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Review Article | Open Access

Revisiting chemoresistance in ovarian cancer: Mechanism, biomarkers, and precision medicine

Chong Guoa, Chaoying Songa, Jiali Zhanga, Yisong Gaoa, Yuying Qia, Zongyao Zhaoa, Chengfu Yuana,b,c( )
College of Medical Science, China Three Gorges University, Yichang, Hubei 443002, PR China
Third-Grade Pharmacological Laboratory on Chinese Medicine Approved by State Administration of Traditional Chinese Medicine, China Three Gorges University, Yichang, Hubei 443002, PR China
Hubei Key Laboratory of Tumor Microenvironment and Immunotherapy, China Three Gorges University, Yichang, Hubei 443002, PR China

Peer review under responsibility of Chongqing Medical University.

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Abstract

Among the gynecological cancers, ovarian cancer is the most lethal. Its therapeutic options include a combination of chemotherapy with platinum-based compounds and cytoreductive surgery. Most ovarian cancer patients exhibit an initial response to platinum-based therapy, however, platinum resistance has led to up to 80% of this responsive cohort becoming refractory. Ovarian cancer recurrence and drug resistance to current chemotherapeutic options is a global challenge. Chemo-resistance is a complex phenomenon that involves multiple genes and signal transduction pathways. Therefore, it is important to elucidate on the underlying molecular mechanisms involved in chemo-resistance. This inform decisions regarding therapeutic management and help in the identification of novel and effective drug targets. Studies have documented the individual biomarkers of platinum-resistance in ovarian cancer that are potential therapeutic targets. This review summarizes the molecular mechanisms of platinum resistance in ovarian cancer, novel drug targets, and clinical outcomes.

Keywords

Ovarian cancerMechanismsClinical outcomesMolecular biomarkersPlatinum resistance

References

1

Cabasag CJ, Arnold M, Butler J, et al. The influence of birth cohort and calendar period on global trends in ovarian cancer incidence. Int J Cancer. 2020;146(3): 749-758.
Crossref Google Scholar
2

Pujade-Lauraine E, Combe P. Recurrent ovarian cancer. Ann Oncol. 2016;27(Suppl 1): i63-i65.
Crossref Google Scholar
3

Bickell NA, Egorova N, Prasad-Hayes M, et al. Secondary surgery versus chemotherapy for recurrent ovarian cancer. Am J Clin Oncol. 2018;41(5): 458-464.
Crossref Google Scholar
4

Rosendahl M, Mosgaard BJ, Steffensen KD. Treatment of primary and recurrent ovarian cancer. Ugeskr Laeger. 2018;180(4): V03170213.
Google Scholar
5

Gershenson DM, Bodurka DC, Coleman RL, Lu KH, Malpica A, Sun CC. Hormonal maintenance therapy for women with low-grade serous cancer of the ovary or peritoneum. J Clin Oncol. 2017;35(10): 1103-1111.
Crossref Google Scholar
6

Coleman RL, Oza AM, Lorusso D, et al. Rucaparib maintenance treatment for recurrent ovarian carcinoma after response to platinum therapy (ARIEL3): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2017;390(10106): 1949-1961.
Crossref Google Scholar
7

Coscia F, Lengyel E, Duraiswamy J, et al. Multi-level proteomics identifies CT45 as a chemosensitivity mediator and immunotherapy target in ovarian cancer. Cell. 2018;175(1): 159-170.
Crossref Google Scholar
8

Samuel P, Pink RC, Brooks SA, Carter DR. miRNAs and ovarian cancer: a miRiad of mechanisms to induce cisplatin drug resistance. Expert Rev Anticancer Ther. 2016;16(1): 57-70.
Crossref Google Scholar
9

Mezzanzanica D, Canevari S, Cecco LD, Bagnoli M. miRNA control of apoptotic programs: focus on ovarian cancer. Expert Rev Mol Diagn. 2011;11(3): 277-286.
Crossref Google Scholar
10

Jiang Y, Jiang J, Jia H, Qiao Z, Zhang J. Recovery of miR-139-5p in ovarian cancer reverses cisplatin resistance by targeting C-Jun. Cell Physiol Biochem. 2018;51(1): 129-141.
Crossref Google Scholar
11

Zhang Y, Huang S, Guo Y, Li L. MiR-1294 confers cisplatin resistance in ovarian Cancer cells by targeting IGF1R. Biomed Pharmacother. 2018;106: 1357-1363.
Crossref Google Scholar
12

Vera O, Jimenez J, Pernia O, et al. DNA methylation of miR-7 is a mechanism involved in platinum response through MAFG overexpression in cancer cells. Theranostics. 2017;7(17): 4118-4134.
Crossref Google Scholar
13

Choi YE, Meghani K, Brault ME, et al. Platinum and PARP inhibitor resistance due to overexpression of MicroRNA-622 in BRCA1-mutant ovarian cancer. Cell Rep. 2016;14(3): 429-439.
Crossref Google Scholar
14

Meghani K, Fuchs W, Detappe A, et al. Multifaceted impact of MicroRNA 493-5p on genome-stabilizing pathways induces platinum and PARP inhibitor resistance in BRCA2-mutated carcinomas. Cell Rep. 2018;23(1): 100-111.
Crossref Google Scholar
15

Wei Z, Liu Y, Wang Y, et al. Downregulation of Foxo3 and TRIM31 by miR-551b in side population promotes cell proliferation, invasion, and drug resistance of ovarian cancer. Med Oncol. 2016;33(11): 126.
Crossref Google Scholar
16

