Overcoming ABCB1 mediated multidrug resistance in castration resistant prostate cancer.
Humans
Male
Prostatic Neoplasms, Castration-Resistant
/ drug therapy
Drug Resistance, Neoplasm
/ drug effects
ATP Binding Cassette Transporter, Subfamily B
/ metabolism
Cell Line, Tumor
Docetaxel
/ pharmacology
Drug Resistance, Multiple
/ drug effects
Taxoids
/ pharmacology
Antineoplastic Agents
/ pharmacology
Journal
Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092
Informations de publication
Date de publication:
01 Aug 2024
01 Aug 2024
Historique:
received:
08
04
2024
accepted:
24
07
2024
revised:
19
07
2024
medline:
2
8
2024
pubmed:
2
8
2024
entrez:
1
8
2024
Statut:
epublish
Résumé
Prostate cancer (PCa) is the second leading cause of cancer-related death in American men. PCa that relapses after hormonal therapies, referred to as castration resistant PCa (CRPC), often presents with metastases (mCRPC) that are the major cause of mortality. The few available therapies for mCRPC patients include taxanes docetaxel (DTX) and cabazitaxel (CBZ). However, development of resistance limits their clinical use. Mechanistically, resistance arises through upregulation of multidrug resistance (MDR) proteins such as MDR1/ABCB1, making ABCB1 an attractive therapeutic target. Yet, ABCB1 inhibitors failed to be clinically useful due to low specificity and toxicity issues. To study taxanes resistance, we produced CBZ resistant C4-2B cells (RC4-2B) and documented resistance to both CBZ and DTX in cell culture and in 3D prostaspheres settings. RNAseq identified increased expression of ABCB1 in RC4-2B, that was confirmed by immunoblotting and immunofluorescent analysis. ABCB1-specific inhibitor elacridar reversed CBZ and DTX resistance in RC4-2B cells, confirming ABCB1-mediated resistance mechanism. In a cell-based screen using a curated library of cytotoxic drugs, we found that DNA damaging compounds Camptothecin (CPT) and Cytarabine (Ara-C) overcame resistance as seen by similar cytotoxicity in parental C4-2B and resistant RC4-2B. Further, these compounds were cytotoxic to multiple PC cells resistant to taxanes with high ABCB1 expression and, therefore, can be used to conquer the acquired resistance to taxanes in PCa. Finally, inhibition of cyclin-dependent kinases 4/6 (CDK4/6) with small molecule inhibitors (CDK4/6i) potentiated cytotoxic effect of CPT or Ara-C in both parental and resistant cells. Overall, our findings indicate that DNA damaging agents CPT and Ara-C alone or in combination with CDK4/6i can be suggested as a new treatment regimen in CRPC patients, including those that are resistant to taxanes.
Identifiants
pubmed: 39090086
doi: 10.1038/s41419-024-06949-3
pii: 10.1038/s41419-024-06949-3
doi:
Substances chimiques
ATP Binding Cassette Transporter, Subfamily B
0
ABCB1 protein, human
0
Docetaxel
15H5577CQD
Taxoids
0
cabazitaxel
51F690397J
Antineoplastic Agents
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
558Subventions
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Dental and Craniofacial Research (NIDCR)
ID : R01DE026707
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Dental and Craniofacial Research (NIDCR)
ID : R01DE026707
Organisme : U.S. Department of Health & Human Services | NIH | National Cancer Institute (NCI)
ID : R21CA198820
Organisme : U.S. Department of Health & Human Services | NIH | National Cancer Institute (NCI)
ID : P30CA247796
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R01GM145745
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R01GM145745
Informations de copyright
© 2024. The Author(s).
