3D heterospecies spheroids of pancreatic stroma and cancer cells demonstrate key phenotypes of pancreatic ductal adenocarcinoma
Open accessAbstract
Pancreatic ductal adenocarcinoma (PDAC) is one of the most lethal malignancies, partly due to the dense desmoplasia and a lack of suitable model systems to study. In the present work, we developed a 3D heterospecies spheroid model to study the microenvironmental interactions between tumor cells and stellate cells which can also be employed to test therapeutic regimens. We set up monospheroids and heterospheroids made up from murine pancreatic stellate cells (mPSCs) and human PDAC cells (Panc1), which allowed for direct isolation of mRNA from a mixed cell population followed by an in silico separation of the RNA-seq reads. Global transcript level changes for cells in heterospheroids versus monospheroids were calculated, followed by gene set enrichment analysis and molecular subtype analysis. We observed an apparent shift of Panc1 from the classical to the squamous/basal-like phenotype upon co-culture with mPSCs. Moreover, mPSCs acquired a different cancer-associated fibroblast-related phenotype upon co-culture with Panc1. We analyzed the tumor cell-specific chemosensitivities towards gemcitabine, paclitaxel and SN38 and compared these to published pharmacotranscriptomic signatures. In conclusion, our heterospecies spheroid model reflected key aspects of PDAC and facilitated the study of intercellular interactions between tumor and stroma while additionally proving to be a good model for studying therapeutic responses.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Compared with 2D cell cultures, 3D spheroids more closely resemble PDAC tumours in structure and increased chemoresistance, providing a more accurate drug response.
“compared to 2D cell cultures, 3D spheroids more closely resemble PDAC tumours in terms of their structure and their increased chemoresistance, providing a more accurate drug response [38]”
From Pyrvinium Pamoate Alone and With Gemcitabine Exhibits Anti‐Pancreatic Cancer Activity in <scp>2D</scp> and <scp>3D</scp> Cell Culture Models (2024) · cites this paper as [38]
The Introduction says 3D cultures more closely resemble in vivo conditions than monolayers and that spheroids show increased chemoresistance. The Conclusion says the PDAC co-culture model recapitulates key tumour features and is suitable for drug testing. The paper does not establish that its drug responses are more accurate than those from 2D cultures. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
NIH Image to ImageJ: 25 years of image analysis
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012) · Nature Methods · doi:10.1038/nmeth.2089 · Cited by 64,638 · see citing works
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625 · see citing works
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
KEGG: Kyoto Encyclopedia of Genes and Genomes
Kanehisa, M. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.1.27 · Cited by 37,077 · see citing works
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232 · see citing works
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
Liao, Y., Smyth, G. K., & Shi, W. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt656 · Cited by 27,219 · see citing works
Siegel, R. L., Miller, K. D., & Jemal, A. (2020) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21590 · Cited by 20,444 · see citing works
The Molecular Signatures Database Hallmark Gene Set Collection
Liberzon, A., Birger, C., Thorvaldsdóttir, H., Ghandi, M., Mesirov, J. P., & Tamayo, P. (2015) · Cell Systems · doi:10.1016/j.cels.2015.12.004 · Cited by 13,807 · see citing works
Primer3—new capabilities and interfaces
Untergasser, A., Cutcutache, I., Kõressaar, T., Ye, J., Faircloth, B., Remm, M., & Rozen, S. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks596 · Cited by 9,165 · see citing works
FOLFIRINOX versus Gemcitabine for Metastatic Pancreatic Cancer
Conroy, T., Desseigne, F., Ychou, M., Bouché, O., Guimbaud, R., Bécouarn, Y., Adenis, A., Raoul, J.-L., Gourgou-Bourgade, S., de la Fouchardière, C., et al. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1011923 · Cited by 7,810 · see citing works
McCarthy, D. J., Chen, Y., & Smyth, G. K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks042 · Cited by 5,195 · see citing works
TCGAbiolinks: an R/Bioconductor package for integrative analysis of TCGA data
Colaprico, A., Silva, T. C., Olsen, C., Garofano, L., Cava, C., Garolini, D., Sabedot, T. S., Malta, T. M., Pagnotta, S. M., Castiglioni, I., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1507 · Cited by 4,137 · see citing works
A framework for advancing our understanding of cancer-associated fibroblasts
Sahai, E., Astsaturov, I., Cukierman, E., DeNardo, D. G., Egeblad, M., Evans, R. M., Fearon, D., Greten, F. R., Hingorani, S. R., Hunter, T., et al. (2020) · Nature Reviews Cancer · doi:10.1038/s41568-019-0238-1 · Cited by 3,863 · see citing works
Genomic analyses identify molecular subtypes of pancreatic cancer
Bailey, P., Chang, D. K., Nones, K., Johns, A. L., Patch, A.-M., Gingras, M.-C., Miller, D. K., Christ, A. N., Bruxner, T. J. C., Quinn, M. C., et al. (2016) · Nature · doi:10.1038/nature16965 · Cited by 3,621 · cited 2× · see citing works
“The DEGs of Panc1 were comared to the classical/basal-like signatures [5] , progenitor/squamous ignatures [6] and chemosensitivity signatures [36] using Fisher’s exact est.”
BackgroundMethodDistinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer
Öhlund, D., Handly-Santana, A., Biffi, G., Elyada, E., Almeida, A. S., Ponz-Sarvise, M., Corbo, V., Oni, T. E., Hearn, S. A., Lee, E. J., et al. (2017) · Journal of Experimental Medicine · doi:10.1084/jem.20162024 · Cited by 2,590 · see citing works
Elyada, E., Bolisetty, M., Laise, P., Flynn, W. F., Courtois, E. T., Burkhart, R. A., Teinor, J. A., Belleau, P., Biffi, G., Lucito, M. S., et al. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-0094 · Cited by 2,241 · see citing works
Moffitt, R. A., Marayati, R., Flate, E. L., Volmar, K. E., Loeza, S. G. H., Hoadley, K. A., Rashid, N. U., Williams, L. A., Eaton, S. C., Chung, A. H., et al. (2015) · Nature Genetics · doi:10.1038/ng.3398 · Cited by 2,194 · see citing works
Stromal Elements Act to Restrain, Rather Than Support, Pancreatic Ductal Adenocarcinoma
Rhim, A. D., Oberstein, P. E., Thomas, D. H., Mirek, E. T., Palermo, C. F., Sastra, S. A., Dekleva, E. N., Saunders, T., Becerra, C. P., Tattersall, I. W., et al. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.04.021 · Cited by 2,085 · see citing works
Integrated genomic characterization of pancreatic ductal adenocarcinoma
Raphael, B. J., Hruban, R. H., Aguirre, A. J., Moffitt, R. A., Yeh, J. J., Stewart, C., Robertson, A. G., Cherniack, A. D., Gupta, M., Getz, G., et al. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.07.007 · Cited by 2,019 · see citing works
Self-citationKleeff, J., Korc, M., Apte, M., La Vecchia, C., Johnson, C. D., Biankin, A. V., Neale, R. E., Tempero, M., Tuveson, D. A., Hruban, R. H., et al. (2016) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2016.22 · Cited by 1,982 · see citing works
Subtypes of pancreatic ductal adenocarcinoma and their differing responses to therapy
Collisson, E. A., Sadanandam, A., Olson, P., Gibb, W. J., Truitt, M., Gu, S., Cooc, J., Weinkle, J., Kim, G. E., Jakkula, L., et al. (2011) · Nature Medicine · doi:10.1038/nm.2344 · Cited by 1,967 · see citing works
Biffi, G., Oni, T. E., Spielman, B., Hao, Y., Elyada, E., Park, Y., Preall, J., & Tuveson, D. A. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-0710 · Cited by 1,360 · see citing works
Kolde, R. (2010) · doi:10.32614/cran.package.pheatmap · Cited by 1,267 · see citing works
Diversity and biology of cancer-associated fibroblasts
Biffi, G., & Tuveson, D. A. (2021) · Physiological Reviews · doi:10.1152/physrev.00048.2019 · Cited by 1,265 · see citing works
Spherical Cancer Models in Tumor Biology
Weiswald, L., Bellet, D. H., & Dangles‐Marie, V. (2015) · Neoplasia · doi:10.1016/j.neo.2014.12.004 · Cited by 1,138 · see citing works
Whole-exome sequencing of pancreatic cancer defines genetic diversity and therapeutic targets
Witkiewicz, A. K., McMillan, E. A., Balaji, U., Baek, G., Lin, W.-C., Mansour, J., Mollaee, M., Wagner, K.-U., Koduru, P., Yopp, A., et al. (2015) · Nature Communications · doi:10.1038/ncomms7744 · Cited by 1,115 · see citing works
Organoid Profiling Identifies Common Responders to Chemotherapy in Pancreatic Cancer
Tiriac, H., Belleau, P., Engle, D. D., Plenker, D., Deschênes, A., Somerville, T. D. D., Froeling, F. E. M., Burkhart, R. A., Denroche, R. E., Jang, G.-H., et al. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-0349 · Cited by 1,092 · see citing works