Echevarria-Vargas IM, Valiyeva F, Vivas-Mejia PE. Upregulation of miR-21 in cisplatin resistant ovarian cancer via JNK-1/c-Jun pathway. PLoS One. 2014;9(5): e97094.
Crossref Google Scholar
17

Li X, Chen W, Jin Y, et al. miR-142-5p enhances cisplatin-induced apoptosis in ovarian cancer cells by targeting multiple anti-apoptotic genes. Biochem Pharmacol. 2019;161: 98-112.
Crossref Google Scholar
18

Arrighetti N, Cossa G, De Cecco L, et al. PKC-alpha modulation by miR-483-3p in platinum-resistant ovarian carcinoma cells. Toxicol Appl Pharmacol. 2016;310: 9-19.
Crossref Google Scholar
19

Ramalho S, Andrade LAA, Filho CC, et al. Role of discoidin domain receptor 2 (DDR2) and microRNA-182 in survival of women with high-grade serous ovarian cancer. Tumour Biol. 2019;41(1): 1010428318823988.
Crossref Google Scholar
20

Munoz-Galvan S, Felipe-Abrio B, Verdugo-Sivianes EM, et al. Downregulation of MYPT1 increases tumor resistance in ovarian cancer by targeting the Hippo pathway and increasing the stemness. Mol Cancer. 2020;19(1): 7.
Crossref Google Scholar
21

Wang T, Hao D, Yang S, et al. miR-211 facilitates platinum chemosensitivity by blocking the DNA damage response (DDR) in ovarian cancer. Cell Death Dis. 2019;10(7): 495.
Crossref Google Scholar
22

Sestito R, Cianfrocca R, Rosano L, et al. miR-30a inhibits endothelin A receptor and chemoresistance in ovarian carcinoma. Oncotarget. 2016;7(4): 4009-4023.
Crossref Google Scholar
23

Sun C, Li N, Yang Z, et al. miR-9 regulation of BRCA1 and ovarian cancer sensitivity to cisplatin and PARP inhibition. J Natl Cancer Inst. 2013;105(22): 1750-1758.
Crossref Google Scholar
24

Hisamatsu T, McGuire M, Wu SY, et al. PRKRA/PACT expression promotes chemoresistance of mucinous ovarian cancer. Mol Cancer Ther. 2019;18(1): 162-172.
Crossref Google Scholar
25

Worku T, Bhattarai D, Ayers D, et al. Long non-coding RNAs: the new horizon of gene regulation in ovarian cancer. Cell Physiol Biochem. 2017;44(3): 948-966.
Crossref Google Scholar
26

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(7): 452-464.
Crossref Google Scholar
27

Wong CC, Lim SH, Sagineedu SR, Lajis NH, Stanslas J. SRJ09, a promising anticancer drug lead: elucidation of mechanisms of antiproliferative and apoptogenic effects and assessment of in vivo antitumor efficacy. Pharmacol Res. 2016;107: 66-78.
Crossref Google Scholar
28

Ferreira Cda S, Maganhin CC, Simoes Rdos S, Girao MJ, Baracat EC, . Melatonin: cell death modulator. Rev Assoc Med Bras (1992). 2010;56(6): 715-718.
Crossref Google Scholar
29

Wang J, Wu GS. Role of autophagy in cisplatin resistance in ovarian cancer cells. J Biol Chem. 2014;289(24): 17163-17173.
Crossref Google Scholar
30

Zhang D, Ding L, Li Y, et al. Midkine derived from cancer-associated fibroblasts promotes cisplatin-resistance via up-regulation of the expression of lncRNA ANRIL in tumour cells. Sci Rep. 2017;7(1): 16231.
Crossref Google Scholar
31

Li J, Yang S, Su N, et al. Overexpression of long non-coding RNA HOTAIR leads to chemoresistance by activating the Wnt/beta-catenin pathway in human ovarian cancer. Tumour Biol. 2016;37(2): 2057-2065.
Crossref Google Scholar
32

Liu E, Liu Z, Zhou Y, Mi R, Wang D. Overexpression of long non-coding RNA PVT1 in ovarian cancer cells promotes cisplatin resistance by regulating apoptotic pathways. Int J Clin Exp Med. 2015;8(11): 20565-20572.
Google Scholar
33

Hu J, Zhang L, Mei Z, et al. Interaction of E3 ubiquitin ligase MARCH7 with long noncoding RNA MALAT1 and autophagy-related protein ATG7 promotes autophagy and invasion in ovarian cancer. Cell Physiol Biochem. 2018;47(2): 654-666.
Crossref Google Scholar
34

Lu YM, Shang C, Ou YL, et al. miR-200c modulates ovarian cancer cell metastasis potential by targeting zinc finger E-box-binding homeobox 2 (ZEB2) expression. Med Oncol. 2014;31(8): 134.
Crossref Google Scholar
35

Matouk IJ, Raveh E, Abu-lail R, et al. Oncofetal H19 RNA promotes tumor metastasis. Biochim Biophys Acta. 2014;1843(7): 1414-1426.
Crossref Google Scholar
36

Zheng ZG, Xu H, Suo SS, et al. The essential role of H19 contributing to cisplatin resistance by regulating glutathione metabolism in high-grade serous ovarian cancer. Sci Rep. 2016;6: 26093.
Crossref Google Scholar
37

