Cisplatin resistance driver claspin is a target for immunotherapy in urothelial carcinoma.
Cisplatin resistance
Claspin
Immunotherapy
Urothelial carcinoma
Journal
Cancer immunology, immunotherapy : CII
ISSN: 1432-0851
Titre abrégé: Cancer Immunol Immunother
Pays: Germany
ID NLM: 8605732
Informations de publication
Date de publication:
Jul 2023
Jul 2023
Historique:
received:
10
11
2022
accepted:
25
01
2023
medline:
15
6
2023
pubmed:
17
2
2023
entrez:
16
2
2023
Statut:
ppublish
Résumé
Bladder cancer is a major and fatal urological disease. Cisplatin is a key drug for the treatment of bladder cancer, especially in muscle-invasive cases. In most cases of bladder cancer, cisplatin is effective; however, resistance to cisplatin has a significant negative impact on prognosis. Thus, a treatment strategy for cisplatin-resistant bladder cancer is essential to improve the prognosis. In this study, we established a cisplatin-resistant (CR) bladder cancer cell line using an urothelial carcinoma cell lines (UM-UC-3 and J82). We screened for potential targets in CR cells and found that claspin (CLSPN) was overexpressed. CLSPN mRNA knockdown revealed that CLSPN had a role in cisplatin resistance in CR cells. In our previous study, we identified human leukocyte antigen (HLA)-A*02:01-restricted CLSPN peptide by HLA ligandome analysis. Thus, we generated a CLSPN peptide-specific cytotoxic T lymphocyte clone that recognized CR cells at a higher level than wild-type UM-UC-3 cells. These findings indicate that CLSPN is a driver of cisplatin resistance and CLSPN peptide-specific immunotherapy may be effective for cisplatin-resistant cases.
Identifiants
pubmed: 36795123
doi: 10.1007/s00262-023-03388-5
pii: 10.1007/s00262-023-03388-5
doi:
Substances chimiques
Cisplatin
Q20Q21Q62J
CLSPN protein, human
0
Adaptor Proteins, Signal Transducing
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2057-2065Subventions
Organisme : Japan Science and Technology Agency
ID : JPMJCR15G3
Organisme : Japan Agency for Medical Research and Development
ID : 20cm0106352h0002
Organisme : Japan Agency for Medical Research and Development
ID : 22ama221317h0001
Organisme : Japan Agency for Medical Research and Development
ID : 16770510
Organisme : Japan Society for the Promotion of Science
ID : 20H03460
Organisme : Japan Society for the Promotion of Science
ID : 17H01540
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Saginala K, Barsouk A, Aluru JS et al (2020) Epidemiology of bladder cancer. Med Sci. https://doi.org/10.3390/medsci8010015
doi: 10.3390/medsci8010015
Sung H, Ferlay J, Siegel RL et al (2021) Global cancer statistics 2020: globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249
doi: 10.3322/caac.21660
pubmed: 33538338
Patel VG, Oh WK, Galsky MD (2020) Treatment of muscle-invasive and advanced bladder cancer in 2020. CA Cancer J Clin 70:404–423
doi: 10.3322/caac.21631
pubmed: 32767764
Berdik C (2017) Unlocking bladder cancer. Nature 551:S34–S35
doi: 10.1038/551S34a
pubmed: 29117159
Guallar-Garrido S, Julián E (2020) Bacillus calmette-guérin (BCG) therapy for bladder cancer: an update. Immunotargets Ther 9:1–11
doi: 10.2147/ITT.S202006
pubmed: 32104666
pmcid: 7025668
Bellmunt J, de Wit R, Vaughn DJ et al (2017) Pembrolizumab as second-line therapy for advanced urothelial carcinoma. N Engl J Med 376:1015–1026
doi: 10.1056/NEJMoa1613683
pubmed: 28212060
pmcid: 5635424
