pubmed: 18418074
doi: 10.4161/cc.7.10.5930
Sakai, W. et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature 451, 1116–1120 (2008). This study shows that secondary intragenic BRCA2 mutations restore the wild-type reading frame as a mechanism of resistance to cisplatin in cancer cell lines and clinical specimens.
pubmed: 18264087
pmcid: 2577037
doi: 10.1038/nature06633
Zhao, W., Wiese, C., Kwon, Y., Hromas, R. & Sung, P. The BRCA tumor suppressor network in chromosome damage repair by homologous recombination. Annu. Rev. Biochem. 88, 221–245 (2019).
pubmed: 30917004
pmcid: 7004434
doi: 10.1146/annurev-biochem-013118-111058
Harris, A. L. DNA repair and resistance to chemotherapy. Cancer Surv. 4, 601–624 (1985).
pubmed: 3916657
Lord, C. J. & Ashworth, A. The DNA damage response and cancer therapy. Nature 481, 287–294 (2012).
pubmed: 22258607
doi: 10.1038/nature10760
Nickoloff, J. A., Jones, D., Lee, S. H., Williamson, E. A. & Hromas, R. Drugging the cancers addicted to DNA repair. J. Natl. Cancer Inst. 109, djx059 (2017).
pmcid: 5436301
doi: 10.1093/jnci/djx059
Miki, Y. et al. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266, 66–71 (1994).
pubmed: 7545954
doi: 10.1126/science.7545954
Wooster, R. et al. Identification of the breast cancer susceptibility gene BRCA2. Nature 378, 789–792 (1995).
pubmed: 8524414
doi: 10.1038/378789a0
Nik-Zainal, S. et al. Landscape of somatic mutations in 560 breast cancer whole-genome sequences. Nature 534, 47–54 (2016).
pubmed: 27135926
pmcid: 4910866
doi: 10.1038/nature17676
von Minckwitz, G. et al. Neoadjuvant carboplatin in patients with triple-negative and HER2-positive early breast cancer (GeparSixto; GBG 66): a randomised phase 2 trial. Lancet Oncol. 15, 747–756 (2014).
doi: 10.1016/S1470-2045(14)70160-3
Telli, M. L. et al. Homologous recombination deficiency (HRD) score predicts response to platinum-containing neoadjuvant chemotherapy in patients with triple-negative breast cancer. Clin. Cancer Res. 22, 3764–3773 (2016).
pubmed: 26957554
pmcid: 6773427
doi: 10.1158/1078-0432.CCR-15-2477
Silver, D. P. et al. Efficacy of neoadjuvant cisplatin in triple-negative breast cancer. J. Clin. Oncol. 28, 1145–1153 (2010).
pubmed: 20100965
pmcid: 2834466
doi: 10.1200/JCO.2009.22.4725
Vollebergh, M. A. et al. An aCGH classifier derived from BRCA1-mutated breast cancer and benefit of high-dose platinum-based chemotherapy in HER2-negative breast cancer patients. Ann. Oncol. 22, 1561–1570 (2011).
pubmed: 21135055
doi: 10.1093/annonc/mdq624
Vollebergh, M. A. et al. Genomic patterns resembling BRCA1- and BRCA2-mutated breast cancers predict benefit of intensified carboplatin-based chemotherapy. Breast Cancer Res. 16, R47 (2014).
pubmed: 24887359
pmcid: 4076636
doi: 10.1186/bcr3655
Bryant, H. E. et al. Specific killing of BRCA2-deficient tumors with inhibitors of poly(ADP-ribose) polymerase. Nature 434, 913–917 (2005).
doi: 10.1038/nature03443
pubmed: 15829966
Farmer, H. et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434, 917–921 (2005).
pubmed: 15829967
doi: 10.1038/nature03445
Ledermann, J. et al. Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol. 15, 852–861 (2014).
pubmed: 24882434
doi: 10.1016/S1470-2045(14)70228-1
Ledermann, J. A. & Pujade-Lauraine, E. Olaparib as maintenance treatment for patients with platinum-sensitive relapsed ovarian cancer. Ther. Adv. Med. Oncol. 11, 1758835919849753 (2019).
pubmed: 31205507
pmcid: 6535754
doi: 10.1177/1758835919849753
Welsh, C. et al. Reduced levels of XPA, ERCC1 and XPF DNA repair proteins in testis tumor cell lines. Int. J. Cancer 110, 352–361 (2004).
pubmed: 15095299
doi: 10.1002/ijc.20134
Fenske, A. E. et al. Cisplatin resistance induced in germ cell tumor cells is due to reduced susceptibility towards cell death but not to altered DNA damage induction or repair. Cancer Lett. 324, 171–178 (2012).