Sajadpoor Z, Amini-Farsani Z, Teimori H, et al. Valproic acid promotes apoptosis and cisplatin sensitivity through downregulation of H19 noncoding RNA in ovarian A2780 cells. Appl Biochem Biotechnol. 2018;185(4): 1132-1144.
Crossref Google Scholar
38

Zhang J, Liu J, Xu X, Li L. Curcumin suppresses cisplatin resistance development partly via modulating extracellular vesicle-mediated transfer of MEG3 and miR-214 in ovarian cancer. Cancer Chemother Pharmacol. 2017;79(3): 479-487.
Crossref Google Scholar
39

Cocquerelle C, Mascrez B, Hetuin D, Bailleul B. Mis-splicing yields circular RNA molecules. FASEB J. 1993;7(1): 155-160.
Crossref Google Scholar
40

Memczak S, Jens M, Elefsinioti A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495(7441): 333-338.
Crossref Google Scholar
41

Li Z, Huang C, Bao C, et al. Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol. 2015;22(3): 256-264.
Crossref Google Scholar
42

Tang W, Ji M, He G, et al. Silencing CDR1as inhibits colorectal cancer progression through regulating microRNA-7. Onco Targets Ther. 2017;10: 2045-2056.
Crossref Google Scholar
43

Zhao Z, Ji M, Wang Q, He N, Li Y. Circular RNA Cdr1as upregulates SCAI to suppress cisplatin resistance in ovarian cancer via miR-1270 suppression. Mol Ther Nucleic Acids. 2019;18: 24-33.
Crossref Google Scholar
44

Prasetyanti PR, Medema JP. Intra-tumor heterogeneity from a cancer stem cell perspective. Mol Cancer. 2017;16(1): 41.
Crossref Google Scholar
45

Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010;29(34): 4741-4751.
Crossref Google Scholar
46

Ruscito I, Cacsire Castillo-Tong D, Vergote I, et al. Exploring the clonal evolution of CD133/aldehyde-dehydrogenase-1 (ALDH1)-positive cancer stem-like cells from primary to recurrent high-grade serous ovarian cancer (HGSOC). A study of the Ovarian Cancer Therapy-Innovative Models Prolong Survival (OCTIPS) Consortium. Eur J Cancer. 2017;79: 214-225.
Crossref Google Scholar
47

Steg AD, Bevis KS, Katre AA, et al. Stem cell pathways contribute to clinical chemoresistance in ovarian cancer. Clin Cancer Res. 2012;18(3): 869-881.
Crossref Google Scholar
48

Le Page C, Ouellet V, Madore J, et al. Gene expression profiling of primary cultures of ovarian epithelial cells identifies novel molecular classifiers of ovarian cancer. Br J Cancer. 2006;94(3): 436-445.
Crossref Google Scholar
49

Le Page C, Puiffe ML, Meunier L, et al. BMP-2 signaling in ovarian cancer and its association with poor prognosis. J Ovarian Res. 2009;2: 4.
Crossref Google Scholar
50

Choi YJ, Ingram PN, Yang K, et al. Identifying an ovarian cancer cell hierarchy regulated by bone morphogenetic protein 2. Proc Natl Acad Sci U S A. 2015;112(50): E6882-E6888.
Crossref Google Scholar
51

Annunziata CM, O'Shaughnessy J. Poly (ADP-ribose) polymerase as a novel therapeutic target in cancer. Clin Cancer Res. 2010;16(18): 4517-4526.
Crossref Google Scholar
52

Kryczek I, Liu S, Roh M, et al. Expression of aldehyde dehydrogenase and CD133 defines ovarian cancer stem cells. Int J Cancer. 2012;130(1): 29-39.
Crossref Google Scholar
53

Bourguignon LY, Peyrollier K, Xia W, Gilad E. Hyaluronan-CD44 interaction activates stem cell marker Nanog, Stat-3-mediated MDR1 gene expression, and ankyrin-regulated multidrug efflux in breast and ovarian tumor cells. J Biol Chem. 2008;283(25): 17635-17651.
Crossref Google Scholar
54

Ottevanger PB. Ovarian cancer stem cells more questions than answers. Semin Cancer Biol. 2017;44: 67-71.
Crossref Google Scholar
55

Cao L, Petrusca DN, Satpathy M, Nakshatri H, Petrache I, Matei D. Tissue transglutaminase protects epithelial ovarian cancer cells from cisplatin-induced apoptosis by promoting cell survival signaling. Carcinogenesis. 2008;29(10): 1893-1900.
Crossref Google Scholar
56

Cao L, Shao M, Schilder J, Guise T, Mohammad KS, Matei D. Tissue transglutaminase links TGF-beta, epithelial to mesenchymal transition and a stem cell phenotype in ovarian cancer. Oncogene. 2012;31(20): 2521-2534.
Crossref Google Scholar
57

Davidson B, Holth A, Hellesylt E, et al. The clinical role of epithelial-mesenchymal transition and stem cell markers in advanced-stage ovarian serous carcinoma effusions. Hum Pathol. 2015;46(1): 1-8.
Crossref Google Scholar
58

Huang RY, Chung VY, Thiery JP. Targeting pathways contributing to epithelial-mesenchymal transition (EMT) in epithelial ovarian cancer. Curr Drug Targets. 2012;13(13): 1649-1653.
Crossref Google Scholar
59

Patch AM, Christie EL, Etemadmoghadam D, et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature. 2015;521(7553): 489-494.
Crossref Google Scholar
60