Galsky MD, Arija JÁA, Bamias A et al (2020) Atezolizumab with or without chemotherapy in metastatic urothelial cancer (IMvigor130): a multicentre, randomised, placebo-controlled phase 3 trial. Lancet 395:1547–1557
doi: 10.1016/S0140-6736(20)30230-0
pubmed: 32416780
Powles T, Park SH, Voog E et al (2020) Avelumab maintenance therapy for advanced or metastatic urothelial carcinoma. N Engl J Med 383:1218–1230
doi: 10.1056/NEJMoa2002788
pubmed: 32945632
Bajorin DF, Witjes JA, Gschwend JE et al (2021) Adjuvant nivolumab versus placebo in muscle-invasive urothelial carcinoma. N Engl J Med 384:2102–2114
doi: 10.1056/NEJMoa2034442
pubmed: 34077643
pmcid: 8215888
Inoue R, Hirohashi Y, Kitamura H et al (2017) GRIK2 has a role in the maintenance of urothelial carcinoma stem-like cells, and its expression is associated with poorer prognosis. Oncotarget 8:28826–28839
doi: 10.18632/oncotarget.16259
pubmed: 28418868
pmcid: 5438695
Hu Y, Smyth GK (2009) ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 347:70–78
doi: 10.1016/j.jim.2009.06.008
pubmed: 19567251
Miyata H, Hirohashi Y, Yamada S et al (2022) GRIK2 is a target for bladder cancer stem-like cell-targeting immunotherapy. Cancer Immunol Immunother 71:795–806
doi: 10.1007/s00262-021-03025-z
pubmed: 34405274
Morita R, Hirohashi Y, Torigoe T et al (2016) Olfactory receptor family 7 subfamily c member 1 is a novel marker of colon cancer-initiating cells and is a potent target of immunotherapy. Clin Cancer Res 22:3298–3309
doi: 10.1158/1078-0432.CCR-15-1709
pubmed: 26861454
Haberle V, Forrest ARR, Hayashizaki Y et al (2015) CAGEr: precise TSS data retrieval and high-resolution promoterome mining for integrative analyses. Nucleic Acids Res 43:e51
doi: 10.1093/nar/gkv054
pubmed: 25653163
pmcid: 4417143
Frith MC, Valen E, Krogh A et al (2008) A code for transcription initiation in mammalian genomes. Genome Res 18:1–12
doi: 10.1101/gr.6831208
pubmed: 18032727
pmcid: 2134772
Yu G, Wang L-G, Han Y, He Q-Y (2012) Clusterprofiler: an R package for comparing biological themes among gene clusters. OMICS 16:284–287
doi: 10.1089/omi.2011.0118
pubmed: 22455463
pmcid: 3339379
Morita R, Hirohashi Y, Nakatsugawa M et al (2014) Production of multiple CTL epitopes from multiple tumor-associated antigens. Methods Mol Biol 1139:345–355
doi: 10.1007/978-1-4939-0345-0_28
pubmed: 24619692
Hirano N, Butler MO, Xia Z et al (2006) Engagement of CD83 ligand induces prolonged expansion of CD8+ T cells and preferential enrichment for antigen specificity. Blood 107:1528–1536
doi: 10.1182/blood-2005-05-2073
pubmed: 16239433
pmcid: 1895397
Matsuki M, Hirohashi Y, Nakatsugawa M et al (2022) Tumor-infiltrating CD8+ T cells recognize a heterogeneously expressed functional neoantigen in clear cell renal cell carcinoma. Cancer Immunol Immunother 71:905–918
doi: 10.1007/s00262-021-03048-6
pubmed: 34491407
Barr MP, Gray SG, Hoffmann AC et al (2013) Generation and characterisation of cisplatin-resistant non-small cell lung cancer cell lines displaying a stem-like signature. PLoS ONE 8:e54193
doi: 10.1371/journal.pone.0054193
pubmed: 23349823
pmcid: 3547914
Vallo S, Michaelis M, Rothweiler F et al (2015) Drug-resistant urothelial cancer cell lines display diverse sensitivity profiles to potential second-line therapeutics. Transl Oncol 8:210–216
doi: 10.1016/j.tranon.2015.04.002
pubmed: 26055179
pmcid: 4487788
