Experimental microdissection enables functional harmonisation of pancreatic cancer subtypes
Open accessAbstract
Objective: Pancreatic ductal adenocarcinoma (PDA) has among the highest stromal fractions of any cancer and this has complicated attempts at expression-based molecular classification. The goal of this work is to profile purified samples of human PDA epithelium and stroma and examine their respective contributions to gene expression in bulk PDA samples. Design: We used laser capture microdissection (LCM) and RNA sequencing to profile the expression of 60 matched pairs of human PDA malignant epithelium and stroma samples. We then used these data to train a computational model that allowed us to infer tissue composition and generate virtual compartment-specific expression profiles from bulk gene expression cohorts. Results: Our analysis found significant variation in the tissue composition of pancreatic tumours from different public cohorts. Computational removal of stromal gene expression resulted in the reclassification of some tumours, reconciling functional differences between different cohorts. Furthermore, we established a novel classification signature from a total of 110 purified human PDA stroma samples, finding two groups that differ in the extracellular matrix-associated and immune-associated processes. Lastly, a systematic evaluation of cross-compartment subtypes spanning four patient cohorts indicated partial dependence between epithelial and stromal molecular subtypes. Conclusion: Our findings add clarity to the nature and number of molecular subtypes in PDA, expand our understanding of global transcriptional programmes in the stroma and harmonise the results of molecular subtyping efforts across independent cohorts.
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?
Mauer et al. found that isolated epithelial tissues supported the Moffitt classical or basal-like subtypes, with no evidence of Bailey ADEX or Collisson exocrine-like subtypes in epithelial-enriched tumor samples.
“Mauer et al., found isolated epithelial tissues supported the Moffitt “classical” or “basal-like” subtypes, while they found no evidence of the Bailey “ADEX” subtype or Collisson “exocrine-like” subtypes in epithelial enriched tumor samples132.”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [132]
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
Siegel, R. L., Miller, K. D., & Jemal, A. (2017) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21387 · Cited by 14,712 · see citing works
Core Signaling Pathways in Human Pancreatic Cancers Revealed by Global Genomic Analyses
Jones, S., Zhang, X., Parsons, D. W., Lin, J. C.-H., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Kamiyama, H., Jimeno, A., et al. (2008) · Science · doi:10.1126/science.1164368 · Cited by 3,969 · 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 · see citing works
Olive, K. P., Jacobetz, M. A., Davidson, C. J., Gopinathan, A., McIntyre, D., Honess, D., Madhu, B., Goldgraben, M. A., Caldwell, M. E., Allard, D., et al. (2009) · Science · doi:10.1126/science.1171362 · Cited by 3,170 · see citing works
Self-citationWhole genomes redefine the mutational landscape of pancreatic cancer
Initiative, A. P. C. G., Waddell, N., Pajic, M., Patch, A.-M., Chang, D. K., Kassahn, K. S., Bailey, P., Johns, A. L., Miller, D., Nones, K., et al. (2015) · Nature · doi:10.1038/nature14169 · Cited by 2,642 · see citing works
Provenzano, P. P., Cuevas, C., Chang, A. E., Goel, V. K., Von Hoff, D. D., & Hingorani, S. R. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.01.007 · Cited by 2,195 · 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
Self-citationPancreatic cancer genomes reveal aberrations in axon guidance pathway genes
Initiative, A. P. C. G., Biankin, A. V., Waddell, N., Kassahn, K. S., Gingras, M.-C., Muthuswamy, L. B., Johns, A. L., Miller, D. K., Wilson, P. J., Patch, A.-M., et al. (2012) · Nature · doi:10.1038/nature11547 · Cited by 2,058 · 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-citationSubtypes 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
Systematic pan-cancer analysis of tumour purity
Aran, D., Sirota, M., & Butte, A. J. (2015) · Nature Communications · doi:10.1038/ncomms9971 · Cited by 1,206 · see citing works
The Human Protein Atlas—a tool for pathology
Pontén, F., Jirström, K., & Uhlén, M. (2008) · The Journal of Pathology · doi:10.1002/path.2440 · Cited by 1,126 · see citing works
Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer
Jacobetz, M. A., Chan, D. S., Neesse, A., Bapiro, T. E., Cook, N., Frese, K. K., Feig, C., Nakagawa, T., Caldwell, M. E., Zecchini, H. I., et al. (2013) · Gut · doi:10.1136/gutjnl-2012-302529 · Cited by 1,120 · 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
Laklai, H., Miroshnikova, Y. A., Pickup, M. W., Collisson, E. A., Kim, G., Barrett, A., Hill, R. C., Lakins, J. N., Schlaepfer, D. D., Mouw, J. K., et al. (2016) · Nature Medicine · doi:10.1038/nm.4082 · Cited by 598 · see citing works
Stromal biology and therapy in pancreatic cancer: a changing paradigm
Neeße, A., Algül, H., Tuveson, D. A., & Gress, T. M. (2015) · Gut · doi:10.1136/gutjnl-2015-309304 · Cited by 562 · see citing works
Comprehensive comparative analysis of RNA sequencing methods for degraded or low input samples
Adiconis, X., Borges-Rivera, D., Satija, R., DeLuca, D. S., Busby, M., Berlin, A. M., Sivachenko, A., Thompson, D. A., Wysoker, A., Fennell, T., et al. (2013) · Europe PMC (PubMed Central) · doi:10.1038/nmeth.2483 · Cited by 508 · see citing works
Berger, A. C., García, M. L., Hoffman, J. P., Regine, W. F., Abrams, R. A., Safran, H. P., Konski, A. A., Benson, A. B., Macdonald, J. S., & Willett, C. G. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.18.6288 · Cited by 372 · see citing works
Hruban, R. H., Pitman, M. B., & Klimstra, D. S. (2007) · American Registry of PathologyWashington, DC eBooks · doi:10.55418/9781933477022 · Cited by 371 · see citing works
Pancreatic cancer: why is it so hard to treat?