Références
Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72:7–33.
pubmed: 35020204
doi: 10.3322/caac.21708
Egan A, Dong Y, Zhang H, Qi Y, Balk SP, Sartor O. Castration-resistant prostate cancer: adaptive responses in the androgen axis. Cancer Treat Rev. 2014;40:426–33.
pubmed: 24139549
doi: 10.1016/j.ctrv.2013.09.011
Abidi A. Cabazitaxel: A novel taxane for metastatic castration-resistant prostate cancer-current implications and future prospects. J Pharm Pharmacother. 2013;4:230–7.
doi: 10.4103/0976-500X.119704
de Bono JS, Oudard S, Ozguroglu M, Hansen S, Machiels JP, Kocak I, et al. Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet. 2010;376:1147–54.
pubmed: 20888992
doi: 10.1016/S0140-6736(10)61389-X
de Leeuw R, Berman-Booty LD, Schiewer MJ, Ciment SJ, Den RB, Dicker AP, et al. Novel actions of next-generation taxanes benefit advanced stages of prostate cancer. Clin Cancer Res. 2015;21:795–807.
pubmed: 25691773
pmcid: 4333741
doi: 10.1158/1078-0432.CCR-14-1358
Teply BA, Hauke RJ. Chemotherapy options in castration-resistant prostate cancer. Indian J Urol. 2016;32:262–70.
pubmed: 27843207
pmcid: 5054655
doi: 10.4103/0970-1591.191239
Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N. Engl J Med. 2004;351:1502–12.
pubmed: 15470213
doi: 10.1056/NEJMoa040720
Vaishampayan U. Therapeutic options and multifaceted treatment paradigms in metastatic castrate-resistant prostate cancer. Curr Opin Oncol. 2014;26:265–73.
pubmed: 24626129
pmcid: 4238025
doi: 10.1097/CCO.0000000000000066
Pezaro CJ, Omlin AG, Altavilla A, Lorente D, Ferraldeschi R, Bianchini D, et al. Activity of cabazitaxel in castration-resistant prostate cancer progressing after docetaxel and next-generation endocrine agents. Eur Urol. 2014;66:459–65.
pubmed: 24411987
doi: 10.1016/j.eururo.2013.11.044
Corn PG, Agarwal N, Araujo JC, Sonpavde G. Taxane-based Combination Therapies for Metastatic Prostate Cancer. Eur Urol Focus. 2019;5:369–80.
Rowinsky EK, Eisenhauer EA, Chaudhry V, Arbuck SG, Donehower RC. Clinical toxicities encountered with paclitaxel (Taxol). Semin Oncol. 1993;20:1–15.
pubmed: 8102012
Bumbaca B, Li W. Taxane resistance in castration-resistant prostate cancer: mechanisms and therapeutic strategies. Acta Pharm Sin B. 2018;8:518–29.
pubmed: 30109177
pmcid: 6089846
doi: 10.1016/j.apsb.2018.04.007
Lombard AP, Liu C, Armstrong CM, Cucchiara V, Gu X, Lou W, et al. ABCB1 Mediates Cabazitaxel-Docetaxel Cross-Resistance in Advanced Prostate Cancer. Mol Cancer Ther. 2017;16:2257–66.
pubmed: 28698198
pmcid: 5628132
doi: 10.1158/1535-7163.MCT-17-0179
Canil CM, Tannock IF. Is there a role for chemotherapy in prostate cancer? Br J Cancer. 2004;91:1005–11.
pubmed: 15150548
pmcid: 2747715
doi: 10.1038/sj.bjc.6601850
Armstrong CM, Gao AC. Drug resistance in castration resistant prostate cancer: resistance mechanisms and emerging treatment strategies. Am J Clin Exp Urol. 2015;3:64–76.
pubmed: 26309896
pmcid: 4539108
Wood KW, Cornwell WD, Jackson JR. Past and future of the mitotic spindle as an oncology target. Curr Opin Pharm. 2001;1:370–7.
doi: 10.1016/S1471-4892(01)00064-9
Rieder CL, Maiato H. Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev Cell. 2004;7:637–51.
pubmed: 15525526
doi: 10.1016/j.devcel.2004.09.002
Morse DL, Gray H, Payne CM, Gillies RJ. Docetaxel induces cell death through mitotic catastrophe in human breast cancer cells. Mol Cancer Ther. 2005;4:1495–504.