Lund RJ, Huhtinen K, Salmi J, et al. DNA methylation and transcriptome changes associated with cisplatin resistance in ovarian cancer. Sci Rep. 2017;7(1): 1469.
Crossref Google Scholar
61

Sorensen PS. Multiple sclerosis. Generic glatiramer acetate-a step toward cheaper MS drugs? Nat Rev Neurol. 2016;12(1): 5-6.
Crossref Google Scholar
62

Tomar T, Alkema NG, Schreuder L, et al. Methylome analysis of extreme chemoresponsive patients identifies novel markers of platinum sensitivity in high-grade serous ovarian cancer. BMC Med. 2017;15(1): 116.
Crossref Google Scholar
63

de Leon M, Cardenas H, Vieth E, et al. Transmembrane protein 88 (TMEM88) promoter hypomethylation is associated with platinum resistance in ovarian cancer. Gynecol Oncol. 2016;142(3): 539-547.
Crossref Google Scholar
64

Bonito NA, Borley J, Wilhelm-Benartzi CS, Ghaem-Maghami S, Brown R. Epigenetic regulation of the homeobox gene MSX1 associates with platinum-resistant disease in high-grade serous epithelial ovarian cancer. Clin Cancer Res. 2016;22(12): 3097-3104.
Crossref Google Scholar
65

Kondrashova O, Topp M, Nesic K, et al. Methylation of all BRCA1 copies predicts response to the PARP inhibitor rucaparib in ovarian carcinoma. Nat Commun. 2018;9(1): 3970.
Crossref Google Scholar
66

Pan JX, Qu F, Wang FF, et al. Aberrant SERPINE1 DNA methylation is involved in carboplatin induced epithelial-mesenchymal transition in epithelial ovarian cancer. Arch Gynecol Obstet. 2017;296(6): 1145-1152.
Crossref Google Scholar
67

Fang F, Munck J, Tang J, et al. The novel, small-molecule DNA methylation inhibitor SGI-110 as an ovarian cancer chemosensitizer. Clin Cancer Res. 2014;20(24): 6504-6516.
Crossref Google Scholar
68

Fang F, Cardenas H, Huang H, et al. Genomic and epigenomic signatures in ovarian cancer associated with resensitization to platinum drugs. Cancer Res. 2018;78(3): 631-644.
Crossref Google Scholar
69

Mase S, Shinjo K, Totani H, et al. ZNF671 DNA methylation as a molecular predictor for the early recurrence of serous ovarian cancer. Cancer Sci. 2019;110(3): 1105-1116.
Crossref Google Scholar
70

Flanagan JM, Wilson A, Koo C, et al. Platinum-based chemotherapy induces methylation changes in blood DNA associated with overall survival in patients with ovarian cancer. Clin Cancer Res. 2017;23(9): 2213-2222.
Crossref Google Scholar
71

Sonnemann J, Gange J, Pilz S, et al. Comparative evaluation of the treatment efficacy of suberoylanilide hydroxamic acid (SAHA) and paclitaxel in ovarian cancer cell lines and primary ovarian cancer cells from patients. BMC Cancer. 2006;6: 183.
Crossref Google Scholar
72

Pchejetski D, Alfraidi A, Sacco K, Alshaker H, Muhammad A, Monzon L. Histone deacetylases as new therapy targets for platinum-resistant epithelial ovarian cancer. J Cancer Res Clin Oncol. 2016;142(8): 1659-1671.
Crossref Google Scholar
73

Modesitt SC, Sill M, Hoffman JS, Bender DP. A phase Ⅱ study of vorinostat in the treatment of persistent or recurrent epithelial ovarian or primary peritoneal carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol. 2008;109(2): 182-186.
Crossref Google Scholar
74

Ulasi Ⅱ, Ijoma CK, Onodugo OD. A community-based study of hypertension and cardio-metabolic syndrome in semi-urban and rural communities in Nigeria. BMC Health Serv Res. 2010;10: 71.
Crossref Google Scholar
75

Griffith DM, Duff B, Suponitsky KY, et al. Novel trans-platinum complexes of the histone deacetylase inhibitor valproic acid; synthesis, in vitro cytotoxicity and mutagenicity. J Inorg Biochem. 2011;105(6): 793-799.
Crossref Google Scholar
76

Dizon DS, Blessing JA, Penson RT, et al. A phase Ⅱ evaluation of belinostat and carboplatin in the treatment of recurrent or persistent platinum-resistant ovarian, fallopian tube, or primary peritoneal carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol. 2012;125(2): 367-371.
Crossref Google Scholar
77

Wilson AJ, Holson E, Wagner F, et al. The DNA damage mark pH2AX differentiates the cytotoxic effects of small molecule HDAC inhibitors in ovarian cancer cells. Cancer Biol Ther. 2011;12(6): 484-493.
Crossref Google Scholar
78

Weberpals JI, O'Brien AM, Niknejad N, Garbuio KD, Clark-Knowles KV, Dimitroulakos J. The effect of the histone deacetylase inhibitor M344 on BRCA1 expression in breast and ovarian cancer cells. Cancer Cell Int. 2011;11(1): 29.
Crossref Google Scholar
79

Ong PS, Wang XQ, Lin HS, Chan SY, Ho PC. Synergistic effects of suberoylanilide hydroxamic acid combined with cisplatin causing cell cycle arrest independent apoptosis in platinum-resistant ovarian cancer cells. Int J Oncol. 2012;40(5): 1705-1713.
Google Scholar
80

