Exosomal miR-493 suppresses MAD2L1 and induces chemoresistance to intraperitoneal paclitaxel therapy in gastric cancer patients with peritoneal metastasis.
Humans
MicroRNAs
/ genetics
Stomach Neoplasms
/ drug therapy
Paclitaxel
/ pharmacology
Drug Resistance, Neoplasm
/ genetics
Exosomes
/ metabolism
Peritoneal Neoplasms
/ secondary
Cell Line, Tumor
Male
Female
Mad2 Proteins
/ metabolism
Middle Aged
Gene Expression Regulation, Neoplastic
/ drug effects
Aged
Antineoplastic Agents, Phytogenic
/ pharmacology
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
02 May 2024
02 May 2024
Historique:
received:
25
12
2023
accepted:
29
04
2024
medline:
3
5
2024
pubmed:
3
5
2024
entrez:
2
5
2024
Statut:
epublish
Résumé
Intraperitoneal (IP) chemotherapy with paclitaxel (PTX) for gastric cancer (GC) with peritoneal metastasis (PM) is considered a promising treatment approach, however, there are no useful biomarkers to predict the efficacy of IP therapy. We examined the association between intra-peritoneal exosomes, particularly exosomal micro-RNAs (exo-miRNAs), and IP-chemo sensitivity. MKN45 cells that were cultured with intra-peritoneal exosomes from patients who did not respond to IP therapy with PTX (IP
Identifiants
pubmed: 38698201
doi: 10.1038/s41598-024-60967-x
pii: 10.1038/s41598-024-60967-x
doi:
Substances chimiques
MicroRNAs
0
Paclitaxel
P88XT4IS4D
Mad2 Proteins
0
MAD2L1 protein, human
0
MIRN493 microRNA, human
0
Antineoplastic Agents, Phytogenic
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
10075Informations de copyright
© 2024. The Author(s).
Références
Sung, H. et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71, 209–249 (2021).
pubmed: 33538338
doi: 10.3322/caac.21660
Siegel, R. L., Miller, K. D. & Jemal, A. Cancer statistics, 2019. CA Cancer J. Clin. 69, 7–34 (2019).
pubmed: 30620402
doi: 10.3322/caac.21551
Siegel, R. L., Miller, K. D., Wagle, N. S. & Jemal, A. Cancer statistics, 2023. CA Cancer J. Clin. 73, 17–48 (2023).
pubmed: 36633525
doi: 10.3322/caac.21763
Nashimoto, A. et al. Gastric cancer treated in 2002 in Japan: 2009 annual report of the JGCA nationwide registry. Gastric Cancer 16, 1–27 (2013).
pubmed: 22729699
doi: 10.1007/s10120-012-0163-4
Zhu, B. Y. et al. Prognostic factors and recurrence patterns in T4 gastric cancer patients after curative resection. J. Cancer 10, 1181–1188 (2019).
pubmed: 30854127
pmcid: 6400673
doi: 10.7150/jca.28993
Sugarbaker, P. H. & Yonemura, Y. Clinical pathway for the management of resectable gastric cancer with peritoneal seeding: Best palliation with a ray of hope for cure. Oncology 58, 96–107 (2000).
pubmed: 10705236
doi: 10.1159/000012086
Cunningham, D. et al. Capecitabine and oxaliplatin for advanced esophagogastric cancer. N. Engl. J. Med. 358, 36–46 (2008).
pubmed: 18172173
doi: 10.1056/NEJMoa073149
Yamada, Y. et al. Phase III study comparing oxaliplatin plus S-1 with cisplatin plus S-1 in chemotherapy-naïve patients with advanced gastric cancer. Ann. Oncol. 26, 141–148 (2015).
pubmed: 25316259
doi: 10.1093/annonc/mdu472
Bang, Y. J. et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): A phase 3, open-label, randomised controlled trial. Lancet 376, 687–697 (2010).
pubmed: 20728210
doi: 10.1016/S0140-6736(10)61121-X
Kang, Y. K. et al. Nivolumab plus chemotherapy versus placebo plus chemotherapy in patients with HER2-negative, untreated, unresectable advanced or recurrent gastric or gastro-oesophageal junction cancer (ATTRACTION-4): A randomised, multicentre, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 23, 234–247 (2022).