pubmed: 16227398
doi: 10.1158/1535-7163.MCT-05-0130
Chen JG, Horwitz SB. Differential mitotic responses to microtubule-stabilizing and -destabilizing drugs. Cancer Res. 2002;62:1935–8.
pubmed: 11929805
Holland AJ, Cleveland DW. Beyond genetics: surprising determinants of cell fate in antitumor drugs. Cancer Cell. 2008;14:103–5.
pubmed: 18691543
pmcid: 3132553
doi: 10.1016/j.ccr.2008.07.010
Gascoigne KE, Taylor SS. Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell. 2008;14:111–22.
pubmed: 18656424
doi: 10.1016/j.ccr.2008.07.002
Gascoigne KE, Taylor SS. How do anti-mitotic drugs kill cancer cells? J Cell Sci. 2009;122:2579–85.
pubmed: 19625502
doi: 10.1242/jcs.039719
Wertz IE, Kusam S, Lam C, Okamoto T, Sandoval W, Anderson DJ, et al. Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature. 2011;471:110–4.
pubmed: 21368834
doi: 10.1038/nature09779
Brito DA, Rieder CL. Mitotic checkpoint slippage in humans occurs via cyclin B destruction in the presence of an active checkpoint. Curr Biol. 2006;16:1194–200.
pubmed: 16782009
pmcid: 2749311
doi: 10.1016/j.cub.2006.04.043
Brito DA, Yang Z, Rieder CL. Microtubules do not promote mitotic slippage when the spindle assembly checkpoint cannot be satisfied. J Cell Biol. 2008;182:623–9.
pubmed: 18710927
pmcid: 2518701
doi: 10.1083/jcb.200805072
Schnerch D, Follo M, Krohs J, Felthaus J, Engelhardt M, Wasch R. Monitoring APC/C activity in the presence of chromosomal misalignment in unperturbed cell populations. Cell Cycle. 2012;11:310–21.
pubmed: 22214763
doi: 10.4161/cc.11.2.18737
Song L, Rape M. Substrate-specific regulation of ubiquitination by the anaphase-promoting complex. Cell Cycle. 2011;10:52–56.
pubmed: 21191176
pmcid: 3048074
doi: 10.4161/cc.10.1.14387
Mantel C, Guo Y, Lee MR, Han MK, Rhorabough S, Kim KS, et al. Cells enter a unique intermediate 4N stage, not 4N-G1, after aborted mitosis. Cell Cycle. 2008;7:484–92.
pubmed: 18235235
doi: 10.4161/cc.7.4.5316
Wysong DR, Chakravarty A, Hoar K, Ecsedy JA. The inhibition of Aurora A abrogates the mitotic delay induced by microtubule perturbing agents. Cell Cycle. 2009;8:876–88.
pubmed: 19221504
doi: 10.4161/cc.8.6.7897
Erenpreisa JE, Ivanov A, Dekena G, Vitina A, Krampe R, Freivalds T, et al. Arrest in metaphase and anatomy of mitotic catastrophe: mild heat shock in two human osteosarcoma cell lines. Cell Biol Int. 2000;24:61–70.
pubmed: 10772764
doi: 10.1006/cbir.1999.0466
Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ. 2008;15:1153–62.
pubmed: 18404154
doi: 10.1038/cdd.2008.47
Roninson IB, Broude EV, Chang BD. If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist Updat. 2001;4:303–13.
pubmed: 11991684
doi: 10.1054/drup.2001.0213
Sazonova EV, Kopeina GS, Imyanitov EN, Zhivotovsky B. Platinum drugs and taxanes: can we overcome resistance? Cell Death Discov. 2021;7:155.
pubmed: 34226520
pmcid: 8257727
doi: 10.1038/s41420-021-00554-5
Ji X, Lu Y, Tian H, Meng X, Wei M, Cho WC. Chemoresistance mechanisms of breast cancer and their countermeasures. Biomed Pharmacother. 2019;114:108800.
