Analysis of Gene Expression in 3D Spheroids Highlights a Survival Role for ASS1 in Mesothelioma
Open accessAbstract
To investigate the underlying causes of chemoresistance in malignant pleural mesothelioma, we have studied mesothelioma cell lines as 3D spheroids, which acquire increased chemoresistance compared to 2D monolayers. We asked whether the gene expression of 3D spheroids would reveal mechanisms of resistance. To address this, we measured gene expression of three mesothelioma cell lines, M28, REN and VAMT, grown as 2D monolayers and 3D spheroids. A total of 209 genes were differentially expressed in common by the three cell lines in 3D (138 upregulated and 71 downregulated), although a clear resistance pathway was not apparent. We then compared the list of 3D genes with two publicly available datasets of gene expression of 56 pleural mesotheliomas compared to normal tissues. Interestingly, only three genes were increased in both 3D spheroids and human tumors: argininosuccinate synthase 1 (ASS1), annexin A4 (ANXA4) and major vault protein (MVP); of these, ASS1 was the only consistently upregulated of the three genes by qRT-PCR. To measure ASS1 protein expression, we stained 2 sets of tissue microarrays (TMA): one with 88 pleural mesothelioma samples and the other with additional 88 pleural mesotheliomas paired with matched normal tissues. Of the 176 tumors represented on the two TMAs, ASS1 was expressed in 87 (50%; staining greater than 1 up to 3+). For the paired samples, ASS1 expression in mesothelioma was significantly greater than in the normal tissues. Reduction of ASS1 expression by siRNA significantly sensitized mesothelioma spheroids to the pro-apoptotic effects of bortezomib and of cisplatin plus pemetrexed. Although mesothelioma is considered by many to be an ASS1-deficient tumor, our results show that ASS1 is elevated at the mRNA and protein levels in mesothelioma 3D spheroids and in human pleural mesotheliomas. We also have uncovered a survival role for ASS1, which may be amenable to targeting to undermine mesothelioma multicellular resistance.
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Gene expression patterns in spheroids more closely resemble those found in solid tumors than in monolayer cultures.
“gene expression patterns in spheroids more closely resemble those found in solid tumors than in monolayer cultures [112,193,194].”
From Modeling Tumor Microenvironment Complexity In Vitro: Spheroids as Physiologically Relevant Tumor Models and Strategies for Their Analysis (2025) · cites this paper as [193]
The Results section (“ASS1, ANXA4 and MVP are elevated in both 3D spheroids and patients”; page not available) reports three genes elevated in both mesothelioma spheroids relative to monolayers and patient tumors relative to normal tissue. It does not establish that spheroids’ overall gene-expression patterns resemble solid tumors more closely than monolayer patterns do. (LLM, conf=0.84)
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Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Robust Locally Weighted Regression and Smoothing Scatterplots
Cleveland, W. S. (1979) · Journal of the American Statistical Association · doi:10.1080/01621459.1979.10481038 · Cited by 11,594 · see citing works
Mutation of the mouse klotho gene leads to a syndrome resembling ageing
Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997) · Nature · doi:10.1038/36285 · Cited by 3,837 · see citing works
Yang, Y., Dudoit, S., Luu, P., Lin, D., Peng, V., Ngai, J., & Speed, T. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.4.e15 · Cited by 3,722 · see citing works
Spheroid-based drug screen: Considerations and practical approach
Friedrich, J., Seidel, C., Ebner, R., & Kunz-Schughart, L. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.226 · Cited by 1,742 · see citing works
Arginine deprivation and argininosuccinate synthetase expression in the treatment of cancer
