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Identification of Quercetin as a Natural MMP1 Inhibitor for Overcoming Cisplatin Resistance in Epithelial Ovarian Cancer.

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Τίτλος: Identification of Quercetin as a Natural MMP1 Inhibitor for Overcoming Cisplatin Resistance in Epithelial Ovarian Cancer.
Συγγραφείς: Wang S; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.; Chinese Medicine Guangdong Laboratory (Hengqin Laboratory), Guangdong-Macao ln-Depth Cooperation Zone in Hengqin, 519000, China., Zhao Z; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China., Yu L; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China., Wang J; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China., Ouyang Y; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.; Chinese Medicine Guangdong Laboratory (Hengqin Laboratory), Guangdong-Macao ln-Depth Cooperation Zone in Hengqin, 519000, China., Zhou H; Chinese Medicine Guangdong Laboratory (Hengqin Laboratory), Guangdong-Macao ln-Depth Cooperation Zone in Hengqin, 519000, China., Shen W; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.; The First Clinical Medical College, Nanjing University of Chinese Medicine, Nanjing, 210023, Jiangsu, China; Collaborative Innovation Center of Traditional Chinese Medicine Prevention and Treatment of Tumor, Nanjing, 210023, Jiangsu, China., Wu Q; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.; Chinese Medicine Guangdong Laboratory (Hengqin Laboratory), Guangdong-Macao ln-Depth Cooperation Zone in Hengqin, 519000, China.
Πηγή: Journal of Cancer [J Cancer] 2025 May 31; Vol. 16 (8), pp. 2578-2594. Date of Electronic Publication: 2025 May 31 (Print Publication: 2025).
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Ivyspring International Publisher Country of Publication: Australia NLM ID: 101535920 Publication Model: eCollection Cited Medium: Print ISSN: 1837-9664 (Print) Linking ISSN: 18379664 NLM ISO Abbreviation: J Cancer Subsets: PubMed not MEDLINE
Imprint Name(s): Original Publication: Wyoming, N.S.W. : Ivyspring International Publisher, 2010-
Περίληψη: Background: It is challenging to find a therapeutic Chinese medicine monomer (CHMs) for platinum-resistant patients, who currently have few treatment options, due to the complex mechanisms and the large number of CHMs available. This study aimed to identify CHM to overcome cisplatin resistance in EOC through bioinformatics analysis with in vitro experiment. Methods: This study used a strategy opposite to conventional network pharmacology. RNA expression of cisplatin sensitive and resistant EOC cell lines was obtained from the GEO database. Through differential expression gene (DEG) analysis, PPI network analysis, and survival analysis, we identified hub genes related to platinum resistance. CHMs targeting these hub genes were identified from the HIT 2.0 and molecular docking, molecular dynamics (MD) simulations, and SPR assay were used to validate their binding ability. Then, the anti-cancer effects of CHM in cisplatin-resistant cell lines were verified via in vitro experiment. Results: 16 hub genes were selected through DEG and PPI network analysis. Following validation via survival analysis in the TCGA-OV cohort, the investigation ultimately focused on MMP1. Western blotting results demonstrated that MAPK signaling pathway activation induced MMP1 expression in cisplatin-resistant EOC cells. 22 CHMs targeting MMP1 were found in HIT 2.0 and quercetin was demonstrated the strong affinity of quercetin for MMP1 via molecular docking, MD simulations and SPR assay. Quercetin also exhibited strong binding affinity to other hub genes, including EGR1, STAT1, and PRKCA. In vitro experiments demonstrated that quercetin effectively inhibited the proliferation, apoptosis resistance, invasion, and migration of cisplatin-resistant EOC cells. The combination of cisplatin and quercetin had a strong synergistic effect, as indicated by the ZIP synergy score (≥10). Conclusion: Our study identified quercetin, which functions by targeting multiple cisplatin resistance-related proteins, including MMP1, as a potential therapeutic CHM for cisplatin resistant EOC. This study also explored quercetin's mechanisms against platinum-resistant ovarian cancer. By identifying hub platinum-resistance associated genes and screening potential CHMs through bioinformatics, computer simulation, and in vitro experiments, this integrated analytical approach also offers a reference for discovering CHMs for other diseases.
(© The author(s).)
Competing Interests: Competing Interests: The authors have declared that no competing interest exists.