Gatti L, Benedetti V, De Cesare M, et al. Synergistic interaction between the novel histone deacetylase inhibitor ST2782 and the proteasome inhibitor bortezomib in platinum-sensitive and resistant ovarian carcinoma cells. J Inorg Biochem. 2012;113: 94-101.
Crossref Google Scholar
81

Damia G, Broggini M. Platinum resistance in ovarian cancer: role of DNA repair. Cancers (Basel). 2019;11(1): 119.
Crossref Google Scholar
82

Konstantinopoulos PA, Ceccaldi R, Shapiro GI, D'Andrea AD. Homologous recombination deficiency: exploiting the fundamental vulnerability of ovarian cancer. Cancer Discov. 2015;5(11): 1137-1154.
Crossref Google Scholar
83

Ratner ES, Zhu YL, Penketh PG, et al. Triapine potentiates platinum-based combination therapy by disruption of homologous recombination repair. Br J Cancer. 2016;114(7): 777-786.
Crossref Google Scholar
84

Tumiati M, Hietanen S, Hynninen J, et al. A functional homologous recombination assay predicts primary chemotherapy response and long-term survival in ovarian cancer patients. Clin Cancer Res. 2018;24(18): 4482-4493.
Crossref Google Scholar
85

Pennington KP, Walsh T, Harrell MI, et al. Germline and somatic mutations in homologous recombination genes predict platinum response and survival in ovarian, fallopian tube, and peritoneal carcinomas. Clin Cancer Res. 2014;20(3): 764-775.
Crossref Google Scholar
86

Alsop K, Fereday S, Meldrum C, et al. BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian Ovarian Cancer Study Group. J Clin Oncol. 2012;30(21): 2654-2663.
Crossref Google Scholar
87

Weigelt B, Comino-Mendez I, de Bruijn I, et al. Diverse BRCA1 and BRCA2 reversion mutations in circulating cell-free DNA of therapy-resistant breast or ovarian cancer. Clin Cancer Res. 2017;23(21): 6708-6720.
Crossref Google Scholar
88

Cook SA, Tinker AV. PARP inhibitors and the evolving landscape of ovarian cancer management: a review. BioDrugs. 2019;33(3): 255-273.
Crossref Google Scholar
89

Pan Z, Xie X. BRCA mutations in the manifestation and treatment of ovarian cancer. Oncotarget. 2017;8(57): 97657-97670.
Crossref Google Scholar
90

Faraoni I, Graziani G. Role of BRCA mutations in cancer treatment with poly(ADP-ribose) polymerase (PARP) inhibitors. Cancers (Basel). 2018;10(12): 487.
Crossref Google Scholar
91

Madariaga A, Lheureux S, Oza AM. Tailoring ovarian cancer treatment: implications of BRCA1/2 mutations. Cancers (Basel). 2019;11(3): 416.
Crossref Google Scholar
92

Sandhu SK, Schelman WR, Wilding G, et al. The poly(ADP-ribose) polymerase inhibitor niraparib (MK4827) in BRCA mutation carriers and patients with sporadic cancer: a phase 1 dose-escalation trial. Lancet Oncol. 2013;14(9): 882-892.
Crossref Google Scholar
93

Swisher EM, Lin KK, Oza AM, et al. Rucaparib in relapsed, platinum-sensitive high-grade ovarian carcinoma (ARIEL2 Part 1): an international, multicentre, open-label, phase 2 trial. Lancet Oncol. 2017;18(1): 75-87.
Crossref Google Scholar
94

Lin KK, Harrell MI, Oza AM, et al. BRCA reversion mutations in circulating tumor DNA predict primary and acquired resistance to the PARP inhibitor rucaparib in high-grade ovarian carcinoma. Cancer Discov. 2019;9(2): 210-219.
Crossref Google Scholar
95

Lorusso D, Scambia G, Pignata S, et al. Prospective phase Ⅱ trial of trabectedin in BRCA-mutated and/or BRCAness phenotype recurrent ovarian cancer patients: the MITO 15 trial. Ann Oncol. 2016;27(3): 487-493.
Crossref Google Scholar
96

Konstantinopoulos PA, Spentzos D, Karlan BY, et al. Gene expression profile of BRCAness that correlates with responsiveness to chemotherapy and with outcome in patients with epithelial ovarian cancer. J Clin Oncol. 2010;28(22): 3555-3561.
Crossref Google Scholar
97

Bast RC Jr. Molecular approaches to personalizing management of ovarian cancer. Ann Oncol. 2011;22(Suppl 8): ⅷ5-ⅷ15.
Crossref Google Scholar
98

Sessa C. Update on PARP1 inhibitors in ovarian cancer. Ann Oncol. 2011;22(Suppl 8): ⅷ72-ⅷ76.
Crossref Google Scholar
99

Wysham WZ, Mhawech-Fauceglia P, Li H, et al. BRCAness profile of sporadic ovarian cancer predicts disease recurrence. PLoS One. 2012;7(1): e30042.
Crossref Google Scholar
100

Romero I, Bast RC Jr. Minireview: human ovarian cancer: biology, current management, and paths to personalizing therapy. Endocrinology. 2012;153(4): 1593-1602.
Crossref Google Scholar
101

Saldivar JS, Wu X, Follen M, Gershenson D. Nucleotide excision repair pathway review Ⅰ: implications in ovarian cancer and platinum sensitivity. Gynecol Oncol. 2007;107(1 Suppl 1): S56-S71.
Crossref Google Scholar
102