Delage, B., Fennell, D. A., Nicholson, L., McNeish, I., Lemoine, N. R., Crook, T., & Szlosarek, P. W. (2010) · International Journal of Cancer · doi:10.1002/ijc.25202 · Cited by 441 · see citing works
Self-citationDiversion of aspartate in ASS1-deficient tumours fosters de novo pyrimidine synthesis
Rabinovich, S., Adler, L., Yizhak, K., Sarver, A., Silberman, A., Agron, S., Stettner, N., Sun, Q., Brandis, A., Helbling, D., et al. (2015) · Nature · doi:10.1038/nature15529 · Cited by 382 · see citing works
Guo, G., Chmielecki, J., Goparaju, C. M. V., Heguy, A., Dolgalev, I., Carbone, M., Seepo, S., Meyerson, M. M., & Pass, H. I. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-1008 · Cited by 321 · see citing works
Incidence and distribution of argininosuccinate synthetase deficiency in human cancers
Dillon, B. J., Prieto, V. G., Curley, S. A., Ensor, M., Holtsberg, F. W., Bomalaski, J. S., & Clark, M. A. (2004) · Cancer · doi:10.1002/cncr.20057 · Cited by 317 · see citing works
López‐Ríos, F., Chuai, S., Flores, R. M., Shimizu, S., Ohno, T., Wakahara, K., Illei, P. B., Hussain, S., Krug, L. M., Zakowski, M. F., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3907 · Cited by 247 · see citing works
Gordon, G. J., Rockwell, G. N., Jensen, R. V., Rheinwald, J. G., Glickman, J. N., Aronson, J. P., Pottorf, B. J., Nitz, M. D., Richards, W. G., Sugarbaker, D. J., et al. (2005) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)62492-3 · Cited by 194 · see citing works
Self-citationLind, D. S. (2004) · Journal of Nutrition · doi:10.1093/jn/134.10.2837s · Cited by 186 · see citing works
Szlosarek, P. W., Klampatsa, A., Pallaska, A., Sheaff, M. T., Smith, P., Crook, T., Grimshaw, M. J., Steele, J. P. C., Rudd, R., Balkwill, F. R., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1101 · Cited by 181 · see citing works
Self-citationSpotted Long Oligonucleotide Arrays for Human Gene Expression AnalysisPreprint
Barczak, A. J., Rodriguez, M. W., Hanspers, K., Koth, L. L., Tai, Y. C., Bolstad, B. M., Speed, T. P., & Erle, D. J. (2003) · Genome Research · doi:10.1101/gr.1048803 · Cited by 179 · see citing works
Using Gene Expression Ratios to Predict Outcome Among Patients With Mesothelioma
Gordon, G. J., Jensen, R. V., Hsiao, L., Gullans, S. R., Blumenstock, J. E., Richards, W. G., Jaklitsch, M. T., Sugarbaker, D. J., & Bueno, R. (2003) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/95.8.598 · Cited by 177 · see citing works
Self-citationErnst, A., Hofmann, S., Ahmadi, R., Becker, N., Korshunov, A., Engel, F., Hartmann, C. J., Felsberg, J., Sabel, M., Peterziel, H., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-0695 · Cited by 171 · see citing works
Syed, N., Langer, J., Janczar, K., Singh, P., Nigro, C. L., Lattanzio, L., Coley, H. M., Hatzimichael, E. C., Bomalaski, J. S., Szlosarek, P. W., et al. (2013) · Cell Death and Disease · doi:10.1038/cddis.2012.197 · Cited by 167 · see citing works
Huang, H.-Y., Wu, W.-R., Wang, Y.-H., Wang, J., Fang, F.-M., Tsai, J.-W., Li, S.-H., Hung, H.-C., Yu, S.-C., Lan, J., et al. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-2641 · Cited by 154 · see citing works
p53 and Kirsten-ras mutations in human mesothelioma cell lines.
Metcalf, R. A., Welsh, J. A., Bennett, W. P., Seddon, M. B., Lehman, T. A., Pelin, K., Linnainmaa, K., Tammilehto, L., Mattson, K. V., & Gerwin, B. I. (1992) · PubMed · Cited by 151 · see citing works
Barbone, D., Yang, T., Morgan, J. R., Gaudino, G., & Broaddus, V. C. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m709698200 · Cited by 148 · see citing works
Self-citationDelage, B., Luong, P., Maharaj, L., Ó’Riain, C., Syed, N., Crook, T., Hatzimichael, E. C., Papoudou‐Bai, A., Mitchell, T. J., Whittaker, S. J., et al. (2012) · Cell Death and Disease · doi:10.1038/cddis.2012.83 · Cited by 144 · see citing works
Gene expression profiling of malignant mesothelioma.