pubmed: 35030335
doi: 10.1016/S1470-2045(21)00692-6
Janjigian, Y. Y. et al. First-line nivolumab plus chemotherapy versus chemotherapy alone for advanced gastric, gastro-oesophageal junction, and oesophageal adenocarcinoma (CheckMate 649): A randomised, open-label, phase 3 trial. Lancet 398, 27–40 (2021).
pubmed: 34102137
pmcid: 8436782
doi: 10.1016/S0140-6736(21)00797-2
Ishigami, H. et al. Phase III trial comparing intraperitoneal and intravenous paclitaxel plus S-1 versus cisplatin plus S-1 in patients with gastric cancer with peritoneal metastasis: PHOENIX-GC Trial. J. Clin. Oncol. 36, 1922–1929 (2018).
pubmed: 29746229
doi: 10.1200/JCO.2018.77.8613
Ishigami, H. et al. Intraperitoneal chemotherapy as adjuvant or perioperative chemotherapy for patients with type 4 scirrhous gastric cancer: PHOENIX-GC2 Trial. J. Clin. Med. 10, 5666 (2021).
pubmed: 34884367
pmcid: 8658657
doi: 10.3390/jcm10235666
Valadi, H. et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654–659 (2007).
pubmed: 17486113
doi: 10.1038/ncb1596
Weidle, U. et al. Down-regulated microRNAs in gastric carcinoma may be targets for therapeutic intervention and replacement therapy. Anticancer Res. 41(9), 4185–4202 (2021).
pubmed: 34475038
doi: 10.21873/anticanres.15223
Shibamoto, J. et al. Removal of small extracellular vesicles inhibits the progression of peritoneal dissemination in gastric cancer. Gastric Cancer 25, 712–725 (2022).
pubmed: 35368210
doi: 10.1007/s10120-022-01293-x
Goldie, B. J. et al. Activity-associated miRNA are packaged in Map1b-enriched exosomes released from depolarized neurons. Nucleic Acids Res. 42, 9195–9208 (2014).
pubmed: 25053844
pmcid: 4132720
doi: 10.1093/nar/gku594
Miyazaki, K. et al. An exosome-based liquid biopsy signature for pre-operative identification of lymph node metastasis in patients with pathological high-risk T1 colorectal cancer. Mol. Cancer 22, 2 (2023).
pubmed: 36609320
pmcid: 9817247
doi: 10.1186/s12943-022-01685-8
So, J. B. Y. et al. Development and validation of a serum microRNA biomarker panel for detecting gastric cancer in a high-risk population. Gut 70, 829–837 (2021).
pubmed: 33028667
doi: 10.1136/gutjnl-2020-322065
Ohzawa, H. et al. Exosomal microRNA in peritoneal fluid as a biomarker of peritoneal metastases from gastric cancer. Ann. Gastroenterol. Surg. 4, 84–93 (2020).
pubmed: 32021962
doi: 10.1002/ags3.12296
Luo, J. et al. Exosomal hsa-let-7g-3p and hsa-miR-10395-3p derived from peritoneal lavage predict peritoneal metastasis and the efficacy of neoadjuvant intraperitoneal and systemic chemotherapy in patients with gastric cancer. Gastric Cancer 26, 364–378 (2023).
pubmed: 36738390
doi: 10.1007/s10120-023-01368-3
Sugezawa, K. et al. GPX4 regulates tumor cell proliferation via suppressing ferroptosis and exhibits prognostic significance in gastric cancer. Anticancer Res. 42, 5719–5729 (2022).
pubmed: 36456115
doi: 10.21873/anticanres.16079
Andersen, C. L., Jensen, J. L. & Ørntoft, T. F. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245–5250 (2004).
pubmed: 15289330
doi: 10.1158/0008-5472.CAN-04-0496
Okazaki, M. et al. The effect of HIF-1α and PKM1 expression on acquisition of chemoresistance. Cancer Manag. Res. 10, 1865–1874 (2018).