Slyskova J, Sabatella M, Ribeiro-Silva C, et al. Base and nucleotide excision repair facilitate resolution of platinum drugs-induced transcription blockage. Nucleic Acids Res. 2018;46(18): 9537-9549.
Crossref Google Scholar
103

Martin LP, Hamilton TC, Schilder RJ. Platinum resistance: the role of DNA repair pathways. Clin Cancer Res. 2008;14(5): 1291-1295.
Crossref Google Scholar
104

Scurry J, van Zyl B, Gulliver D, et al. Nucleotide excision repair protein ERCC1 and tumour-infiltrating lymphocytes are potential biomarkers of neoadjuvant platinum resistance in high grade serous ovarian cancer. Gynecol Oncol. 2018;151(2): 306-310.
Crossref Google Scholar
105

Ishibashi M, Toyoshima M, Zhang X, et al. Tyrosine kinase receptor TIE-1 mediates platinum resistance by promoting nucleotide excision repair in ovarian cancer. Sci Rep. 2018;8(1): 13207.
Crossref Google Scholar
106

Yerlici VT, Lu MW, Hoge CR, et al. Programmed genome rearrangements in Oxytricha produce transcriptionally active extrachromosomal circular DNA. Nucleic Acids Res. 2019;47(18): 9741-9760.
Crossref Google Scholar
107

Wu S, Turner KM, Nguyen N, et al. Circular ecDNA promotes accessible chromatin and high oncogene expression. Nature. 2019;575(7784): 699-703.
Crossref Google Scholar
108

Sunnerhagen P, Sjoberg RM, Karlsson AL, Lundh L, Bjursell G. Molecular cloning and characterization of small polydisperse circular DNA from mouse 3T6 cells. Nucleic Acids Res. 1986;14(20): 7823-7838.
Crossref Google Scholar
109

Bertelsen AH, Humayun MZ, Karfopoulos SG, Rush MG. Molecular characterization of small polydisperse circular deoxyribonucleic acid from an African green monkey cell line. Biochemistry. 1982;21(9): 2076-2085.
Crossref Google Scholar
110

Turner KM, Deshpande V, Beyter D, et al. Extrachromosomal oncogene amplification drives tumour evolution and genetic heterogeneity. Nature. 2017;543(7643): 122-125.
Crossref Google Scholar
111

Vogt N, Gibaud A, Lemoine F, de la Grange P, Debatisse M, Malfoy B. Amplicon rearrangements during the extrachromosomal and intrachromosomal amplification process in a glioma. Nucleic Acids Res. 2014;42(21): 13194-13205.
Crossref Google Scholar
112

Kumar P, Dillon LW, Shibata Y, Jazaeri AA, Jones DR, Dutta A. Normal and cancerous tissues release extrachromosomal circular DNA (eccDNA) into the circulation. Mol Cancer Res. 2017;15(9): 1197-1205.
Crossref Google Scholar
113

Shibata Y, Kumar P, Layer R, et al. Extrachromosomal microDNAs and chromosomal microdeletions in normal tissues. Science. 2012;336(6077): 82-86.
Crossref Google Scholar
114

Poon C, Duan X, Chan C, Han W, Lin W. Nanoscale coordination polymers codeliver carboplatin and gemcitabine for highly effective treatment of platinum-resistant ovarian cancer. Mol Pharm. 2016;13(11): 3665-3675.
Crossref Google Scholar
115

Salzano G, Navarro G, Trivedi MS, De Rosa G, Torchilin VP. Multifunctional polymeric micelles Co-loaded with anti-survivin siRNA and paclitaxel overcome drug resistance in an animal model of ovarian cancer. Mol Cancer Ther. 2015;14(4): 1075-1084.
Crossref Google Scholar
116

He C, Liu D, Lin W. Self-assembled nanoscale coordination polymers carrying siRNAs and cisplatin for effective treatment of resistant ovarian cancer. Biomaterials. 2015;36: 124-133.
Crossref Google Scholar
117

Yavuz MS, Cheng Y, Chen J, et al. Gold nanocages covered by smart polymers for controlled release with near-infrared light. Nat Mater. 2009;8(12): 935-939.
Crossref Google Scholar
118
Siwak DR, Tari AM, Lopez-Berestein G. The potential of drug-carrying immunoliposomes as anticancer agents. Commentary re: J. W. Park et al., Anti-HER2 immunoliposomes: enhanced efficacy due to targeted delivery. Clin. Cancer Res. 8: 1172-1181, 2002. Clin Cancer Res. 2002;8(4): 955-956.
119

Butler JS, Sadler PJ. Targeted delivery of platinum-based anticancer complexes. Curr Opin Chem Biol. 2013;17(2): 175-188.
Crossref Google Scholar
120

Liu T, Yacoub R, Taliaferro-Smith LD, et al. Combinatorial effects of lapatinib and rapamycin in triple-negative breast cancer cells. Mol Cancer Ther. 2011;10(8): 1460-1469.
Crossref Google Scholar
121

Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol. 2007;2(12): 751-760.
Crossref Google Scholar
122

Qi R, Wang Y, Bruno PM, et al. Author Correction: nanoparticle conjugates of a highly potent toxin enhance safety and circumvent platinum resistance in ovarian cancer. Nat Commun. 2020;11(1): 1940.
Crossref Google Scholar
123

Min Y, Mao CQ, Chen S, Ma G, Wang J, Liu Y. Combating the drug resistance of cisplatin using a platinum prodrug based delivery system. Angew Chem Int Ed Engl. 2012;51(27): 6742-6747.
Crossref Google Scholar
124