pubmed: 22613583
doi: 10.1016/j.canlet.2012.05.009
Bagrodia, A. et al. Genetic determinants of cisplatin resistance in patients with advanced germ cell tumors. J. Clin. Oncol. 34, 4000–4007 (2016).
pubmed: 27646943
pmcid: 5477828
doi: 10.1200/JCO.2016.68.7798
Luvero, D. et al. Ovarian cancer relapse: from the latest scientific evidence to the best practice. Crit. Rev. Oncol. Hematol. 140, 28–38 (2019).
pubmed: 31176270
doi: 10.1016/j.critrevonc.2019.05.014
Lo Russo, G., Imbimbo, M. & Garassino, M. C. Is the chemotherapy era in advanced non-small cell lung cancer really over? Maybe not yet. Tumori 3, 223–225 (2016).
doi: 10.5301/tj.5000479
Gately, D. P. & Howell, S. B. Cellular accumulation of the anticancer agent cisplatin: a review. Br. J. Cancer 67, 1171–1176 (1993).
pubmed: 8512802
pmcid: 1968522
doi: 10.1038/bjc.1993.221
Harrach, S. & Ciarimboli, G. Role of transporters in the distribution of platinum-based drugs. Front. Pharmacol. 6, 85 (2015).
pubmed: 25964760
pmcid: 4408848
doi: 10.3389/fphar.2015.00085
Pan, B. F., Sweet, D. H., Pritchard, J. B., Chen, R. & Nelson, J. A. A transfected cell model for the renal toxin transporter, rOCT2. Toxicol. Sci. 47, 181–186 (1999).
pubmed: 10220855
doi: 10.1093/toxsci/47.2.181
Jong, N. N., Nakanishi, T., Liu, J. J., Tamai, I. & McKeage, M. J. Oxaliplatin transport mediated by organic cation/carnitine transporters OCTN1 and OCTN2 in overexpressing human embryonic kidney 293 cells and rat dorsal root ganglion neurons. J. Pharmacol. Exp. Ther. 338, 537–547 (2011).
pubmed: 21606177
doi: 10.1124/jpet.111.181297
Ishida, S., Lee, J., Thiele, D. J. & Herskowitz, I. Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctr1 in yeast and mammals. Proc. Natl Acad. Sci. USA 99, 14298–14302 (2002).
pubmed: 12370430
doi: 10.1073/pnas.162491399
pmcid: 137878
Wen, X. et al. Transgenic expression of the human MRP2 transporter reduces cisplatin accumulation and nephrotoxicity in Mrp2-null mice. Am. J. Pathol. 184, 1299–1308 (2014).
pubmed: 24641901
pmcid: 4005989
doi: 10.1016/j.ajpath.2014.01.025
Myint, K., Li, Y., Paxton, J. & McKeage, M. Multidrug resistance-associated protein 2 (MRP2) mediated transport of oxaliplatin-derived platinum in membrane vesicles. PLoS ONE 10, e0130727 (2015).
pubmed: 26131551
pmcid: 4488857
doi: 10.1371/journal.pone.0130727
Myint, K. et al. Identification of MRP2 as a targetable factor limiting oxaliplatin accumulation and response in gastrointestinal cancer. Sci. Rep. 9, 2245 (2019).
pubmed: 30783141
pmcid: 6381153
doi: 10.1038/s41598-019-38667-8
Hall, M. D., Okabe, M., Shen, D. W., Liang, X. J. & Gottesman, M. M. The role of cellular accumulation in determining sensitivity to platinum-based chemotherapy. Annu. Rev. Pharmacol. Toxicol. 48, 495–535 (2008).
pubmed: 17937596
doi: 10.1146/annurev.pharmtox.48.080907.180426
De Luca, A. et al. A structure-based mechanism of cisplatin resistance mediated by glutathione transferase P1-1. Proc. Natl Acad. Sci. USA 116, 13943–13951 (2019).
pubmed: 31221747
doi: 10.1073/pnas.1903297116
pmcid: 6628828
Planells-Cases, R. et al. Subunit composition of VRAC channels determines substrate specificity and cellular resistance to Pt-based anti-cancer drugs. EMBO J. 34, 2993–3008 (2015). This study demonstrates that around 50% of cisplatin uptake is dependent on the LRRC8A and LRRC8D VRAC subunits.
pubmed: 26530471
pmcid: 4687416
doi: 10.15252/embj.201592409
He, Y. J. et al. DYNLL1 binds to MRE11 to limit DNA end resection in BRCA1-deficient cells. Nature 563, 522–526 (2018).
pubmed: 30464262
pmcid: 7155769
doi: 10.1038/s41586-018-0670-5
Sorensen, B. H., Dam, C. S., Sturup, S. & Lambert, I. H. Dual role of LRRC8A-containing transporters on cisplatin resistance in human ovarian cancer cells. J. Inorg. Biochem. 160, 287–295 (2016).