Single-cell sequencing reveals dissociation-induced gene expression in tissue subpopulations
van den Brink, S. C., Sage, F., Vértesy, Á., Spanjaard, B., Peterson-Maduro, J., Baron, C. S., Robin, C., & van Oudenaarden, A. (2017) · Nature Methods · doi:10.1038/nmeth.4437 · Cited by 1,072 · see citing works
Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors
Stylianopoulos, T., Martin, J. D., Chauhan, V. P., Jain, S. R., Diop-Frimpong, B., Bardeesy, N., Smith, B. L., Ferrone, C. R., Hornicek, F. J., Boucher, Y., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1213353109 · Cited by 943 · see citing works
Kamphorst, J. J., Nofal, M., Commisso, C., Hackett, S. R., Lu, W., Grabocka, E., Vander Heiden, M. G., Miller, G., Drebin, J. A., Bar-Sagi, D., et al. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-2211 · Cited by 893 · see citing works
Molecular subtypes of pancreatic cancer
Collisson, E. A., Bailey, P., Chang, D. K., & Biankin, A. V. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0109-y · Cited by 892 · see citing works
Secreted PCSK9 decreases the number of LDL receptors in hepatocytes and inlivers of parabiotic mice
Lagace, T. A., Curtis, D. E., Garuti, R., McNutt, M. C., Park, S. W., Prather, H. B., Anderson, N. N., Ho, Y. K., Hammer, R. E., & Horton, J. D. (2006) · Journal of Clinical Investigation · doi:10.1172/jci29383 · Cited by 681 · see citing works
Transcription phenotypes of pancreatic cancer are driven by genomic events during tumor evolution
Chan-Seng-Yue, M., Kim, J. C., Wilson, G. W., Ng, K., Figueroa, E. F., O’Kane, G. M., Connor, A. A., Denroche, R. E., Grant, R. C., McLeod, J., et al. (2020) · Nature Genetics · doi:10.1038/s41588-019-0566-9 · Cited by 669 · see citing works
Stromal Microenvironment Shapes the Intratumoral Architecture of Pancreatic Cancer
Ligorio, M., Sil, S., Malagon-Lopez, J., Nieman, L. T., Misale, S., Pilato, M. D., Ebright, R. Y., Karabacak, M., Kulkarni, A. S., Liu, A., et al. (2018) · Cell · doi:10.1016/j.cell.2019.05.012 · Cited by 526 · see citing works
Sonic Hedgehog Promotes Desmoplasia in Pancreatic Cancer
Bailey, J. M., Swanson, B. J., Hamada, T., Eggers, J. P., Singh, P. K., Caffrey, T. C., Ouellette, M. M., & Hollingsworth, M. A. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0291 · Cited by 520 · see citing works
Longati, P., Jia, X., Eimer, J., Wagman, A., Witt, M.-R., Rehnmark, S., Verbeke, C., Toftgård, R., Löhr, M., & Heuchel, R. L. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-95 · Cited by 394 · see citing works
Self-citationMicroenvironmental Determinants of Pancreatic Cancer
Heßmann, E., Buchholz, S., Demir, İ. E., Singh, S. K., Gress, T. M., Ellenrieder, V., & Neeße, A. (2020) · Physiological Reviews · doi:10.1152/physrev.00042.2019 · Cited by 329 · see citing works
Löhr, M. J., Schmidt, C., Ringel, J., Kluth, M., Müller, P., Nizze, H., & Jesnowski, R. (2001) · PubMed · Cited by 323 · see citing works
Self-citationSipos, B., Möser, S., Kalthoff, H., Török, V., Löhr, M. J., & Klöppel, G. (2003) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-003-0784-4 · Cited by 309 · see citing works
Self-citationVennDiagram: Generate High-Resolution Venn and Euler Plots
Chen, H. (2011) · doi:10.32614/cran.package.venndiagram · Cited by 291 · see citing works
Xenome—a tool for classifying reads from xenograft samples