Kobayashi G, Sentani K, Hattori T et al (2019) Clinicopathological significance of claspin overexpression and its association with spheroid formation in gastric cancer. Hum Pathol 84:8–17
doi: 10.1016/j.humpath.2018.09.001
pubmed: 30240769
Peschiaroli A, Dorrello NV, Guardavaccaro D et al (2006) SCFbetaTrCP-mediated degradation of claspin regulates recovery from the DNA replication checkpoint response. Mol Cell 23:319–329
doi: 10.1016/j.molcel.2006.06.013
pubmed: 16885022
Hirohashi Y, Torigoe T, Tsukahara T et al (2016) Immune responses to human cancer stem-like cells/cancer-initiating cells. Cancer Sci 107:12–17
doi: 10.1111/cas.12830
pubmed: 26440127
Prager BC, Xie Q, Bao S, Rich JN (2019) Cancer stem cells: the architects of the tumor ecosystem. Cell Stem Cell 24:41–53
doi: 10.1016/j.stem.2018.12.009
pubmed: 30609398
pmcid: 6350931
Park CY, Tseng D, Weissman IL (2009) Cancer stem cell-directed therapies: recent data from the laboratory and clinic. Mol Ther 17:219–230
doi: 10.1038/mt.2008.254
pubmed: 19066601
Ulsamer A, Martínez-Limón A, Bader S et al (2022) Regulation of claspin by the p38 stress-activated protein kinase protects cells from DNA damage. Cell Rep 40:111375
doi: 10.1016/j.celrep.2022.111375
pubmed: 36130506
Bianco JN, Bergoglio V, Lin Y-L et al (2019) Overexpression of claspin and timeless protects cancer cells from replication stress in a checkpoint-independent manner. Nat Commun 10:910
doi: 10.1038/s41467-019-08886-8
pubmed: 30796221
pmcid: 6385232
Kobayashi G, Sentani K, Babasaki T et al (2020) Claspin overexpression is associated with high-grade histology and poor prognosis in renal cell carcinoma. Cancer Sci 111:1020–1027
doi: 10.1111/cas.14299
pubmed: 31912588
pmcid: 7060467
Kobayashi G, Hayashi T, Sentani K et al (2021) Clinicopathological significance of claspin overexpression and its efficacy as a novel biomarker for the diagnosis of urothelial carcinoma. Virchows Arch. https://doi.org/10.1007/s00428-021-03239-7
doi: 10.1007/s00428-021-03239-7
pubmed: 34842980
Babasaki T, Sentani K, Sekino Y et al (2021) Overexpression of claspin promotes docetaxel resistance and is associated with prostate-specific antigen recurrence in prostate cancer. Cancer Med 10:5574–5588
doi: 10.1002/cam4.4113
pubmed: 34240817
pmcid: 8366092
Jia Y, Cheng X, Liang W et al (2022) CLSPN is a potential biomarker associated with poor prognosis in low-grade gliomas based on a multi-database analysis. Curr Res Transl Med 70:103345
doi: 10.1016/j.retram.2022.103345
pubmed: 35487167
Smits VAJ, Cabrera E, Freire R, Gillespie DA (2019) Claspin-checkpoint adaptor and DNA replication factor. FEBS J 286:441–455
doi: 10.1111/febs.14594
pubmed: 29931808
Kloetzel PM (2001) Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2:179–187
doi: 10.1038/35056572
pubmed: 11265247
Andersson HA, Barry MA (2004) Maximizing antigen targeting to the proteasome for gene-based vaccines. Mol Ther 10:432–446
doi: 10.1016/j.ymthe.2004.05.035
pubmed: 15336644
Park M-J, Kim E-K, Han J-Y et al (2010) Fusion of the human cytomegalovirus pp65 antigen with both ubiquitin and ornithine decarboxylase additively enhances antigen presentation to CD8(+) T cells in human dendritic cells. Hum Gene Ther 21:957–967
doi: 10.1089/hum.2009.216
pubmed: 20218861
Sasaya T, Kubo T, Murata K et al (2022) Cisplatin-induced HSF1-HSP90 axis enhances the expression of functional PD-L1 in oral squamous cell carcinoma. Cancer Med. https://doi.org/10.1002/cam4.5310
doi: 10.1002/cam4.5310
pubmed: 36200687
pmcid: 9972142