pubmed: 27112899
doi: 10.1016/j.jinorgbio.2016.04.004
Perez, R. P. Cellular and molecular determinants of cisplatin resistance. Eur. J. Cancer 34, 1535–1542 (1998).
pubmed: 9893624
doi: 10.1016/S0959-8049(98)00227-5
Cossa, G., Gatti, L., Zunino, F. & Perego, P. Strategies to improve the efficacy of platinum compounds. Curr. Med. Chem. 16, 2355–2365 (2009).
pubmed: 19601785
doi: 10.2174/092986709788682083
Perego, P. et al. Association between cisplatin resistance and mutation of p53 gene and reduced bax expression in ovarian carcinoma cell systems. Cancer Res. 56, 556–562 (1996).
pubmed: 8564971
Wu, A. Y. et al. Fn14 overcomes cisplatin resistance of high-grade serous ovarian cancer by promoting Mdm2-mediated p53-R248Q ubiquitination and degradation. J. Exp. Clin. Cancer Res. 38, 176 (2019).
pubmed: 31023317
pmcid: 6485139
doi: 10.1186/s13046-019-1171-6
Hanna, N. H. & Einhorn, L. H. Testicular cancer — discoveries and updates. N. Engl. J. Med. 371, 2005–2016 (2014).
pubmed: 25409373
doi: 10.1056/NEJMra1407550
Swisher, E. M. et al. Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Res. 68, 2581–2586 (2008). This study describes secondary BRCA1 mutations as a mechanism of resistance to cisplatin in ovarian carcinoma clinical specimens.
pubmed: 18413725
pmcid: 2674369
doi: 10.1158/0008-5472.CAN-08-0088
Rottenberg, S. et al. Selective induction of chemotherapy resistance of mammary tumors in a conditional mouse model for hereditary breast cancer. Proc. Natl Acad. Sci. USA 104, 12117–12122 (2007).
pubmed: 17626183
doi: 10.1073/pnas.0702955104
pmcid: 1914039
Pajic, M. et al. Selected alkylating agents can overcome drug tolerance of G0-like tumor cells and eradicate BRCA1-deficient mammary tumors in mice. Clin. Cancer Res. 23, 7020–7033 (2017).
pubmed: 28821557
doi: 10.1158/1078-0432.CCR-17-1279
Jaspers, J. E. et al. Loss of 53BP1 causes PARP inhibitor resistance in Brca1-mutated mouse mammary tumors. Cancer Discov. 3, 68–81 (2013).
pubmed: 23103855
doi: 10.1158/2159-8290.CD-12-0049
Cavallo, F. et al. Reduced proficiency in homologous recombination underlies the high sensitivity of embryonal carcinoma testicular germ cell tumors to cisplatin and poly(ADP-ribose) polymerase inhibition. PLoS ONE 7, e51563 (2012).
pubmed: 23251575
pmcid: 3520950
doi: 10.1371/journal.pone.0051563
Chaudhuri, A. R. et al. Replication fork stability confers chemoresistance in BRCA-deficient cells. Nature 535, 382–387 (2016). This paper demonstrates the relevance of replication fork stability as a determinant of resistance to cisplatin.
pmcid: 4959813
doi: 10.1038/nature18325
Becker, J. R. et al. The ASCIZ–DYNLL1 axis promotes 53BP1-dependent non-homologous end joining and PARP inhibitor sensitivity. Nat. Commun. 9, 5406 (2018).
pubmed: 30559443
pmcid: 6297349
doi: 10.1038/s41467-018-07855-x
Elaimy, A. L. et al. The VEGF receptor neuropilin 2 promotes homologous recombination by stimulating YAP/TAZ-mediated Rad51 expression. Proc. Natl Acad. Sci. USA 116, 14174–14180 (2019).
pubmed: 31235595
doi: 10.1073/pnas.1821194116
pmcid: 6628806
Liptay, M., Barbosa, J. S. & Rottenberg, S. Replication fork remodeling and therapy escape in DNA damage response-deficient cancers. Front. Oncol. 10, 670 (2020).
pubmed: 32432041
pmcid: 7214843
doi: 10.3389/fonc.2020.00670
Schlacher, K. et al. Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145, 529–542 (2011).
pubmed: 21565612
pmcid: 3261725
doi: 10.1016/j.cell.2011.03.041
Li, Q. et al. ERCC2 helicase domain mutations confer nucleotide excision repair deficiency and drive cisplatin sensitivity in muscle-invasive bladder cancer. Clin. Cancer Res. 25, 977–988 (2019).