References: Nature. 2011 Dec 21;480(7378):S82-3. (PMID: 22190085)
Oncol Rep. 2022 Apr;47(4):. (PMID: 35211759)
Ann Oncol. 2021 Apr;32(4):512-521. (PMID: 33453391)
Crit Rev Food Sci Nutr. 2018 Jun 13;58(9):1428-1447. (PMID: 28001084)
Int J Gynecol Cancer. 2013 Feb;23(2):256-63. (PMID: 23358177)
Front Cell Infect Microbiol. 2022 Aug 15;12:964469. (PMID: 36046748)
FEBS Open Bio. 2023 Aug;13(8):1495-1506. (PMID: 37151134)
Lancet Oncol. 2022 Aug;23(8):e374-e384. (PMID: 35901833)
Nat Clin Pract Oncol. 2006 Nov;3(11):604-11. (PMID: 17080178)
Cell Signal. 2024 Jul;119:111180. (PMID: 38642782)
Chem Biol Drug Des. 2020 Feb;95(2):215-223. (PMID: 31512406)
Kaohsiung J Med Sci. 2021 Feb;37(2):128-135. (PMID: 33280258)
Mol Cancer. 2024 Oct 1;23(1):218. (PMID: 39354529)
Phytother Res. 2016 Jan;30(1):84-9. (PMID: 26503061)
J Ethnopharmacol. 2023 Jun 12;309:116306. (PMID: 36858276)
Clin Cancer Res. 1996 Apr;2(4):659-68. (PMID: 9816216)
Gynecol Oncol. 2011 Feb;120(2):247-55. (PMID: 21093894)
Front Oncol. 2024 Sep 09;14:1446328. (PMID: 39314630)
J Cancer. 2025 Jan 1;16(1):92-109. (PMID: 39744564)
Chin J Nat Med. 2023 May;21(5):323-332. (PMID: 37245871)
J Transl Med. 2023 Dec 19;21(1):920. (PMID: 38115108)
Nat Commun. 2017 Mar 06;8:14470. (PMID: 28262727)
Cancer Drug Resist. 2022 Apr 3;5(2):304-316. (PMID: 35800369)
Expert Rev Anticancer Ther. 2017 Dec;17(12):1147-1158. (PMID: 29086618)
Pharmacol Res. 2020 Sep;159:104934. (PMID: 32464330)
Anticancer Res. 2019 Dec;39(12):6443-6455. (PMID: 31810908)
J Ethnopharmacol. 2025 Jan 30;337(Pt 1):118811. (PMID: 39251149)
Phytomedicine. 2022 Jan;95:153786. (PMID: 34785104)
Int J Mol Sci. 2020 Dec 20;21(24):. (PMID: 33419373)
J Exp Clin Cancer Res. 2018 Feb 20;37(1):32. (PMID: 29458390)
Trends Pharmacol Sci. 2022 Feb;43(2):136-150. (PMID: 34895945)
Cancers (Basel). 2022 Feb 09;14(4):. (PMID: 35205603)
Cancer Biol Med. 2020 Feb 15;17(1):60-75. (PMID: 32296587)
J Ethnopharmacol. 2024 Jul 15;329:118144. (PMID: 38583732)
Breast Cancer (Dove Med Press). 2024 Dec 20;16:993-1004. (PMID: 39720358)
J Biol Chem. 2013 Aug 16;288(33):23740-50. (PMID: 23833193)
Expert Opin Investig Drugs. 2021 Jul;30(7):695-707. (PMID: 34082614)
Contributed Indexing: Keywords: Cisplatin resistance; Epithelial ovarian cancer; In vitro validation.; MMP1; Molecular docking; Natural products
Entry Date(s): Date Created: 20250619 Latest Revision: 20250620
Update Code: 20260130
PubMed Central ID: PMC12171002
DOI: 10.7150/jca.110517
PMID: 40535817
Βάση Δεδομένων: MEDLINE
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  Data: Identification of Quercetin as a Natural MMP1 Inhibitor for Overcoming Cisplatin Resistance in Epithelial Ovarian Cancer.
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  Data: <searchLink fieldCode="AU" term="%22Wang+S%22">Wang S</searchLink>; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.; Chinese Medicine Guangdong Laboratory (Hengqin Laboratory), Guangdong-Macao ln-Depth Cooperation Zone in Hengqin, 519000, China.<br /><searchLink fieldCode="AU" term="%22Zhao+Z%22">Zhao Z</searchLink>; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.<br /><searchLink fieldCode="AU" term="%22Yu+L%22">Yu L</searchLink>; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.<br /><searchLink fieldCode="AU" term="%22Wang+J%22">Wang J</searchLink>; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.<br /><searchLink fieldCode="AU" term="%22Ouyang+Y%22">Ouyang Y</searchLink>; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.; Chinese Medicine Guangdong Laboratory (Hengqin Laboratory), Guangdong-Macao ln-Depth Cooperation Zone in Hengqin, 519000, China.<br /><searchLink fieldCode="AU" term="%22Zhou+H%22">Zhou H</searchLink>; Chinese Medicine Guangdong Laboratory (Hengqin Laboratory), Guangdong-Macao ln-Depth Cooperation Zone in Hengqin, 519000, China.<br /><searchLink fieldCode="AU" term="%22Shen+W%22">Shen W</searchLink>; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.; The First Clinical Medical College, Nanjing University of Chinese Medicine, Nanjing, 210023, Jiangsu, China; Collaborative Innovation Center of Traditional Chinese Medicine Prevention and Treatment of Tumor, Nanjing, 210023, Jiangsu, China.<br /><searchLink fieldCode="AU" term="%22Wu+Q%22">Wu Q</searchLink>; Faculty of Chinese Medicine and State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, 999078 Macao, China.; Chinese Medicine Guangdong Laboratory (Hengqin Laboratory), Guangdong-Macao ln-Depth Cooperation Zone in Hengqin, 519000, China.