Oberstein, P. E., & Olive, K. P. (2013) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x13478680 · Cited by 334 · see citing works
Self-citationYachida, S., White, C. M., Naito, Y., Zhong, Y., Brosnan, J. A., Macgregor-Das, A. M., Morgan, R. A., Saunders, T., Laheru, D. A., Herman, J. M., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-1215 · Cited by 280 · see citing works
Inflammatory networks and immune surveillance of pancreatic carcinoma
Vonderheide, R. H., & Bayne, L. J. (2013) · Current Opinion in Immunology · doi:10.1016/j.coi.2013.01.006 · Cited by 200 · see citing works
Nicolle, R., Blum, Y., Marisa, L., Loncle, C., Gayet, O., Moutardier, V., Turrini, O., Giovannini, M. F., Bian, B., Bigonnet, M., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.11.003 · Cited by 199 · see citing works
Frantz, V. (1959) · Medical Entomology and Zoology · Cited by 100 · see citing works
Shanker, S., Paulson, A., Edenberg, H. J., Peak, A., Perera, A. G., Alekseyev, Y. O., Beckloff, N., Bivens, N. J., DONNELLY, R. J., Gillaspy, A. F., et al. (2015) · Journal of Biomolecular Techniques JBT · doi:10.7171/jbt.15-2601-001 · Cited by 69 · see citing works
He, J., Maurer, H. C., Holmstrom, S. R., Su, T., Ahmed, A., Hibshoosh, H. H., Chabot, J. A., Oberstein, P. E., Sepulveda, A. R., Genkinger, J. M., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/288779 · Cited by 4 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Pancreatic cancer: Advances and challenges
Halbrook, C. J., Lyssiotis, C. A., Pasca di Magliano, M., & Maitra, A. (2023) · Cell · doi:10.1016/j.cell.2023.02.014 · Cited by 1,321 · 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
Cross-tissue organization of the fibroblast lineage
Buechler, M., Pradhan, R., Krishnamurty, A. T., Cox, C. B., Calviello, A. K., Wang, A. W., Yang, Y., Tam, L., Caothien, R., Roose-Girma, M., et al. (2021) · Nature · doi:10.1038/s41586-021-03549-5 · Cited by 941 · see citing works
Dominguez, C. X., Müller, S., Keerthivasan, S., Koeppen, H., Hung, J., Gierke, S., Breart, B., Foreman, O., Bainbridge, T. W., Castiglioni, A., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-0644 · Cited by 857 · see citing works
Proteogenomic characterization of pancreatic ductal adenocarcinoma
Cao, L., Huang, C., Cui Zhou, D., Hu, Y., Lih, T. M., Savage, S. R., Krug, K., Clark, D. J., Schnaubelt, M., Chen, L., et al. (2021) · Cell · doi:10.1016/j.cell.2021.08.023 · Cited by 578 · see citing works
Accurate and efficient detection of gene fusions from RNA sequencing data
Uhrig, S., Ellermann, J., Walther, T., Burkhardt, P., Fröhlich, M., Hutter, B., Toprak, U. H., Neumann, O., Stenzinger, A., Scholl, C., et al. (2021) · Genome Research · doi:10.1101/gr.257246.119 · Cited by 526 · see citing works
LRRC15(+) myofibroblasts dictate the stromal setpoint to suppress tumour immunity
Krishnamurty, A. T., Shyer, J. A., Thai, M., Gandham, V., Buechler, M. B., Yang, Y. A., Pradhan, R. N., Wang, A. W., Sanchez, P. L., Qu, Y., et al. (2022) · Nature · doi:10.1038/s41586-022-05272-1 · Cited by 436 · see citing works
Spatially confined sub-tumor microenvironments in pancreatic cancer
Grünwald, B. T., Devisme, A., Andrieux, G., Vyas, F., Aliar, K., McCloskey, C. W., Macklin, A., Jang, G. H., Denroche, R., Romero, J. M., et al. (2021) · Cell · doi:10.1016/j.cell.2021.09.022 · Cited by 433 · see citing works
Wang, S., Zheng, Y., Yang, F., Zhu, L., Zhu, X.-Q., Wang, Z.-F., Wu, X.-L., Zhou, C.-H., Yan, J.-Y., Hu, B.-Y., et al. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00659-4 · Cited by 369 · see citing works
Microenvironmental 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
Zhou, D. C., Jayasinghe, R. G., Chen, S., Herndon, J. M., Iglesia, M. D., Navale, P., Wendl, M. C., Caravan, W., Sato, K., Storrs, E. P., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01157-1 · Cited by 282 · see citing works