Conway, T., Wazny, J., Bromage, A., Tymms, M., Sooraj, D., Williams, E. D., & Beresford-Smith, B. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts236 · Cited by 276 · see citing works
Ciccolini, J., Serdjebi, C., Peters, G. J., & Giovannetti, E. (2016) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-016-3003-0 · Cited by 243 · see citing works
TP63-mediated enhancer reprogramming drives the squamous subtype of pancreatic ductal adenocarcinoma
Somerville, T. D. D., Xu, Y., Miyabayashi, K., Tiriac, H., Cleary, C. R., Maia-Silva, D., Milazzo, J. P., Tuveson, D. A., & Vakoc, C. R. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.051 · Cited by 225 · see citing works
Modeling Pancreatic Cancer with Organoids
Baker, L. A., Tiriac, H., Clevers, H. C., & Tuveson, D. A. (2016) · Trends in cancer · doi:10.1016/j.trecan.2016.03.004 · Cited by 212 · see citing works
Heßmann, E., Patzak, M. S., Klein, L., Chen, N., Kari, V., Ramu, I., Bapiro, T. E., Frese, K. K., Gopinathan, A., Richards, F. M., et al. (2017) · Gut · doi:10.1136/gutjnl-2016-311954 · Cited by 198 · see citing works
Self-citationLee, J.-H., Kim, S.-K., Khawar, I. A., Jeong, S.-Y., Chung, S. H., & Kuh, H. (2018) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-017-0654-6 · Cited by 195 · see citing works
Kuen, J., Darowski, D., Kluge, T., & Majety, M. (2017) · PLOS ONE · doi:10.1371/journal.pone.0182039 · Cited by 192 · see citing works
Pancreatic Cancer Stroma: Friend or Foe?
Gore, J., & Korc, M. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.05.026 · Cited by 184 · see citing works
Desmoplasia and Chemoresistance in Pancreatic Cancer
Schober, M., Jesenofsky, R., Faissner, R., Weidenauer, C., Hagmann, W., Michl, P., Heuchel, R. L., Haas, S., & Löhr, M. J. (2014) · Cancers · doi:10.3390/cancers6042137 · Cited by 184 · see citing works
Self-citationABCG2 overexpression in colon cancer cells resistant to SN38 and in irinotecan‐treated metastases
Candeil, L., Gourdier, I., Peyron, D., Vezzio, N., Copois, V., Bibeau, F., Orsetti, B., Scheffer, G. L., Ychou, M., Khan, Q. A., et al. (2004) · International Journal of Cancer · doi:10.1002/ijc.20032 · Cited by 180 · see citing works
Alqahtani, F. Y., Aleanizy, F. S., Eltahir, E., Alkahtani, H. M., & AlQuadeib, B. T. (2019) · Profiles of drug substances, excipients, and related methodology · doi:10.1016/bs.podrm.2018.11.001 · Cited by 160 · see citing works
The plasticity of pancreatic cancer metabolism in tumor progression and therapeutic resistance
Biancur, D. E., & Kimmelman, A. C. (2018) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2018.04.011 · Cited by 151 · see citing works
Generation of an in vitro 3D PDAC stroma rich spheroid model
Ware, M. J., Keshishian, V., Law, J. J., Ho, J. C., Favela, C. A., Rees, P. C. T., Smith, B., Sayeeduddin, M., Hwang, R. F., Rajapakshe, K., et al. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.08.041 · Cited by 146 · see citing works
Lee, J. J., Bernard, V., Semaan, A., Monberg, M. E., Huang, J., Stephens, B. M., Lin, D., Rajapakshe, K. I., Weston, B. R., Bhutani, M. S., et al. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-3925 · Cited by 128 · see citing works
3D approaches to model the tumor microenvironment of pancreatic cancer
Bort, E. T., Kieler, M., Sharma, S., Candido, J. B., & Loessner, D. (2020) · Theranostics · doi:10.7150/thno.42441 · Cited by 117 · see citing works