Yu C, Ding B, Zhang X, et al. Targeted iron nanoparticles with platinum-(Ⅳ) prodrugs and anti-EZH2 siRNA show great synergy in combating drug resistance in vitro and in vivo. Biomaterials. 2018;155: 112-123.
Crossref Google Scholar
125

Lee PS, Teaberry VS, Bland AE, et al. Elevated MAL expression is accompanied by promoter hypomethylation and platinum resistance in epithelial ovarian cancer. Int J Cancer. 2010;126(6): 1378-1389.
Crossref Google Scholar
126

Mohell N, Alfredsson J, Fransson A, et al. APR-246 overcomes resistance to cisplatin and doxorubicin in ovarian cancer cells. Cell Death Dis. 2015;6(6): e1794.
Crossref Google Scholar
127

Reyes-Gonzalez JM, Armaiz-Pena GN, Mangala LS, et al. Targeting c-MYC in platinum-resistant ovarian cancer. Mol Cancer Ther. 2015;14(10): 2260-2269.
Crossref Google Scholar
128

Hudson CD, Savadelis A, Nagaraj AB, et al. Altered glutamine metabolism in platinum resistant ovarian cancer. Oncotarget. 2016;7(27): 41637-41649.
Crossref Google Scholar
129

Chen Y, Camacho SC, Silvers TR, et al. Inhibition of the nuclear export receptor XPO1 as a therapeutic target for platinum-resistant ovarian cancer. Clin Cancer Res. 2017;23(6): 1552-1563.
Crossref Google Scholar
130

Moore KN, Martin LP, O'Malley DM, et al. Safety and activity of mirvetuximab soravtansine (IMGN853), a folate receptor alpha-targeting antibody-drug conjugate, in platinum-resistant ovarian, fallopian tube, or primary peritoneal cancer: a phase Ⅰ expansion study. J Clin Oncol. 2017;35(10): 1112-1118.
Crossref Google Scholar
131

Mukherjee A, Huynh V, Gaines K, Reh WA, Vasquez KM. Targeting the high-mobility group box 3 protein sensitizes chemoresistant ovarian cancer cells to cisplatin. Cancer Res. 2019;79(13): 3185-3191.
Crossref Google Scholar
132

Li Z, Zhou W, Zhang Y, et al. ERK regulates HIF1alpha-mediated platinum resistance by directly targeting PHD2 in ovarian cancer. Clin Cancer Res. 2019;25(19): 5947-5960.
Crossref Google Scholar
133

Marchetti C, Palaia I, De Felice F, et al. Tyrosine-kinases inhibitors in recurrent platinum-resistant ovarian cancer patients. Cancer Treat Rev. 2016;42: 41-46.
Crossref Google Scholar
134

Bauerschlag DO, Hilpert F, Meier W, et al. Evaluation of potentially predictive markers for anti-angiogenic therapy with sunitinib in recurrent ovarian cancer patients. Transl Oncol. 2013;6(3): 305-310.
Crossref Google Scholar
135

Baumann KH, du Bois A, Meier W, et al. A phase Ⅱ trial (AGO 2.11) in platinum-resistant ovarian cancer: a randomized multicenter trial with sunitinib (SU11248) to evaluate dosage, schedule, tolerability, toxicity and effectiveness of a multitargeted receptor tyrosine kinase inhibitor monotherapy. Ann Oncol. 2012;23(9): 2265-2271.
Crossref Google Scholar
136

Sartori A, Corno C, De Cesare M, et al. Efficacy of a selective binder of alphaVbeta3 integrin linked to the tyrosine kinase inhibitor sunitinib in ovarian carcinoma preclinical models. Cancers (Basel). 2019;11(4): 531.
Crossref Google Scholar
137

Harter P, Sehouli J, Kimmig R, et al. Addition of vandetanib to pegylated liposomal doxorubicin (PLD) in patients with recurrent ovarian cancer. A randomized phase Ⅰ/Ⅱ study of the AGO Study Group (AGO-OVAR 2.13). Invest New Drugs. 2013;31(6): 1499-1504.
Crossref Google Scholar
138

Lan CY, Wang Y, Xiong Y, et al. Apatinib combined with oral etoposide in patients with platinum-resistant or platinum-refractory ovarian cancer (AEROC): a phase 2, single-arm, prospective study. Lancet Oncol. 2018;19(9): 1239-1246.
Crossref Google Scholar
139

Jin M, Cai J, Wang X, Zhang T, Zhao Y. Successful maintenance therapy with apatinib inplatinum-resistant advanced ovarian cancer and literature review. Cancer Biol Ther. 2018;19(12): 1088-1092.
Crossref Google Scholar
140

Quinn JM, Greenwade MM, Palisoul ML, et al. Therapeutic inhibition of the receptor tyrosine kinase AXL improves sensitivity to platinum and taxane in ovarian cancer. Mol Cancer Ther. 2019;18(2): 389-398.
Crossref Google Scholar
141

Levy A, Alhazzani K, Dondapati P, et al. Focal adhesion kinase in ovarian cancer: a potential therapeutic target for platinum and taxane-resistant tumors. Curr Cancer Drug Targets. 2019;19(3): 179-188.
Crossref Google Scholar
142

Morgan RD, Clamp AR, Evans DGR, Edmondson RJ, Jayson GC. PARP inhibitors in platinum-sensitive high-grade serous ovarian cancer. Cancer Chemother Pharmacol. 2018;81(4): 647-658.
Crossref Google Scholar
143