pubmed: 29980530
doi: 10.1158/1078-0432.CCR-18-1001
Wojtaszek, J. L. et al. A small molecule targeting mutagenic translesion synthesis improves chemotherapy. Cell 178, 152–159.e11 (2019). This study identifies the first compound that sensitizes cells to cisplatin while inhibiting REV1-dependent mutagenic TLS.
pubmed: 31178121
pmcid: 6644000
doi: 10.1016/j.cell.2019.05.028
Kuczynski, E. A., Sargent, D. J., Grothey, A. & Kerbel, R. S. Drug rechallenge and treatment beyond progression — implications for drug resistance. Nat. Rev. Clin. Oncol. 10, 571–587 (2013).
pubmed: 23999218
pmcid: 4540602
doi: 10.1038/nrclinonc.2013.158
Glasspool, R. M., Teodoridis, J. M. & Brown, R. Epigenetics as a mechanism driving polygenic clinical drug resistance. Br. J. Cancer 94, 1087–1092 (2006).
pubmed: 16495912
pmcid: 2361257
doi: 10.1038/sj.bjc.6603024
Sharma, S. V. et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69–80 (2010). This paper demonstrates the occurrence of unstable and non-hereditable drug resistance upon cisplatin treatment.
pubmed: 20371346
pmcid: 2851638
doi: 10.1016/j.cell.2010.02.027
Borst, P. Cancer drug pan-resistance: pumps, cancer stem cells, quiescence, epithelial to mesenchymal transition, blocked cell death pathways, persisters or what? Open Biol. 2, 120066 (2012).
pubmed: 22724067
pmcid: 3376736
doi: 10.1098/rsob.120066
Clevers, H. The cancer stem cell: premises, promises and challenges. Nat. Med. 17, 313–319 (2011).
pubmed: 21386835
doi: 10.1038/nm.2304
Sharma, A. et al. Longitudinal single-cell RNA sequencing of patient-derived primary cells reveals drug-induced infidelity in stem cell hierarchy. Nat. Commun. 9, 4931 (2018).
pubmed: 30467425
pmcid: 6250721
doi: 10.1038/s41467-018-07261-3
Hou, M. F. et al. The NuRD complex-mediated p21 suppression facilitates chemoresistance in BRCA-proficient breast cancer. Exp. Cell Res. 359, 458–465 (2017).
pubmed: 28842166
doi: 10.1016/j.yexcr.2017.08.029
Guillemette, S. et al. Resistance to therapy in BRCA2 mutant cells due to loss of the nucleosome remodeling factor CHD4. Genes Dev. 29, 489–494 (2015).
pubmed: 25737278
pmcid: 4358401
doi: 10.1101/gad.256214.114
Almeida, L. O. et al. NFκB mediates cisplatin resistance through histone modifications in head and neck squamous cell carcinoma (HNSCC). FEBS Open Bio 4, 96–104 (2013).
pubmed: 24490130
pmcid: 3907686
doi: 10.1016/j.fob.2013.12.003
Hu, S. et al. Overexpression of EZH2 contributes to acquired cisplatin resistance in ovarian cancer cells in vitro and in vivo. Cancer Biol. Ther. 10, 788–795 (2010).
pubmed: 20686362
doi: 10.4161/cbt.10.8.12913
Brown, R., Curry, E., Magnani, L., Wilhelm-Benartzi, C. S. & Borley, J. Poised epigenetic states and acquired drug resistance in cancer. Nat. Rev. Cancer 14, 747–753 (2014).
pubmed: 25253389
doi: 10.1038/nrc3819
Rottenberg, S. et al. Impact of intertumoral heterogeneity on predicting chemotherapy response of BRCA1-deficient mammary tumors. Cancer Res. 72, 2350–2361 (2012).
pubmed: 22396490
pmcid: 3518318
doi: 10.1158/0008-5472.CAN-11-4201
Schouten, P. C. et al. High XIST and low 53BP1 expression predict poor outcome after high-dose alkylating chemotherapy in patients with a BRCA1-like breast cancer. Mol. Cancer Ther. 15, 190–198 (2016).
pubmed: 26637364
doi: 10.1158/1535-7163.MCT-15-0470
Sun, W., Zu, Y., Fu, X. & Deng, Y. Knockdown of lncRNA-XIST enhances the chemosensitivity of NSCLC cells via suppression of autophagy. Oncol. Rep. 38, 3347–3354 (2017).
pubmed: 29130102
pmcid: 5783579
Cassinelli, G. et al. Targeting the Akt kinase to modulate survival, invasiveness and drug resistance of cancer cells. Curr. Med. Chem. 20, 1923–1945 (2013).
pubmed: 23410153
doi: 10.2174/09298673113209990106
Cossa, G. et al. Modulation of sensitivity to antitumor agents by targeting the MAPK survival pathway. Curr. Pharm. Des. 19, 883–894 (2013).