Singhal, S. K., Wiewrodt, R. G., Malden, L. D., Amin, K. M., Matzie, K. A., Friedberg, J. S., Kucharczuk, J. C., Litzky, L. A., Johnson, S. W., Kaiser, L. R., et al. (2003) · PubMed · Cited by 134 · see citing works
Nicholson, L. J., Smith, P. R., Hiller, L., Szlosarek, P. W., Kimberley, C., Sehouli, J., Koensgen, D., Mustea, A., Schmid, P., & Crook, T. (2009) · International Journal of Cancer · doi:10.1002/ijc.24546 · Cited by 133 · see citing works
Successful adenovirus-mediated gene transfer in an in vivo model of human malignant mesothelioma
Smythe, W. R., Kaiser, L. R., Hwang, H. C., Amin, K. M., Pilewski, J. M., Eck, S., Wilson, J. M., & Albelda, S. Μ. (1994) · The Annals of Thoracic Surgery · doi:10.1016/0003-4975(94)90090-6 · Cited by 131 · see citing works
Nonrandom chromosome alterations in human malignant mesothelioma.
Popescu, N. C., Chahinian, A. P., & DiPaolo, J. A. (1988) · PubMed · Cited by 105 · see citing works
Harasawa, R., Mizusawa, H., Nozawa, K., Nakagawa, T., Asada, K., & Kato, I. (1993) · Research in Microbiology · doi:10.1016/0923-2508(93)90057-9 · Cited by 101 · see citing works
Resistance of pleural mesothelioma cell lines to apoptosis: relation to expression of Bcl-2 and Bax
Narasimhan, S. R., Yang, L., Gerwin, B. I., & Broaddus, V. C. (1998) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1998.275.1.l165 · Cited by 91 · see citing works
Self-citationCrispi, S., Calogero, R., Santini, M., Mellone, P., Vincenzi, B., Citro, G., Vicidomini, G., Fasano, S., Meccariello, R., Cobellis, G., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007016 · Cited by 90 · see citing works
SV40-Dependent AKT Activity Drives Mesothelial Cell Transformation after Asbestos Exposure
Cacciotti, P., Barbone, D., Porta, C., Altomare, D. A., Testa, J. R., Mutti, L., & Gaudino, G. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0127 · Cited by 90 · see citing works
Self-citationPathogenesis of malignant ascites formation: initiating events that lead to fluid accumulation.
Nagy, J. A., Herzberg, K. T., Dvorak, J. M., & Dvorak, H. F. (1993) · PubMed · Cited by 90 · see citing works
Four-Gene Expression Ratio Test for Survival in Patients Undergoing Surgery for Mesothelioma
Gordon, G. J., Dong, L., Yeap, B. Y., Richards, W. G., Glickman, J. N., Edenfield, H., Mani, M., Colquitt, R. B., Maulik, G., Oss, B. V., et al. (2009) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djp061 · Cited by 89 · see citing works
Self-citationFennell, D. A., & Rudd, R. (2004) · The Lancet Oncology · doi:10.1016/s1470-2045(04)01492-5 · Cited by 78 · see citing works
Self-citationValidation of Genomics-Based Prognostic Tests in Malignant Pleural Mesothelioma
Gordon, G. J., Rockwell, G. N., Godfrey, P. A., Jensen, R. V., Glickman, J. N., Yeap, B. Y., Richards, W. G., Sugarbaker, D. J., & Bueno, R. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-2181 · Cited by 78 · see citing works
Self-citationSakai, Y., Yamagami, S., & Nakazawa, K. (2009) · Cells Tissues Organs · doi:10.1159/000272316 · Cited by 74 · see citing works
Szlosarek, P. W., Luong, P., Phillips, M. M., Baccarini, M., Ellis, S. M., Szyszko, T. A., Sheaff, M. T., & Avril, N. E. (2013) · Journal of Clinical Oncology · doi:10.1200/jco.2012.42.1784 · Cited by 74 · see citing works
Kim, H., Phung, Y., & Ho, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039556 · Cited by 68 · see citing works
Melaiu, O., Cristaudo, A., Melissari, E., Russo, M. D., Bonotti, A., Bruno, R., Foddis, R., Gemignani, F., Pellegrini, S., & Landi, S. (2011) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2011.12.003 · Cited by 60 · see citing works
Shan, Y., Hsu, H., Lai, M.-D., Yen, M., Chen, W.-C., Fang, J.-H., Weng, T., & Chen, Y. (2015) · Scientific Reports · doi:10.1038/srep09783 · Cited by 58 · see citing works
Broaddus, V. C., Dansen, T. B., Abayasiriwardana, K. S., Wilson, S. M., Finch, A. J., Swigart, L. B., Hunt, A. E., & Evan, G. I. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408190200 · Cited by 57 · see citing works