Rodriguez-Freixinos V, Farinas-Madrid L, Gil-Martin M, et al. Chemotherapy and PARP inhibitors in heavily pretreated BRCA1/2 mutation ovarian cancer (BMOC) patients. Gynecol Oncol. 2019;152(2): 270-277.
Crossref Google Scholar
144

Jenner ZB, Sood AK, Coleman RL. Evaluation of rucaparib and companion diagnostics in the PARP inhibitor landscape for recurrent ovarian cancer therapy. Future Oncol. 2016;12(12): 1439-1456.
Crossref Google Scholar
145

Oza AM, Tinker AV, Oaknin A, et al. Antitumor activity and safety of the PARP inhibitor rucaparib in patients with high-grade ovarian carcinoma and a germline or somatic BRCA1 or BRCA2 mutation: integrated analysis of data from Study 10 and ARIEL2. Gynecol Oncol. 2017;147(2): 267-275.
Crossref Google Scholar
146

Fong PC, Yap TA, Boss DS, et al. Poly(ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol. 2010;28(15): 2512-2519.
Crossref Google Scholar
147

Domchek SM, Aghajanian C, Shapira-Frommer R, et al. Efficacy and safety of olaparib monotherapy in germline BRCA1/2 mutation carriers with advanced ovarian cancer and three or more lines of prior therapy. Gynecol Oncol. 2016;140(2): 199-203.
Crossref Google Scholar
148

Konstantinopoulos PA, Waggoner S, Vidal GA, et al. Single-Arm phases 1 and 2 trial of niraparib in combination with pembrolizumab in patients with recurrent platinum-resistant ovarian carcinoma. JAMA Oncol. 2019;5(8): 1141-1149.
Crossref Google Scholar
149

Alkema NG, Wisman GB, van der Zee AG, van Vugt MA, de Jong S. Studying platinum sensitivity and resistance in high-grade serous ovarian cancer: different models for different questions. Drug Resist Updat. 2016;24: 55-69.
Crossref Google Scholar
150

Chen FD, Chen HH, Ke SC, Zheng LR, Zheng XY. SLC27A2 regulates miR-411 to affect chemo-resistance in ovarian cancer. Neoplasma. 2018;65(6): 915-924.
Crossref Google Scholar
151

Samuel P, Pink RC, Caley DP, Currie JM, Brooks SA, Carter DR. Over-expression of miR-31 or loss of KCNMA1 leads to increased cisplatin resistance in ovarian cancer cells. Tumour Biol. 2016;37(2): 2565-2573.
Crossref Google Scholar
152

Mitra R, Chen X, Greenawalt EJ, et al. Decoding critical long non-coding RNA in ovarian cancer epithelial-to-mesenchymal transition. Nat Commun. 2017;8(1): 1604.
Crossref Google Scholar
153

Yin G, Chen R, Alvero AB, et al. TWISTing stemness, inflammation and proliferation of epithelial ovarian cancer cells through MIR199A2/214. Oncogene. 2010;29(24): 3545-3553.
Crossref Google Scholar
154

Bai L, Wang A, Zhang Y, Xu X, Zhang X. Knockdown of MALAT1 enhances chemosensitivity of ovarian cancer cells to cisplatin through inhibiting the Notch1 signaling pathway. Exp Cell Res. 2018;366(2): 161-171.
Crossref Google Scholar
155

Wu L, Wang X, Guo Y. Long non-coding RNA MALAT1 is upregulated and involved in cell proliferation, migration and apoptosis in ovarian cancer. Exp Ther Med. 2017;13(6): 3055-3060.
Crossref Google Scholar
156

Wang F, Zhou J, Xie X, et al. Involvement of SRPK1 in cisplatin resistance related to long non-coding RNA UCA1 in human ovarian cancer cells. Neoplasma. 2015;62(3): 432-438.
Crossref Google Scholar
157

Yan H, Xia JY, Feng FZ. Long non-coding RNA ENST00000457645 reverses cisplatin resistance in CP70 ovarian cancer cells. Genet Mol Res. 2017;16(1): gmr16019411.
Crossref Google Scholar
158

Ozes AR, Miller DF, Ozes ON, et al. NF-kappaB-HOTAIR axis links DNA damage response, chemoresistance and cellular senescence in ovarian cancer. Oncogene. 2016;35(41): 5350-5361.
Crossref Google Scholar
159

Teschendorff AE, Lee SH, Jones A, et al. HOTAIR and its surrogate DNA methylation signature indicate carboplatin resistance in ovarian cancer. Genome Med. 2015;7: 108.
Crossref Google Scholar
160

Li J, Huang H, Li Y, Li L, Hou W, You Z. Decreased expression of long non-coding RNA GAS5 promotes cell proliferation, migration and invasion, and indicates a poor prognosis in ovarian cancer. Oncol Rep. 2016;36(6): 3241-3250.
Crossref Google Scholar
Genes & Diseases
Volume 9 Issue 3,
May 2022
Pages 668-681
DOI: 10.1016/j.gendis.2020.11.017
Cite this article:
Guo C, Song C, Zhang J, et al. Revisiting chemoresistance in ovarian cancer: Mechanism, biomarkers, and precision medicine. Genes & Diseases, 2022, 9(3): 668-681. https://doi.org/10.1016/j.gendis.2020.11.017

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Received: 06 June 2020
Revised: 29 October 2020
Accepted: 24 November 2020
Published: 01 December 2020
© 2020, Chongqing Medical University.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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