pubmed: 30921705
doi: 10.1016/j.biopha.2019.108800
Sui H, Fan ZZ, Li Q. Signal transduction pathways and transcriptional mechanisms of ABCB1/Pgp-mediated multiple drug resistance in human cancer cells. J Int Med Res. 2012;40:426–35.
pubmed: 22613403
doi: 10.1177/147323001204000204
Perez EA. Impact, mechanisms, and novel chemotherapy strategies for overcoming resistance to anthracyclines and taxanes in metastatic breast cancer. Breast Cancer Res Treat. 2009;114:195–201.
pubmed: 18443902
doi: 10.1007/s10549-008-0005-6
Wilson CS, Davidson GS, Martin SB, Andries E, Potter J, Harvey R, et al. Gene expression profiling of adult acute myeloid leukemia identifies novel biologic clusters for risk classification and outcome prediction. Blood. 2006;108:685–96.
pubmed: 16597596
pmcid: 1895492
doi: 10.1182/blood-2004-12-4633
Patch AM, Christie EL, Etemadmoghadam D, Garsed DW, George J, Fereday S, et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature. 2015;521:489–94.
pubmed: 26017449
doi: 10.1038/nature14410
Katayama R, Sakashita T, Yanagitani N, Ninomiya H, Horiike A, Friboulet L, et al. P-glycoprotein Mediates Ceritinib Resistance in Anaplastic Lymphoma Kinase-rearranged Non-small Cell Lung Cancer. Ebiomedicine. 2016;3:54–66.
pubmed: 26870817
doi: 10.1016/j.ebiom.2015.12.009
Amiri-Kordestani L, Basseville A, Kurdziel K, Fojo AT, Bates SE. Targeting MDR in breast and lung cancer: discriminating its potential importance from the failure of drug resistance reversal studies. Drug Resist Updat. 2012;15:50–61.
pubmed: 22464282
pmcid: 3680361
doi: 10.1016/j.drup.2012.02.002
Kimura Y, Morita SY, Matsuo M, Ueda K. Mechanism of multidrug recognition by MDR1/ABCB1. Cancer Sci. 2007;98:1303–10.
pubmed: 17608770
doi: 10.1111/j.1349-7006.2007.00538.x
Sanchez C, Mendoza P, Contreras HR, Vergara J, McCubrey JA, Huidobro C, et al. Expression of multidrug resistance proteins in prostate cancer is related with cell sensitivity to chemotherapeutic drugs. Prostate. 2009;69:1448–59.
pubmed: 19496068
doi: 10.1002/pros.20991
Abd El-Aziz YS, Spillane AJ, Jansson PJ, Sahni S. Role of ABCB1 in mediating chemoresistance of triple-negative breast cancers. Biosci Rep. 2021;41:BSR20204092.
Vera-Ramirez L, Sanchez-Rovira P, Ramirez-Tortosa CL, Quiles JL, Ramirez-Tortosa M, Lorente JA. Transcriptional shift identifies a set of genes driving breast cancer chemoresistance. PLoS One. 2013;8:e53983.
pubmed: 23326553
pmcid: 3542325
doi: 10.1371/journal.pone.0053983
Lima TS, Souza LO, Iglesias-Gato D, Elversang J, Jorgensen FS, Kallunki T, et al. Itraconazole Reverts ABCB1-Mediated Docetaxel Resistance in Prostate Cancer. Front Pharm. 2022;13:869461.
doi: 10.3389/fphar.2022.869461
Lombard AP, Lou W, Armstrong CM, D’Abronzo LS, Ning S, Evans CP, et al. Activation of the ABCB1 Amplicon in Docetaxel- and Cabazitaxel-Resistant Prostate Cancer Cells. Mol Cancer Ther. 2021;20:2061–70.