Self-citationThe Bcl-2 repertoire of mesothelioma spheroids underlies acquired apoptotic multicellular resistance
Barbone, D., Ryan, J. A., Kolhatkar, N. S., Chacko, A., Jablons, D. M., Sugarbaker, D. J., Bueno, R., Letai, A. G., Coussens, L. M., Fennell, D. A., et al. (2011) · Cell Death and Disease · doi:10.1038/cddis.2011.58 · Cited by 51 · see citing works
Self-citationExpression status of candidate genes in mesothelioma tissues and cell lines
Melaiu, O., Melissari, E., Mutti, L., Bracci, E., Santi, C. D., Iofrida, C., Russo, M. D., Cristaudo, A., Bonotti, A., Cipollini, M., et al. (2014) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2014.11.002 · Cited by 38 · see citing works
CaSm (LSm-1) Overexpression in Lung Cancer and Mesothelioma Is Required for Transformed Phenotypes
Watson, P. M., Miller, S. W., Fraig, M., Cole, D. J., Watson, D. K., & Boylan, A. M. (2008) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2007-0205oc · Cited by 38 · see citing works
Pinton, G., Manente, A. G., Angeli, G., Mutti, L., & Moro, L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036856 · Cited by 37 · see citing works
Barbone, D., Cheung, P., Battula, S. K., Busacca, S., Gray, S. G., Longley, D. B., Bueno, R., Sugarbaker, D. J., Fennell, D. A., & Broaddus, V. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052753 · Cited by 36 · see citing works
Self-citationMalignant pleural mesothelioma cells resist anoikis as quiescent pluricellular aggregates
Daubriac, J., Fleury‐Feith, J., Kheuang, L., Galipon, J., Saint-Albin, A., Renier, A., Giovannini, M., Galateau-Sallé, F., & Jaurand, M. (2009) · Cell Death and Differentiation · doi:10.1038/cdd.2009.32 · Cited by 35 · see citing works
Rienzo, A. D., Dong, L., Yeap, B. Y., Jensen, R. V., Richards, W. G., Gordon, G. J., Sugarbaker, D. J., & Bueno, R. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-0806 · Cited by 27 · see citing works
Self-citationBattisti, S., Valente, D., Albonici, L., Bei, R., Modesti, A., & Palumbo, C. (2012) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2011-0195oc · Cited by 22 · see citing works
Combination of arginine deprivation with TRAIL treatment as a targeted-therapy for mesothelioma.
Wangpaichitr, M., Wu, C., Bigford, G. E., Theodoropoulos, G. E., You, M., Li, Y. Y., Varona-Santos, J., Feun, L. G., Nguyen, D. M., & Savaraj, N. (2014) · PubMed · Cited by 17 · see citing works
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Fang, Y., & Eglen, R. M. (2017) · SLAS Discovery · doi:10.1177/1087057117696795 · Cited by 849 · see citing works
Zoetemelk, M., Rausch, M., Colin, D., Dormond, O., & Nowak-Sliwinska, P. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-42836-0 · Cited by 149 · see citing works
Decarli, M. C., do Amaral, R. L. F., dos Santos, D. P., Tofani, L. B., Katayama, E. T., Rezende, R. A., da Silva, J. V. L., Swiech, K., Suazo, C. A. T., Mota, C., et al. (2021) · Biofabrication · doi:10.1088/1758-5090/abe6f2 · Cited by 132 · see citing works
Anticancer drug discovery using multicellular tumor spheroid models
Zanoni, M., Pignatta, S., Arienti, C., Bonafè, M., & Tesei, A. (2019) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2019.1570129 · Cited by 109 · see citing works
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Tevis, K. M., Colson, Y. L., & Grinstaff, M. W. (2017) · Advanced Biosystems · doi:10.1002/adbi.201700083 · Cited by 104 · see citing works
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Joseph, J. S., Malindisa, S. T., & Ntwasa, M. M. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.81552 · Cited by 101 · see citing works
Kim, S., Lee, M., Song, Y., Lee, S., Choi, I., Park, I.-S., Kim, J., Kim, J., Kim, K. M., & Seo, H. R. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-01912-y · Cited by 67 · see citing works
Shah, S., & D’Souza, G. G. M. (2025) · Cells · doi:10.3390/cells14100732 · Cited by 66 · see citing works
“It has been well established that gene expression patterns in spheroids more closely resemble those found in solid tumors than in monolayer cultures [112,193,194].”