Prognostic and predictive factors in pancreatic cancer
Dell’Aquila, E., Fulgenzi, C. A. M., Minelli, A., Citarella, F., Stellato, M., Pantano, F., Russano, M., Cursano, M. C., Napolitano, A., Zeppola, T., et al. (2020) · Oncotarget · doi:10.18632/oncotarget.27518 · Cited by 96 · see citing works
Squamous trans-differentiation of pancreatic cancer cells promotes stromal inflammation
Somerville, T. D. D., Biffi, G., Daßler‐Plenker, J., Hur, S. K., He, X., Vance, K. E., Miyabayashi, K., Xu, Y., Maia-Silva, D., Klingbeil, O., et al. (2020) · eLife · doi:10.7554/elife.53381 · Cited by 85 · see citing works
Sun, J., Li, N., Oh, K., Dutta, B., Vayttaden, S. J., Lin, B., Ebert, T. S., Nardo, D. D., Davis, J., Bagirzadeh, R., et al. (2016) · Science Signaling · doi:10.1126/scisignal.aab2191 · Cited by 82 · see citing works
Experimental models of pancreatic cancer desmoplasia
Suklabaidya, S., Dash, P., Das, B., Suresh, V., Sasmal, P. K., & Senapati, S. (2017) · Laboratory Investigation · doi:10.1038/labinvest.2017.127 · Cited by 65 · see citing works
A novel pancreatic tumour and stellate cell 3D co-culture spheroid model
Norberg, K. J., Liu, X., Moro, C. F., Strell, C., Nania, S., Blümel, M., Balboni, A., Bozóky, B., Heuchel, R. L., & Löhr, M. J. (2020) · BMC Cancer · doi:10.1186/s12885-020-06867-5 · Cited by 57 · see citing works
Self-citationGong, J., Sachdev, E., Robbins, L., Lin, E. M., Hendifar, A. E., & Mita, M. M. (2017) · Oncology Letters · doi:10.3892/ol.2017.5572 · Cited by 55 · see citing works
Pancreatic Stellate Cell Models for Transcriptional Studies of Desmoplasia-Associated Genes
Mathison, A., Liebl, A., Bharucha, J., Mukhopadhyay, D., Lomberk, G. A., Shah, V. H., & Urrutia, R. A. (2010) · Pancreatology · doi:10.1159/000320540 · Cited by 51 · see citing works
Molecular characterization of irinotecan (SN-38) resistant human breast cancer cell lines
Jandu, H., Aluzaite, K., Fogh, L., Thrane, S. W., Noer, J. B., Proszek, J., Nguyen, K., Hansen, S., Damsgaard, B., Nielsen, S. L., et al. (2016) · BMC Cancer · doi:10.1186/s12885-016-2071-1 · Cited by 44 · see citing works
Assessment of the stromal contribution to Sonic Hedgehog‐dependent pancreatic adenocarcinoma
Damhofer, H., Medema, J. P., Veenstra, V. L., Badea, L., Popescu, I., Roelink, H., & Bijlsma, M. F. (2013) · Molecular Oncology · doi:10.1016/j.molonc.2013.08.004 · Cited by 42 · see citing works
Pancreatic cancer should be treated as a medical emergency
Löhr, M. J. (2014) · BMJ · doi:10.1136/bmj.g5261 · Cited by 31 · see citing works
Self-citationUpcoming Revolutionary Paths in Preclinical Modeling of Pancreatic Adenocarcinoma
Swayden, M., Soubeyran, P., & Iovanna, J. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2019.01443 · Cited by 25 · see citing works
Arvidsson, G., Henriksson, J., Sander, B., & Wright, A. P. H. (2018) · Haematologica · doi:10.3324/haematol.2017.182048 · Cited by 13 · see citing works
Self-citation
Flagged first, then by citations
1 of the 68 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- [59]F.Y. Alqahtani, F.S. Aleanizy, E. El Tahir, H.M. Alkahtani, B.T. AlQuadeib, Chapter Three - Paclitaxel, Vol. 44. Brittain HG (ed). Academic Press, 2019, pp. 205-238. 31029218
Cited by
Sorted by citations
Overcoming therapy resistance in pancreatic cancer: New insights and future directions