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  Data: Background: It is challenging to find a therapeutic Chinese medicine monomer (CHMs) for platinum-resistant patients, who currently have few treatment options, due to the complex mechanisms and the large number of CHMs available. This study aimed to identify CHM to overcome cisplatin resistance in EOC through bioinformatics analysis with in vitro experiment. Methods: This study used a strategy opposite to conventional network pharmacology. RNA expression of cisplatin sensitive and resistant EOC cell lines was obtained from the GEO database. Through differential expression gene (DEG) analysis, PPI network analysis, and survival analysis, we identified hub genes related to platinum resistance. CHMs targeting these hub genes were identified from the HIT 2.0 and molecular docking, molecular dynamics (MD) simulations, and SPR assay were used to validate their binding ability. Then, the anti-cancer effects of CHM in cisplatin-resistant cell lines were verified via in vitro experiment. Results: 16 hub genes were selected through DEG and PPI network analysis. Following validation via survival analysis in the TCGA-OV cohort, the investigation ultimately focused on MMP1. Western blotting results demonstrated that MAPK signaling pathway activation induced MMP1 expression in cisplatin-resistant EOC cells. 22 CHMs targeting MMP1 were found in HIT 2.0 and quercetin was demonstrated the strong affinity of quercetin for MMP1 via molecular docking, MD simulations and SPR assay. Quercetin also exhibited strong binding affinity to other hub genes, including EGR1, STAT1, and PRKCA. In vitro experiments demonstrated that quercetin effectively inhibited the proliferation, apoptosis resistance, invasion, and migration of cisplatin-resistant EOC cells. The combination of cisplatin and quercetin had a strong synergistic effect, as indicated by the ZIP synergy score (≥10). Conclusion: Our study identified quercetin, which functions by targeting multiple cisplatin resistance-related proteins, including MMP1, as a potential therapeutic CHM for cisplatin resistant EOC. This study also explored quercetin's mechanisms against platinum-resistant ovarian cancer. By identifying hub platinum-resistance associated genes and screening potential CHMs through bioinformatics, computer simulation, and in vitro experiments, this integrated analytical approach also offers a reference for discovering CHMs for other diseases.<br /> (© The author(s).)
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  Data: Competing Interests: The authors have declared that no competing interest exists.
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  Data: Nature. 2011 Dec 21;480(7378):S82-3. (PMID: <searchLink fieldCode="PM" term="%2222190085%22">22190085)</searchLink><br />Oncol Rep. 2022 Apr;47(4):. (PMID: <searchLink fieldCode="PM" term="%2235211759%22">35211759)</searchLink><br />Ann Oncol. 2021 Apr;32(4):512-521. (PMID: <searchLink fieldCode="PM" term="%2233453391%22">33453391)</searchLink><br />Crit Rev Food Sci Nutr. 2018 Jun 13;58(9):1428-1447. (PMID: <searchLink fieldCode="PM" term="%2228001084%22">28001084)</searchLink><br />Int J Gynecol Cancer. 2013 Feb;23(2):256-63. (PMID: <searchLink fieldCode="PM" term="%2223358177%22">23358177)</searchLink><br />Front Cell Infect Microbiol. 2022 Aug 15;12:964469. (PMID: <searchLink fieldCode="PM" term="%2236046748%22">36046748)</searchLink><br />FEBS Open Bio. 2023 Aug;13(8):1495-1506. (PMID: <searchLink fieldCode="PM" term="%2237151134%22">37151134)</searchLink><br />Lancet Oncol. 2022 Aug;23(8):e374-e384. (PMID: <searchLink fieldCode="PM" term="%2235901833%22">35901833)</searchLink><br />Nat Clin Pract Oncol. 