Dietz, C., Infanger, M., Romswinkel, A., Strube, F., & Kraus, A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20143601 · Cited by 51 · see citing works
Applicability of tumor spheroids forin vitrochemosensitivity assays
Hamilton, G., & Rath, B. (2018) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1080/17425255.2019.1554055 · Cited by 50 · see citing works
Gangadaran, P., Oh, E. J., Rajendran, R. L., Oh, J. M., Kim, H. M., Kwak, S., Chung, H. Y., Lee, J., Ahn, B., & Hong, C. M. (2023) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2023.05.088 · Cited by 46 · see citing works
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Blanquart, C., Jaurand, M., & Jean, D. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00388 · Cited by 44 · see citing works
Turtoi, M., Anghelache, M., Bucătariu, S., Deleanu, M., Voicu, G., Safciuc, F., Mânduțeanu, I., Fundueanu, G., Simionescu, M., & Călin, M. (2021) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2021.06.174 · Cited by 39 · see citing works
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Shamseddin, M., Obacz, J., Garnett, M. J., Rintoul, R. C., Francies, H. E., & Marciniak, S. J. (2021) · Thorax · doi:10.1136/thoraxjnl-2020-216602 · Cited by 28 · see citing works
Bruno, R., Alì, G., Giannini, R., Proietti, A., Lucchi, M., Chella, A., Melfi, F. M. A., Mussi, A., & Fontanini, G. (2016) · Oncotarget · doi:10.18632/oncotarget.13174 · Cited by 27 · see citing works
Gendre, D. A., Ameti, E., Karenovicŝ, W., Perriraz, N., Triponez, F., & Serre‐Beinier, V. (2021) · Oncotarget · doi:10.18632/oncotarget.28134 · Cited by 24 · see citing works
Sato, Y., Elbadawy, M., Suzuki, K., Tsunedomi, R., Nagano, H., Ishihara, Y., Yamamoto, H., Azakami, D., Uchide, T., Nabeta, R., et al. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114651 · Cited by 22 · see citing works
Mukherjee, S., & Ray, S. K. (2021) · Recent Patents on Anti-Cancer Drug Discovery · doi:10.2174/1574892816666210728115605 · Cited by 18 · see citing works
Overexpressed genes in malignant pleural mesothelioma: implications in clinical management
Barone, E., Gemignani, F., & Landi, S. (2018) · Journal of Thoracic Disease · doi:10.21037/jtd.2017.10.158 · Cited by 18 · see citing works
Barnett, S. E., Kenyani, J., Tripari, M., Butt, Z., Grosman, R., Querques, F., Shaw, L., Silva, L. C., Goate, Z., Marciniak, S. J., et al. (2023) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-22-0635 · Cited by 17 · see citing works
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Dell’Anno, I., Barbarino, M., Barone, E., Giordano, A., Luzzi, L., Bottaro, M., Migliore, L., Agostini, S., Melani, A., Melaiu, O., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144856 · Cited by 16 · see citing works
Borah, A., & Kumar, D. S. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-823966-7.00003-7 · Cited by 15 · see citing works
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Olofsson, K., Carannante, V., Takai, M., Önfelt, B., & Wiklund, M. (2021) · Scientific Reports · doi:10.1038/s41598-021-96288-6 · Cited by 13 · see citing works
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Luna-Nophal, A., Díaz-Castillo, F., Izquierdo-Sánchez, V., Velázquez-Fernández, J. B., Orozco‐Morales, M., Lara‐Mejía, L., Bernáldez-Sarabia, J., Sánchez-Campos, N., Arrieta, O. G., Díaz‐Chávez, J., et al. (2025) · Marine Drugs · doi:10.3390/md23010032 · Cited by 3 · see citing works
3D cell subculturing pillar dish for pharmacogenetic analysis and high-throughput screening
Lee, S., Hwang, H. J., Song, Y. J., Lee, D., Ku, B., Sa, J. K., & Lee, D. W. (2023) · Materials Today Bio · doi:10.1016/j.mtbio.2023.100793 · Cited by 3 · see citing works