pubmed: 34326198
pmcid: 8492550
doi: 10.1158/1535-7163.MCT-20-0983
Kawai K, Sakurai M, Sakai T, Misaki M, Kusano I, Shiraishi T, et al. Demonstration of MDR1 P-glycoprotein isoform expression in benign and malignant human prostate cells by isoform-specific monoclonal antibodies. Cancer Lett. 2000;150:147–53.
pubmed: 10704736
doi: 10.1016/S0304-3835(99)00384-5
Van Brussel JP, Jan Van Steenbrugge G, Van Krimpen C, Bogdanowicz JF, Van Der Kwast TH, Schroder FH, et al. Expression of multidrug resistance related proteins and proliferative activity is increased in advanced clinical prostate cancer. J Urol. 2001;165:130–5.
pubmed: 11125381
doi: 10.1097/00005392-200101000-00032
Lombard AP, Liu C, Armstrong CM, D’Abronzo LS, Lou W, Chen H, et al. Overexpressed ABCB1 Induces Olaparib-Taxane Cross-Resistance in Advanced Prostate Cancer. Transl Oncol. 2019;12:871–8.
pubmed: 31075528
pmcid: 6510951
doi: 10.1016/j.tranon.2019.04.007
Sarwar S, Morozov VM, Purayil H, Daaka Y, Ishov AM. Inhibition of Mps1 kinase enhances taxanes efficacy in castration resistant prostate cancer. Cell Death Dis. 2022;13:868.
pubmed: 36229449
pmcid: 9561175
doi: 10.1038/s41419-022-05312-8
Kumar A, Coleman I, Morrissey C, Zhang X, True LD, Gulati R, et al. Substantial interindividual and limited intraindividual genomic diversity among tumors from men with metastatic prostate cancer. Nat Med. 2016;22:369–78.
pubmed: 26928463
pmcid: 5045679
doi: 10.1038/nm.4053
Abida W, Cyrta J, Heller G, Prandi D, Armenia J, Coleman I, et al. Genomic correlates of clinical outcome in advanced prostate cancer. Proc Natl Acad Sci USA. 2019;116:11428–36.
pubmed: 31061129
pmcid: 6561293
doi: 10.1073/pnas.1902651116
Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6:pl1.
pubmed: 23550210
pmcid: 4160307
doi: 10.1126/scisignal.2004088
Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2:401–4.
pubmed: 22588877
doi: 10.1158/2159-8290.CD-12-0095
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21.
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Christie EL, Pattnaik S, Beach J, Copeland A, Rashoo N, Fereday S, et al. Multiple ABCB1 transcriptional fusions in drug resistant high-grade serous ovarian and breast cancer. Nat Commun. 2019;10:1295.
pubmed: 30894541
pmcid: 6426934
doi: 10.1038/s41467-019-09312-9
Chen H, Shien K, Suzawa K, Tsukuda K, Tomida S, Sato H, et al. Elacridar, a third-generation ABCB1 inhibitor, overcomes resistance to docetaxel in non-small cell lung cancer. Oncol Lett. 2017;14:4349–54.
pubmed: 28959367
pmcid: 5607652
doi: 10.3892/ol.2017.6678
Fassl A, Geng Y, Sicinski P. CDK4 and CDK6 kinases: From basic science to cancer therapy. Science. 2022;375:eabc1495.
pubmed: 35025636
pmcid: 9048628
doi: 10.1126/science.abc1495
Zhou L, Ng DS, Yam JC, Chen LJ, Tham CC, Pang CP, et al. Post-translational modifications on the retinoblastoma protein. J Biomed Sci. 2022;29:33.
pubmed: 35650644
pmcid: 9161509
doi: 10.1186/s12929-022-00818-x
Dang F, Nie L, Zhou J, Shimizu K, Chu C, Wu Z, et al. Inhibition of CK1epsilon potentiates the therapeutic efficacy of CDK4/6 inhibitor in breast cancer. Nat Commun. 2021;12:5386.