pubmed: 22973957
doi: 10.2174/138161213804547187
Jin, L. et al. MAST1 drives cisplatin resistance in human cancers by rewiring cRaf-independent MEK activation. Cancer Cell 34, 315–330.e7 (2018). This study strengthens the relevance of pathways inhibiting cisplatin-induced apoptosis in drug resistance, providing new options for treating resistant cancers with activation of survival pathways.
pubmed: 30033091
pmcid: 6092215
doi: 10.1016/j.ccell.2018.06.012
Cossa, G. et al. Differential outcome of MEK1/2 inhibitor–platinum combinations in platinum-sensitive and -resistant ovarian carcinoma cells. Cancer Lett. 347, 212–224 (2014).
pubmed: 24576622
doi: 10.1016/j.canlet.2014.02.016
Ishibashi, M. et al. Tyrosine kinase receptor TIE-1 mediates platinum resistance by promoting nucleotide excision repair in ovarian cancer. Sci. Rep. 8, 13207 (2018).
pubmed: 30181600
pmcid: 6123490
doi: 10.1038/s41598-018-31069-2
Olive, K. P. et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324, 1457–1461 (2009).
pubmed: 19460966
pmcid: 2998180
doi: 10.1126/science.1171362
Coffelt, S. B. & de Visser, K. E. Immune-mediated mechanisms influencing the efficacy of anticancer therapies. Trends Immunol. 36, 198–216 (2015).
pubmed: 25857662
doi: 10.1016/j.it.2015.02.006
Wu, T. & Dai, Y. Tumor microenvironment and therapeutic response. Cancer Lett. 387, 61–68 (2017).
pubmed: 26845449
doi: 10.1016/j.canlet.2016.01.043
Wang, W. et al. Effector T cells abrogate stroma-mediated chemoresistance in ovarian cancer. Cell 165, 1092–1105 (2016). This study shows that cisplatin resistance can occur by a non-genetic mechanism in the TME in which CAFs regulate thiol metabolism, thereby impairing cisplatin accumulation in ovarian cancer cells.
pubmed: 27133165
pmcid: 4874853
doi: 10.1016/j.cell.2016.04.009
Diaz-Maroto, N. G. et al. Noncanonical TGFβ pathway relieves the blockade of IL1β/TGFβ-mediated crosstalk between tumor and stroma: TGFBR1 and TAK1 inhibition in colorectal cancer. Clin. Cancer Res. 25, 4466–4479 (2019).
doi: 10.1158/1078-0432.CCR-18-3957
Dijkgraaf, E. M. et al. Chemotherapy alters monocyte differentiation to favor generation of cancer-supporting M2 macrophages in the tumor microenvironment. Cancer Res. 73, 2480–2492 (2013).
pubmed: 23436796
doi: 10.1158/0008-5472.CAN-12-3542
Sommariva, M. et al. TLR9 agonists oppositely modulate DNA repair genes in tumor versus immune cells and enhance chemotherapy effects. Cancer Res. 71, 6382–6390 (2011).
pubmed: 21878529
doi: 10.1158/0008-5472.CAN-11-1285
Iida, N. et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342, 967–970 (2013). This study shows in mouse models of cancer that an intact microbiota is required for optimal activity of oxaliplatin, which is associated with induction of ROS contributed by tumour-infiltrating myeloid cells.
pubmed: 24264989
pmcid: 6709532
doi: 10.1126/science.1240527
Bienvenu, P., Caron, L., Gasparutto, D. & Kergonou, J. F. Assessing and counteracting the prooxidant effects of anticancer drugs. EXS 62, 257–265 (1992).
pubmed: 1280494
Socinski, M. A. et al. Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC. N. Engl. J. Med. 378, 2288–2301 (2018).
pubmed: 29863955
doi: 10.1056/NEJMoa1716948
West, H. et al. Atezolizumab in combination with carboplatin plus nab-paclitaxel chemotherapy compared with chemotherapy alone as first-line treatment for metastatic non-squamous non-small-cell lung cancer (IMpower130): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol. 20, 924–937 (2019).
doi: 10.1016/S1470-2045(19)30167-6
pubmed: 31122901
Gandhi, L. et al. Pembrolizumab plus chemotherapy in metastatic non-small-cell lung cancer. N. Engl. J. Med. 378, 2078–2092 (2018).
pubmed: 29658856
doi: 10.1056/NEJMoa1801005
Schmid, P. et al. Pembrolizumab for early triple-negative breast cancer. N. Engl. J. Med. 382, 810–821 (2020).
pubmed: 32101663
doi: 10.1056/NEJMoa1910549
Le, D. T. et al. PD-1 blockade in tumors with mismatch-repair deficiency. N. Engl. J. Med. 372, 2509–2520 (2015).