Espona‐Fiedler, M., Patthey, C., Lindblad, S., Sarró, I., & Öhlund, D. (2024) · Biochemical Pharmacology · doi:10.1016/j.bcp.2024.116492 · Cited by 59 · see citing works
Pre-clinical Models of Metastasis in Pancreatic Cancer
Miquel, M., Zhang, S., & Pilarsky, C. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.748631 · Cited by 53 · see citing works
Pancreatic Ductal Adenocarcinoma: Preclinical in vitro and ex vivo Models
Gündel, B., Liu, X., Löhr, M. J., & Heuchel, R. L. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.741162 · Cited by 35 · see citing works
Self-citationResponsive Nanomaterial Delivery Systems for Pancreatic Cancer Management
Elsherbeny, A., Bayraktutan, H., Öz, U. C., Moloney, C., Ashworth, J., Grabowska, A. M., & Alexander, C. (2023) · Advanced Therapeutics · doi:10.1002/adtp.202300330 · Cited by 25 · see citing works
Deipenbrock, A., Wilmes, B. E., Sommermann, T. G., Abdo, N., Moustakas, K., Raasch, M., Rennert, K., & Teusch, N. E. (2025) · Lab on a Chip · doi:10.1039/d4lc01016g · Cited by 20 · see citing works
Vitacolonna, M., Bruch, R., Schneider, R., Jabs, J., Hafner, M., Reischl, M., & Rudolf, R. (2024) · BMC Cancer · doi:10.1186/s12885-024-13329-9 · Cited by 15 · see citing works
A 3D Bio-Printed-Based Model for Pancreatic Ductal Adenocarcinoma
Godier, C., Baka, Z., Lamy, L., Gribova, V., Marchal, P., Lavall�e, P., Gaffet, É., Bezdetnaya, L., & Alem, H. (2024) · Diseases · doi:10.3390/diseases12090206 · Cited by 14 · see citing works
Gupta, P., Bermejo‐Rodríguez, C., Kocher, H. M., Pérez-Mancera, P. A., & Velliou, E. G. (2024) · Advanced Biology · doi:10.1002/adbi.202300580 · Cited by 12 · see citing works
Photodynamic Stromal Depletion in Pancreatic Ductal Adenocarcinoma
Lintern, N., Smith, A. M., Jayne, D. G., & Khaled, Y. S. (2023) · Cancers · doi:10.3390/cancers15164135 · Cited by 10 · see citing works
Bidan, N., Dunsmore, G., Ugrinic, M., Bied, M., Moreira, M., Deloménie, C., Ginhoux, F., Blériot, C., de la Fuente, M., & Mura, S. (2023) · Drug Delivery and Translational Research · doi:10.1007/s13346-023-01479-5 · Cited by 11 · see citing works
Mapping Tumor–Stroma–ECM Interactions in Spatially Advanced 3D Models of Pancreatic Cancer
Kataki, A.-D., Gupta, P., Cheema, U., Nisbet, A., Wang, Y., Kocher, H. M., Pérez-Mancera, P. A., & Velliou, E. G. (2025) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.5c02296 · Cited by 9 · see citing works
Nielsen, B. S., Madsen, N. H., Larsen, J., Skandorff, I., Gad, M., & Holmstrøm, K. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1386097 · Cited by 8 · see citing works
The importance of preclinical models for cholangiocarcinoma drug discovery
Krendl, F. J., Primavesi, F., Oberhuber, R., Neureiter, D., Ocker, M., Bekric, D., Kiesslich, T., & Mayr, C. (2025) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2025.2457637 · Cited by 7 · see citing works
Serala, K., Bai, J., & Prince, S. (2024) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.70222 · Cited by 6 · see citing works
Tajpara, P., Sobkowiak, M. J., Healy, K., Naud, S., Gündel, B., Halimi, A., Khan, Z. A., Gabarrini, G., Guyader, S. L., Imreh, G., et al. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1553034 · Cited by 6 · see citing works