pubmed: 34508104
pmcid: 8433397
doi: 10.1038/s41467-021-25700-6
Rottenberg S, Nygren AO, Pajic M, van Leeuwen FW, van der Heijden I, van de Wetering K, et al. Selective induction of chemotherapy resistance of mammary tumors in a conditional mouse model for hereditary breast cancer. Proc Natl Acad Sci USA. 2007;104:12117–22.
pubmed: 17626183
pmcid: 1914039
doi: 10.1073/pnas.0702955104
Rottenberg S, Jaspers JE, Kersbergen A, van der Burg E, Nygren AO, Zander SA, et al. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc Natl Acad Sci USA. 2008;105:17079–84.
pubmed: 18971340
pmcid: 2579381
doi: 10.1073/pnas.0806092105
O’Neill AJ, Prencipe M, Dowling C, Fan Y, Mulrane L, Gallagher WM, et al. Characterisation and manipulation of docetaxel resistant prostate cancer cell lines. Mol Cancer. 2011;10:126.
pubmed: 21982118
pmcid: 3203088
doi: 10.1186/1476-4598-10-126
Zhu Y, Liu C, Nadiminty N, Lou W, Tummala R, Evans CP, et al. Inhibition of ABCB1 expression overcomes acquired docetaxel resistance in prostate cancer. Mol Cancer Ther. 2013;12:1829–36.
pubmed: 23861346
pmcid: 3947549
doi: 10.1158/1535-7163.MCT-13-0208
Lee WK, Frank T. Teaching an old dog new tricks: reactivated developmental signaling pathways regulate ABCB1 and chemoresistance in cancer. Cancer Drug Resist. 2021;4:424–52.
pubmed: 35582031
pmcid: 9019277
Fultang N, Illendula A, Lin J, Pandey MK, Klase Z, Peethambaran B. ROR1 regulates chemoresistance in Breast Cancer via modulation of drug efflux pump ABCB1. Sci Rep. 2020;10:1821.
pubmed: 32020017
pmcid: 7000766
doi: 10.1038/s41598-020-58864-0
Lai JI, Tseng YJ, Chen MH, Huang CF, Chang PM. Clinical Perspective of FDA Approved Drugs With P-Glycoprotein Inhibition Activities for Potential Cancer Therapeutics. Front Oncol. 2020;10:561936.
pubmed: 33312947
pmcid: 7704056
doi: 10.3389/fonc.2020.561936
Dash RP, Jayachandra Babu R, Srinivas NR. Therapeutic Potential and Utility of Elacridar with Respect to P-glycoprotein Inhibition: An Insight from the Published In Vitro, Preclinical and Clinical Studies. Eur J Drug Metab Pharmacokinet. 2017;42:915–33.
pubmed: 28374336
doi: 10.1007/s13318-017-0411-4
Chung FS, Santiago JS, Jesus MF, Trinidad CV, See MF. Disrupting P-glycoprotein function in clinical settings: what can we learn from the fundamental aspects of this transporter? Am J Cancer Res. 2016;6:1583–98.
pubmed: 27648351
pmcid: 5004065
Robey RW, Pluchino KM, Hall MD, Fojo AT, Bates SE, Gottesman MM. Revisiting the role of ABC transporters in multidrug-resistant cancer. Nat Rev Cancer. 2018;18:452–64.
pubmed: 29643473
pmcid: 6622180
doi: 10.1038/s41568-018-0005-8
Seo HK, Lee SJ, Kwon WA, Jeong KC. Docetaxel-resistant prostate cancer cells become sensitive to gemcitabine due to the upregulation of ABCB1. Prostate. 2020;80:453–62.
pubmed: 32134535
doi: 10.1002/pros.23946
Patel L, Pritchard CC. Molecular testing of DNA damage response pathways in prostate cancer patients. Curr Opin Oncol. 2023;35:224–30.
pubmed: 36966502
doi: 10.1097/CCO.0000000000000934
Vaidyanathan A, Sawers L, Gannon AL, Chakravarty P, Scott AL, Bray SE, et al. ABCB1 (MDR1) induction defines a common resistance mechanism in paclitaxel- and olaparib-resistant ovarian cancer cells. Br J Cancer. 2016;115:431–41.