pubmed: 26028255
pmcid: 4481136
doi: 10.1056/NEJMoa1500596
Paz-Ares, L. et al. Durvalumab plus platinum–etoposide versus platinum–etoposide in first-line treatment of extensive-stage small-cell lung cancer (CASPIAN): a randomised, controlled, open-label, phase 3 trial. Lancet 394, 1929–1939 (2019).
pubmed: 31590988
doi: 10.1016/S0140-6736(19)32222-6
Kroon, P. et al. Radiotherapy and cisplatin increase immunotherapy efficacy by enabling local and systemic intratumoral T-cell activity. Cancer Immunol. Res. 7, 670–682 (2019).
pubmed: 30782666
doi: 10.1158/2326-6066.CIR-18-0654
Ramakrishnan, R. et al. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J. Clin. Invest. 120, 1111–1124 (2010).
pubmed: 20234093
pmcid: 2846048
doi: 10.1172/JCI40269
Galluzzi, L., Buque, A., Kepp, O., Zitvogel, L. & Kroemer, G. Immunogenic cell death in cancer and infectious disease. Nat. Rev. Immunol. 17, 97–111 (2017).
pubmed: 27748397
doi: 10.1038/nri.2016.107
Ghiringhelli, F. et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1β-dependent adaptive immunity against tumors. Nat. Med. 15, 1170–1178 (2009).
pubmed: 19767732
doi: 10.1038/nm.2028
Obeid, M. et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13, 54–61 (2007).
pubmed: 17187072
doi: 10.1038/nm1523
Tesniere, A. et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 29, 482–491 (2010).
pubmed: 19881547
doi: 10.1038/onc.2009.356
Munn, D. H. & Bronte, V. Immune suppressive mechanisms in the tumor microenvironment. Curr. Opin. Immunol. 39, 1–6 (2016).
pubmed: 26609943
doi: 10.1016/j.coi.2015.10.009
de Biasi, A. R., Villena-Vargas, J. & Adusumilli, P. S. Cisplatin-induced antitumor immunomodulation: a review of preclinical and clinical evidence. Clin. Cancer Res. 20, 5384–5391 (2014).
pubmed: 25204552
pmcid: 4216745
doi: 10.1158/1078-0432.CCR-14-1298
Galluzzi, L., Buque, A., Kepp, O., Zitvogel, L. & Kroemer, G. Immunological effects of conventional chemotherapy and targeted anticancer agents. Cancer Cell 28, 690–714 (2015).
pubmed: 26678337
doi: 10.1016/j.ccell.2015.10.012
Lesterhuis, W. J. et al. Platinum-based drugs disrupt STAT6-mediated suppression of immune responses against cancer in humans and mice. J. Clin. Invest. 121, 3100–3108 (2011). This study highlights the capability of Pt compounds to down-modulate immunosuppressive molecules, particularly PDL2.
pubmed: 21765211
pmcid: 3148725
doi: 10.1172/JCI43656
Blatter, S. et al. Chemotherapy induces an immunosuppressive gene expression signature in residual BRCA1/p53-deficient mouse mammary tumors. J. Mol. Clin. Med. 1, 7–17 (2018).
Grabosch, S. et al. Cisplatin-induced immune modulation in ovarian cancer mouse models with distinct inflammation profiles. Oncogene 38, 2380–2393 (2019).
pubmed: 30518877
doi: 10.1038/s41388-018-0581-9
Khoo, L. T. & Chen, L. Y. Role of the cGAS–STING pathway in cancer development and oncotherapeutic approaches. EMBO Rep. 19, e46935 (2018).
pubmed: 30446584
pmcid: 6280650
doi: 10.15252/embr.201846935
Della Corte, C. M. et al. STING pathway expression identifies NSCLC with an immune-responsive phenotype. J. Thorac. Oncol. 15, 777–791 (2020).
pubmed: 32068166
doi: 10.1016/j.jtho.2020.01.009
pmcid: 7202130
Harabuchi, S. et al. Intratumoral STING activations overcome negative impact of cisplatin on antitumor immunity by inflaming tumor microenvironment in squamous cell carcinoma. Biochem. Biophys. Res. Commun. 522, 408–414 (2020).
pubmed: 31771883
doi: 10.1016/j.bbrc.2019.11.107
Fu, D. et al. T cell recruitment triggered by optimal dose platinum compounds contributes to the therapeutic efficacy of sequential PD-1 blockade in a mouse model of colon cancer. Am. J. Cancer Res. 10, 473–490 (2020).
pubmed: 32195021
pmcid: 7061747
Lips, E. H. et al. BRCAness digitalMLPA profiling predicts benefit of intensified platinum-based chemotherapy in triple-negative and luminal-type breast cancer. Breast Cancer Res. 22, 79 (2020).