pubmed: 30013393
pmcid: 6037278
doi: 10.2147/CMAR.S166136
Tambe, M. et al. Novel Mad2-targeting miR-493-3p controls mitotic fidelity and cancer cells’ sensitivity to paclitaxel. Oncotarget 7, 12267–12285 (2016).
pubmed: 26943585
pmcid: 4914283
doi: 10.18632/oncotarget.7860
Jacquet, P. & Sugarbaker, P. H. Peritoneal-plasma barrier. Cancer Treat Res. 82, 53–63 (1996).
pubmed: 8849943
doi: 10.1007/978-1-4613-1247-5_4
Armstrong, D. K. et al. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N. Engl. J. Med. 354, 34–43 (2006).
pubmed: 16394300
doi: 10.1056/NEJMoa052985
Kitayama, J. et al. Treatment of patients with peritoneal metastases from gastric cancer. Ann. Gastroenterol. Surg. 2, 116–123 (2018).
pubmed: 29863151
pmcid: 5881364
doi: 10.1002/ags3.12060
Rowinsky, E. K. & Donehower, R. C. Paclitaxel (taxol). N. Engl. J. Med. 332, 1004–1014 (1995).
pubmed: 7885406
doi: 10.1056/NEJM199504133321507
Singla, A. K., Garg, A. & Aggarwal, D. Paclitaxel and its formulations. Int. J. Pharm. 235, 179–192 (2002).
pubmed: 11879753
doi: 10.1016/S0378-5173(01)00986-3
Yamamoto, M. et al. Delivery of aPD-L1 antibody to i.p. tumors via direct penetration by i.p. route: Beyond EPR effect. J. Control Release 352, 328–337 (2022).
pubmed: 36280153
doi: 10.1016/j.jconrel.2022.10.032
Eisenhauer, E. A. et al. New response evaluation criteria in solid tumours: Revised RECIST guideline (version 1.1). Eur. J. Cancer 45, 228–247 (2009).
pubmed: 19097774
doi: 10.1016/j.ejca.2008.10.026
Iizumi, S., Takashima, A., Sakamaki, K., Morita, S. & Boku, N. Survival impact of post-progression chemotherapy in advanced gastric cancer: Systematic review and meta-analysis. Cancer Chemother. Pharmacol. 81, 981–989 (2018).
pubmed: 29600386
doi: 10.1007/s00280-018-3569-9
Takashima, A., Iizumi, S. & Boku, N. Survival after failure of first-line chemotherapy in advanced gastric cancer patients: Differences between Japan and the rest of the world. Jpn. J. Clin. Oncol. 47, 583–589 (2017).
pubmed: 28398526
doi: 10.1093/jjco/hyx044
Hasegawa, H. et al. Optimal treatment change criteria for advanced gastric cancer with non-measurable peritoneal metastasis: Symptom/tumor marker-based versus CT-based. Anticancer Res. 34, 5169–5174 (2014).
pubmed: 25202110
Skinner, J. J., Wood, S., Shorter, J., Englander, S. W. & Black, B. E. The Mad2 partial unfolding model: Regulating mitosis through Mad2 conformational switching. J. Cell Biol. 183, 761–768 (2008).
pubmed: 19029339
pmcid: 2592820
doi: 10.1083/jcb.200808122
Kops, G. J., Weaver, B. A. & Cleveland, D. W. On the road to cancer: Aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 5, 773–785 (2005).
pubmed: 16195750
doi: 10.1038/nrc1714
Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell 100, 57–70 (2000).
pubmed: 10647931
doi: 10.1016/S0092-8674(00)81683-9
Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: The next generation. Cell 144, 646–674 (2011).
pubmed: 21376230
doi: 10.1016/j.cell.2011.02.013
Fang, X. & Zhang, P. Aneuploidy and tumorigenesis. Semin. Cell Dev. Biol. 22, 595–601 (2011).
pubmed: 21392584
pmcid: 3651908
doi: 10.1016/j.semcdb.2011.03.002
Bargiela-Iparraguirre, J. et al. Mad2 and BubR1 modulates tumourigenesis and paclitaxel response in MKN45 gastric cancer cells. Cell Cycle 13, 3590–3601 (2014).
pubmed: 25483095
pmcid: 4615044
doi: 10.4161/15384101.2014.962952