pubmed: 27415012
pmcid: 4985349
doi: 10.1038/bjc.2016.203
Boeschen M, Le Duc D, Stiller M, von Laffert M, Schoneberg T, Horn S. Interactive webtool for analyzing drug sensitivity and resistance associated with genetic signatures of cancer cell lines. J Cancer Res Clin Oncol. 2023;149:5539–45.
pubmed: 36472769
doi: 10.1007/s00432-022-04503-2
Lheureux S, Oaknin A, Garg S, Bruce JP, Madariaga A, Dhani NC, et al. EVOLVE: A Multicenter Open-Label Single-Arm Clinical and Translational Phase II Trial of Cediranib Plus Olaparib for Ovarian Cancer after PARP Inhibition Progression. Clin Cancer Res. 2020;26:4206–15.
pubmed: 32444417
doi: 10.1158/1078-0432.CCR-19-4121
Wall ME, Wani MC. Camptothecin and taxol: from discovery to clinic. J Ethnopharmacol. 1996;51:239–53.
pubmed: 9213622
doi: 10.1016/0378-8741(95)01367-9
Venditto VJ, Simanek EE. Cancer therapies utilizing the camptothecins: a review of the in vivo literature. Mol Pharm. 2010;7:307–49.
pubmed: 20108971
pmcid: 3733266
doi: 10.1021/mp900243b
Schmidt KT, Peer CJ, Huitema ADR, Williams MD, Wroblewski S, Schellens JHM, et al. Measurement of NLG207 (formerly CRLX101) nanoparticle-bound and released camptothecin in human plasma. J Pharm Biomed Anal. 2020;181:113073.
pubmed: 31927166
doi: 10.1016/j.jpba.2019.113073
Lin CJ, Lin YL, Luh F, Yen Y, Chen RM. Preclinical effects of CRLX101, an investigational camptothecin-containing nanoparticle drug conjugate, on treating glioblastoma multiforme via apoptosis and antiangiogenesis. Oncotarget. 2016;7:42408–21.
pubmed: 27285755
pmcid: 5173144
doi: 10.18632/oncotarget.9878
Pham E, Yin M, Peters CG, Lee CR, Brown D, Xu P, et al. Preclinical Efficacy of Bevacizumab with CRLX101, an Investigational Nanoparticle-Drug Conjugate, in Treatment of Metastatic Triple-Negative Breast Cancer. Cancer Res. 2016;76:4493–503.
pubmed: 27325647
doi: 10.1158/0008-5472.CAN-15-3435
Pham E, Birrer MJ, Eliasof S, Garmey EG, Lazarus D, Lee CR, et al. Translational impact of nanoparticle-drug conjugate CRLX101 with or without bevacizumab in advanced ovarian cancer. Clin Cancer Res. 2015;21:808–18.
pubmed: 25524310
doi: 10.1158/1078-0432.CCR-14-2810
Almansour AI, Arumugam N, Suresh Kumar R, Mahalingam SM, Sau S, Bianchini G, et al. Design, synthesis and antiproliferative activity of decarbonyl luotonin analogues. Eur J Med Chem. 2017;138:932–41.
pubmed: 28753517
doi: 10.1016/j.ejmech.2017.07.027
Di Francia R, Crisci S, De Monaco A, Cafiero C, Re A, Iaccarino G, et al. Response and Toxicity to Cytarabine Therapy in Leukemia and Lymphoma: From Dose Puzzle to Pharmacogenomic Biomarkers. Cancers. 2021;13:966.
Salvador-Barbero B, Alvarez-Fernández M, Zapatero-Solana E, El Bakkali A, Menéndez MD, López-Casas PP, et al. CDK4/6 Inhibitors Impair Recovery from Cytotoxic Chemotherapy in Pancreatic Adenocarcinoma. Cancer Cell. 2020;37:340–34.
pubmed: 32109375
doi: 10.1016/j.ccell.2020.01.007