pubmed: 32711554
pmcid: 7382055
doi: 10.1186/s13058-020-01313-7
Sarkar, A. Novel platinum compounds and nanoparticles as anticancer agents. Pharm. Pat. Anal. 7, 33–46 (2018).
pubmed: 29227198
doi: 10.4155/ppa-2017-0036
Johnstone, T. C., Suntharalingam, K. & Lippard, S. J. The next generation of platinum drugs: targeted Pt(II) agents, nanoparticle delivery, and Pt(IV) prodrugs. Chem. Rev. 116, 3436–3486 (2016).
pubmed: 26865551
pmcid: 4792284
doi: 10.1021/acs.chemrev.5b00597
Komeda, S. et al. The phosphate clamp: a small and independent motif for nucleic acid backbone recognition. Nucleic Acids Res. 39, 325–336 (2011).
pubmed: 20736180
doi: 10.1093/nar/gkq723
Rosa, N. M. P., Ferreira, F. H. D. C., Farrell, N. P. & Costa, L. A. S. TriplatinNC and biomolecules: building models based on non-covalent interactions. Front. Chem. 7, 307 (2019).
pubmed: 31231629
pmcid: 6558404
doi: 10.3389/fchem.2019.00307
Gatti, L. et al. Novel bis-platinum complexes endowed with an improved pharmacological profile. Mol. Pharm. 7, 207–216 (2010).
pubmed: 19919086
doi: 10.1021/mp900211j
Almaqwashi, A. A. et al. DNA intercalation facilitates efficient DNA-targeted covalent binding of phenanthriplatin. J. Am. Chem. Soc. 141, 1537–1545 (2019).
pubmed: 30599508
pmcid: 6491043
doi: 10.1021/jacs.8b10252
Zheng, Y. R. et al. Pt(IV) prodrugs designed to bind non-covalently to human serum albumin for drug delivery. J. Am. Chem. Soc. 136, 8790–8798 (2014).
pubmed: 24902769
pmcid: 4076294
doi: 10.1021/ja5038269
Arosio, D., Manzoni, L., Corno, C. & Perego, P. Integrin-targeted peptide- and peptidomimetic-drug conjugates for the treatment of tumors. Recent Pat. Anticancer Drug Discov. 12, 148–168 (2017).
pubmed: 28164756
doi: 10.2174/1574892812666170203151930
Stathopoulos, G. P. et al. Comparison of liposomal cisplatin versus cisplatin in non-squamous cell non-small-cell lung cancer. Cancer Chemother. Pharmacol. 68, 945–950 (2011).
pubmed: 21301848
pmcid: 3180559
doi: 10.1007/s00280-011-1572-5
Ghaferi, M., Asadollahzadeh, M. J., Akbarzadeh, A., Ebrahimi Shahmabadi, H. & Alavi, S. E. Enhanced efficacy of PEGylated liposomal cisplatin: in vitro and in vivo evaluation. Int. J. Mol. Sci. 21, 559 (2020).
pmcid: 7013419
doi: 10.3390/ijms21020559
Baumann, P. et al. CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res. 65, 10783–10793 (2005).
pubmed: 16322224
doi: 10.1158/0008-5472.CAN-05-0619
Ashihara, K. et al. Pharmacokinetic evaluation and antitumor potency of liposomal nanoparticle encapsulated cisplatin targeted to CD24-positive cells in ovarian cancer. Oncol. Lett. 19, 1872–1880 (2020).
pubmed: 32194682
pmcid: 7038920
Wolff, J. E., Berrak, S., Koontz Webb, S. E. & Zhang, M. Nitrosourea efficacy in high-grade glioma: a survival gain analysis summarizing 504 cohorts with 24193 patients. J. Neurooncol. 88, 57–63 (2008).
pubmed: 18253699
doi: 10.1007/s11060-008-9533-5
Brock, P. R. et al. Sodium thiosulfate for protection from cisplatin-induced hearing loss. N. Engl. J. Med. 378, 2376–2385 (2018).
pubmed: 29924955
pmcid: 6117111
doi: 10.1056/NEJMoa1801109
Berndtsson, M. et al. Acute apoptosis by cisplatin requires induction of reactive oxygen species but is not associated with damage to nuclear DNA. Int. J. Cancer 120, 175–180 (2007).
pubmed: 17044026
doi: 10.1002/ijc.22132
Alberti, E., Zampakou, M. & Donghi, D. Covalent and non-covalent binding of metal complexes to RNA. J. Inorg. Biochem. 163, 278–291 (2016).
pubmed: 27289348
doi: 10.1016/j.jinorgbio.2016.04.021
Russo Krauss, I., Ferraro, G. & Merlino, A. Cisplatin–protein interactions: unexpected drug binding to N-terminal amine and lysine side chains. Inorg. Chem. 55, 7814–7816 (2016).