3D Models of Mesothelioma in the Study of Mechanisms of Cell Survival
Broaddus, V. C., Follo, C., & Barbone, D. (2017) · Current cancer research · doi:10.1007/978-3-319-53560-9_11 · Cited by 3 · see citing works
Self-citationBlanquart, C., & Scherpereel, A. (2026) · Thorax · doi:10.1136/thorax-2025-223284 · Cited by 1 · see citing works
Huh, H. (2019) · UWSpace (University of Waterloo) · Cited by 1 · see citing works
do Amaral, R. L. F. (2020) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.60.2020.tde-21092021-055958
Voloaca, O. M. (2022) · Sheffield Hallam University · doi:10.7190/shu-thesis-00479
Kim, S., Lee, M., Song, Y., Lee, S.-Y., Choi, I., Park, I.-S., Kim, J., Kim, J.-S., Kim, K. M., & Seo, H. R. (2021) · Figshare · doi:10.6084/m9.figshare.14398443
Kim, S., Lee, M., Song, Y., Lee, S.-Y., Choi, I., Park, I.-S., Kim, J., Kim, J.-S., Kim, K. M., & Seo, H. R. (2021) · Figshare · doi:10.6084/m9.figshare.14398446
Kim, S., Lee, M., Song, Y., Lee, S.-Y., Choi, I., Park, I.-S., Kim, J., Kim, J.-S., Kim, K. M., & Seo, H. R. (2021) · Figshare · doi:10.6084/m9.figshare.14398440
Kim, S., Lee, M., Song, Y., Lee, S.-Y., Choi, I., Park, I.-S., Kim, J., Kim, J.-S., Kim, K. M., & Seo, H. R. (2021) · Figshare · doi:10.6084/m9.figshare.14398449
Immunotherapy resistance and strategies in malignant pleural mesothelioma
Xia, W., Li, S., Zeng, Q., Zhang, Y., 赵娟芝, Tan, X., Ju, S., Zou, W., Chen, C., Li, C., et al. (2026) · Cancer Drug Resistance · doi:10.20517/cdr.2025.215
Goodarzi, S. (2021) · theses.fr (ABES) · doi:10.70675/b0a0d503z93b4z464bz93d6z36d6613fb371
Metabolic vulnerabilities in pleural mesothelioma
Plans-Marin, S., Muñoz‐Pinedo, C., & Nadal, E. (2026) · Oncogenesis · doi:10.1038/s41389-026-00625-1
Poole, K., Miron-Mendoza, M., & Petroll, W. M. (2026) · Bioengineering · doi:10.3390/bioengineering13080876
- Authors
- Barbone, D., Van Dam, L., Follo, C., Jithesh, P. V., Zhang, S.-D., Richards, W. G., Bueno, R., Fennell, D. A., & Broaddus, V. C.
- Affiliations
- San Francisco General Hospital (US)
- Sidra Medical and Research Center (QA)
- Brigham and Women's Hospital (US)
- University of Leicester (GB)
- Corresponding author
- Barbone, Dario
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2016-03-16
- Volume
- 11
- Issue
- 3
- Pages
- e0150044
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4794185
- OpenAlex
- W2313014613
- Cited by
- 48
- References
- 48
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 1 · 2023: 4 · 2022: 6 · 2021: 13 · 2020: 4 · 2019: 6 · 2018: 2 · 2017: 4 · 2016: 1
- FWCI
- 3.88
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Figshare (submittedVersion, cc-by)
- Leicester Research Archive (University of Leicester) (submittedVersion, cc-by)
- Ulster University Research Portal (Ulster University) (submittedVersion, other-oa)
- Funders
- Mesothelioma Applied Research Foundation
- Centre National de la Recherche Scientifique
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Occupational and environmental lung diseases
- Health Sciences › Medicine › Surgery › Intraperitoneal and Appendiceal Malignancies
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- malignant pleural mesothelioma, ASS1, chemoresistance, multicellular spheroids, gene expression profiling, cell survival, bortezomib, cisplatin, pemetrexed, siRNA knockdown, annexin A4, major vault protein, tumor microenvironment
- MeSH terms
- Major Vault Protein, Argininosuccinate Synthase, Cell Survival, Humans, Mesothelioma, Gene Expression Regulation, Enzymologic, Gene Expression Regulation, Neoplastic, Annexin A4, Spheroids, Cellular, Vault Ribonucleoprotein Particles, Cell Line, Tumor
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