2006 Nov;3(11):604-11. (PMID: <searchLink fieldCode="PM" term="%2217080178%22">17080178)</searchLink><br />Cell Signal. 2024 Jul;119:111180. (PMID: <searchLink fieldCode="PM" term="%2238642782%22">38642782)</searchLink><br />Chem Biol Drug Des. 2020 Feb;95(2):215-223. (PMID: <searchLink fieldCode="PM" term="%2231512406%22">31512406)</searchLink><br />Kaohsiung J Med Sci. 2021 Feb;37(2):128-135. (PMID: <searchLink fieldCode="PM" term="%2233280258%22">33280258)</searchLink><br />Mol Cancer. 2024 Oct 1;23(1):218. (PMID: <searchLink fieldCode="PM" term="%2239354529%22">39354529)</searchLink><br />Phytother Res. 2016 Jan;30(1):84-9. (PMID: <searchLink fieldCode="PM" term="%2226503061%22">26503061)</searchLink><br />J Ethnopharmacol. 2023 Jun 12;309:116306. (PMID: <searchLink fieldCode="PM" term="%2236858276%22">36858276)</searchLink><br />Clin Cancer Res. 1996 Apr;2(4):659-68. (PMID: <searchLink fieldCode="PM" term="%229816216%22">9816216)</searchLink><br />Gynecol Oncol. 2011 Feb;120(2):247-55. (PMID: <searchLink fieldCode="PM" term="%2221093894%22">21093894)</searchLink><br />Front Oncol. 2024 Sep 09;14:1446328. (PMID: <searchLink fieldCode="PM" term="%2239314630%22">39314630)</searchLink><br />J Cancer. 2025 Jan 1;16(1):92-109. (PMID: <searchLink fieldCode="PM" term="%2239744564%22">39744564)</searchLink><br />Chin J Nat Med. 2023 May;21(5):323-332. (PMID: <searchLink fieldCode="PM" term="%2237245871%22">37245871)</searchLink><br />J Transl Med. 2023 Dec 19;21(1):920. (PMID: <searchLink fieldCode="PM" term="%2238115108%22">38115108)</searchLink><br />Nat Commun. 2017 Mar 06;8:14470. (PMID: <searchLink fieldCode="PM" term="%2228262727%22">28262727)</searchLink><br />Cancer Drug Resist. 2022 Apr 3;5(2):304-316. (PMID: <searchLink fieldCode="PM" term="%2235800369%22">35800369)</searchLink><br />Expert Rev Anticancer Ther. 2017 Dec;17(12):1147-1158. (PMID: <searchLink fieldCode="PM" term="%2229086618%22">29086618)</searchLink><br />Pharmacol Res. 2020 Sep;159:104934. (PMID: <searchLink fieldCode="PM" term="%2232464330%22">32464330)</searchLink><br />Anticancer Res. 2019 Dec;39(12):6443-6455. (PMID: <searchLink fieldCode="PM" term="%2231810908%22">31810908)</searchLink><br />J Ethnopharmacol. 2025 Jan 30;337(Pt 1):118811. (PMID: <searchLink fieldCode="PM" term="%2239251149%22">39251149)</searchLink><br />Phytomedicine. 2022 Jan;95:153786. (PMID: <searchLink fieldCode="PM" term="%2234785104%22">34785104)</searchLink><br />Int J Mol Sci. 2020 Dec 20;21(24):. (PMID: <searchLink fieldCode="PM" term="%2233419373%22">33419373)</searchLink><br />J Exp Clin Cancer Res. 2018 Feb 20;37(1):32. (PMID: <searchLink fieldCode="PM" term="%2229458390%22">29458390)</searchLink><br />Trends Pharmacol Sci. 2022 Feb;43(2):136-150. (PMID: <searchLink fieldCode="PM" term="%2234895945%22">34895945)</searchLink><br />Cancers (Basel). 2022 Feb 09;14(4):. (PMID: <searchLink fieldCode="PM" term="%2235205603%22">35205603)</searchLink><br />Cancer Biol Med. 2020 Feb 15;17(1):60-75. (PMID: <searchLink fieldCode="PM" term="%2232296587%22">32296587)</searchLink><br />J Ethnopharmacol. 2024 Jul 15;329:118144. (PMID: <searchLink fieldCode="PM" term="%2238583732%22">38583732)</searchLink><br />Breast Cancer (Dove Med Press). 2024 Dec 20;16:993-1004. (PMID: <searchLink fieldCode="PM" term="%2239720358%22">39720358)</searchLink><br />J Biol Chem. 2013 Aug 16;288(33):23740-50. (PMID: <searchLink fieldCode="PM" term="%2223833193%22">23833193)</searchLink><br />Expert Opin Investig Drugs. 2021 Jul;30(7):695-707. (PMID: <searchLink fieldCode="PM" term="%2234082614%22">34082614)</searchLink>
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