pubmed: 27482735
doi: 10.1021/acs.inorgchem.6b01234
Takasato, M. et al. Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature 526, 564–568 (2015).
pubmed: 26444236
doi: 10.1038/nature15695
Freyer, D. R. et al. Effects of sodium thiosulfate versus observation on development of cisplatin-induced hearing loss in children with cancer (ACCL0431): a multicentre, randomised, controlled, open-label, phase 3 trial. Lancet Oncol. 18, 63–74 (2017).
pubmed: 27914822
doi: 10.1016/S1470-2045(16)30625-8
Oun, R., Moussa, Y. E. & Wheate, N. J. The side effects of platinum-based chemotherapy drugs: a review for chemists. Dalton Trans. 47, 6645–6653 (2018).
pubmed: 29632935
doi: 10.1039/C8DT00838H
Lv, F., Ma, Y., Zhang, Y. & Li, Z. Relationship between GSTP1 rs1695 gene polymorphism and myelosuppression induced by platinum-based drugs: a meta-analysis. Int. J. Biol. Markers 33, 364–371 (2018).
pubmed: 30238837
doi: 10.1177/1724600818792897
Crona, D. J. et al. A systematic review of strategies to prevent cisplatin-induced nephrotoxicity. Oncologist 22, 609–619 (2017).
pubmed: 28438887
pmcid: 5423518
doi: 10.1634/theoncologist.2016-0319
Kanat, O., Ertas, H. & Caner, B. Platinum-induced neurotoxicity: a review of possible mechanisms. World J. Clin. Oncol. 8, 329–335 (2017).
pubmed: 28848699
pmcid: 5554876
doi: 10.5306/wjco.v8.i4.329
Avan, A. et al. Platinum-induced neurotoxicity and preventive strategies: past, present, and future. Oncologist 20, 411–432 (2015).
pubmed: 25765877
pmcid: 4391771
doi: 10.1634/theoncologist.2014-0044
Yan, F., Liu, J. J., Ip, V., Jamieson, S. M. & McKeage, M. J. Role of platinum DNA damage-induced transcriptional inhibition in chemotherapy-induced neuronal atrophy and peripheral neurotoxicity. J. Neurochem. 135, 1099–1112 (2015).
pubmed: 26364854
doi: 10.1111/jnc.13355
Karasawa, T. & Steyger, P. S. An integrated view of cisplatin-induced nephrotoxicity and ototoxicity. Toxicol. Lett. 237, 219–227 (2015).
pubmed: 26101797
pmcid: 4516600
doi: 10.1016/j.toxlet.2015.06.012
More, S. S. et al. Role of the copper transporter, CTR1, in platinum-induced ototoxicity. J. Neurosci. 30, 9500–9509 (2010).
pubmed: 20631178
pmcid: 2949060
doi: 10.1523/JNEUROSCI.1544-10.2010
Ciarimboli, G. et al. Organic cation transporter 2 mediates cisplatin-induced oto- and nephrotoxicity and is a target for protective interventions. Am. J. Pathol. 176, 1169–1180 (2010).
pubmed: 20110413
pmcid: 2832140
doi: 10.2353/ajpath.2010.090610
Breglio, A. M. et al. Cisplatin is retained in the cochlea indefinitely following chemotherapy. Nat. Commun. 8, 1654 (2017).
pubmed: 29162831
pmcid: 5698400
doi: 10.1038/s41467-017-01837-1
Sooriyaarachchi, M., Gailer, J., Dolgova, N. V., Pickering, I. J. & George, G. N. Chemical basis for the detoxification of cisplatin-derived hydrolysis products by sodium thiosulfate. J. Inorg. Biochem. 162, 96–101 (2016).
pubmed: 27324827
doi: 10.1016/j.jinorgbio.2016.06.012
Elferink, F., van der Vijgh, W. J., Klein, I. & Pinedo, H. M. Interaction of cisplatin and carboplatin with sodium thiosulfate: reaction rates and protein binding. Clin. Chem. 32, 641–645 (1986).
pubmed: 3513991
doi: 10.1093/clinchem/32.4.641
Allan, S. G., Smyth, J. F., Hay, F. G., Leonard, R. C. & Wolf, C. R. Protective effect of sodium-2-mercaptoethanesulfonate on the gastrointestinal toxicity and lethality of cis-diamminedichloroplatinum. Cancer Res. 46, 3569–3573 (1986).
pubmed: 3085925
Perales-Puchalt, A. et al. Frontline science: microbiota reconstitution restores intestinal integrity after cisplatin therapy. J. Leukoc. Biol. 103, 799–805 (2018).
pubmed: 29537705
doi: 10.1002/JLB.5HI1117-446RR