Self-citationBozóky, B., Moro, C. F., Strell, C., Geyer, N., Heuchel, R. L., Löhr, M. J., Ernberg, I. T., Székely, L., Gerling, M., & Bozóky, B. (2021) · Neoplasia · doi:10.1016/j.neo.2021.11.007 · Cited by 6 · see citing works
Self-citationA promising breakthrough in pancreatic cancer research: The potential of spheroids as 3D models
Jamshidi, N., Jamshidi, N., Chahardehi, A. M., Shams, E., & Chaleshi, V. (2024) · Bioimpacts · doi:10.34172/bi.30241 · Cited by 4 · see citing works
Wu, Z., Zeng, B., Seah, D. H., Ng, I. Z. R., Ding, R. H., Zhang, T., Kalaichelvan, M., You, R., & Fong, E. L. S. (2025) · Advanced Materials · doi:10.1002/adma.202512252 · Cited by 4 · see citing works
High level of ANO1 promotes pancreatic cancer growth in concert with oncogenic KRAS
Zhang, L., Wang, H., Guo, J., Xu, H., Qian, Y., & Sun, M. (2023) · Molecular Biology Reports · doi:10.1007/s11033-023-08293-9 · Cited by 4 · see citing works
Growing Desmoplastic Three-Dimensional Pancreatic Cancer Spheroids from Co-Culture
Bahl, R., Mata, C. V., Neth, B., Meinzinger, L., Deppe, A. C., Jahnke, H., Blackwell, C., Durymanov, M. O., & Reineke, J. (2024) · Journal of Visualized Experiments · doi:10.3791/66625 · Cited by 4 · see citing works
Gündel, B., Liu, X., Pfützenreuter, A.-M., Engelsberger, V., Weiskirchen, R., Löhr, M. J., & Heuchel, R. L. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25179369 · Cited by 2 · see citing works
Self-citationImpact of pancreatic proenzymes on pancreatic ductal adenocarcinoma associated fibroblasts
Toledo, B., González-Titos, A., Hernández-Camarero, P., López‐Ruiz, E., Griñán‐Lisón, C., Giovannetti, E., Marchal, J. A., & Perán, M. (2025) · Scientific Reports · doi:10.1038/s41598-025-24863-2 · Cited by 1 · see citing works
Pyrvinium Pamoate Enhances the Anti-cancer Activities of Gemcitabine in Pancreatic CancerPreprint
Serala, K., Bai, J., & Prince, S. (2024) · Preprints.org · doi:10.20944/preprints202402.1726.v1
Gupta, P., Richardson, J., Wilkinson, M., Victorovich, K. O., Bakkalci, D., Cheema, U., Kocher, H. M., Pérez-Mancera, P. A., & Velliou, E. G. (2026) · Biomaterials Advances · doi:10.1016/j.bioadv.2026.214984
- Authors
- Liu, X., Gündel, B., Li, X., Liu, J., Wright, A., Löhr, M., Arvidsson, G., & Heuchel, R.
- Affiliations
- Karolinska Institutet (SE)
- Corresponding author
- Heuchel, Rainer
- ORCID
- Venue
- Translational Oncology
- Publisher
- Elsevier BV
- Published
- 2021-07
- Volume
- 14
- Issue
- 7
- Pages
- 101107
- ISSN
- 1936-5233 (ISSN-L)
- PMC
- PMC8111319
- OpenAlex
- W3157330003
- Cited by
- 24
- References
- 68
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 10 · 2023: 4 · 2021: 3
- FWCI
- 1.55
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Translational Oncology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- European Commission (861196, 256974)
- China Scholarship Council (201700260279)
- Cancerfonden (CAN2013/780, CAN2017/615, CAN2018/624)
- Vetenskapsrådet (131163, 111252, K2013-67 \u00D7 22322\u201301-3, 2018-05973)
- Topics
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Health Sciences › Medicine › Surgery › Pancreatitis Pathology and Treatment
- Keywords
- pancreatic ductal adenocarcinoma, pancreatic stellate cells, tumor microenvironment, 3D co-culture model, desmoplasia, cancer-associated fibroblasts, tumor stroma, PANC-1 cells, chemosensitivity, gemcitabine, SN-38, gene expression profiling
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