Rashid, N. U., Peng, X. L., Jin, C., Moffitt, R. A., Volmar, K. E., Belt, B. A., Panni, R. Z., Nywening, T. M., Herrera, S. G., Moore, K. J., et al. (2019) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-1467 · Cited by 238 · see citing works
The TLR7/8 agonist R848 remodels tumor and host responses to promote survival in pancreatic cancer
Michaelis, K. A., Norgard, M. A., Zhu, X., Levasseur, P. R., Sivagnanam, S., Liudahl, S. M., Burfeind, K. G., Olson, B. G., Pelz, K. R., Ramos, D. M. A., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12657-w · Cited by 231 · see citing works
Self-citationTumour-selective activity of RAS-GTP inhibition in pancreatic cancer
Wasko, U. N., Jiang, J., Dalton, T. C., Curiel-Garcia, A., Edwards, A. C., Wang, Y., Lee, B., Orlen, M., Tian, S., Stalnecker, C. A., et al. (2024) · Nature · doi:10.1038/s41586-024-07379-z · Cited by 209 · see citing works
Self-citationZhu, Z., Achreja, A., Meurs, N., Animasahun, O., Owen, S., Mittal, A., Parikh, P., Lo, T.-W., Franco-Barraza, J., Shi, J., et al. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0226-5 · Cited by 204 · see citing works
Kemp, S. B., Carpenter, E. S., Steele, N. G., Donahue, K. L., Nwosu, Z. C., Pacheco, A., Velez-Delgado, A., Menjivar, R. E., Lima, F., The, S., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-3929 · Cited by 197 · see citing works
Targeting DNA Damage Response and Replication Stress in Pancreatic Cancer
Dreyer, S. B., Upstill‐Goddard, R., Paulus-Hock, V., Paris, C., Lampraki, E.-M., Dray, E. V., Serrels, B., Caligiuri, G., Rebus, S., Plenker, D., et al. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.09.043 · Cited by 163 · see citing works
Sharbeen, G., McCarroll, J. A., Akerman, A., Kopecky, C., Youkhana, J., Kokkinos, J., Holst, J., Boyer, C. A., Erkan, M., Goldstein, D., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-2496 · Cited by 135 · see citing works
Miyabayashi, K., Baker, L. A., Deschênes, A., Traub, B., Caligiuri, G., Plenker, D., Alagesan, B., Belleau, P., Li, S., Kendall, J., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-0133 · Cited by 125 · see citing works
Defining the KRAS- and ERK-dependent transcriptome in KRAS-mutant cancers
Klomp, J. A., Klomp, J. E., Stalnecker, C. A., Bryant, K. L., Edwards, A. C., Drizyte‐Miller, K., Hibshman, P. S., Diehl, J. N., Lee, Y. S., Morales, A. J., et al. (2024) · Science · doi:10.1126/science.adk0775 · Cited by 133 · see citing works
Espinet, E., Gu, Z., Imbusch, C. D., Giese, N. A., Büscher, M., Safavi, M., Weisenburger, S., Klein, C., Vogel, V., Falcone, M., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-1202 · Cited by 123 · see citing works
Cell of origin influences pancreatic cancer subtype
Flowers, B. M., Xu, H., Mulligan, A. S., Hanson, K. J., Seoane, J. A., Vogel, H., Curtis, C., Wood, L. D., & Attardi, L. D. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-0633 · Cited by 118 · see citing works
Tu, M., Klein, L., Espinet, E., Georgomanolis, T., Wegwitz, F., Li, X., Urbach, L., Danieli‐Mackay, A., Küffer, S., Bojarczuk, K., et al. (2021) · Nature Cancer · doi:10.1038/s43018-021-00258-w · Cited by 112 · see citing works
Poh, A. R., & Ernst, M. (2021) · Cancers · doi:10.3390/cancers13122860 · Cited by 106 · see citing works
Tian, J., Zhu, Y., Rao, M., Cai, Y., Lu, Z., Zou, D., Peng, X., Ying, P., Zhang, M., Niu, S., et al. (2020) · Gut · doi:10.1136/gutjnl-2019-320179 · Cited by 98 · see citing works
Matrix stiffness drives stromal autophagy and promotes formation of a protumorigenic niche
Hupfer, A., Brichkina, A. I., Koeniger, A., Keber, C. U., Denkert, C., Pfefferle, P. I., Helmprobst, F., Pagenstecher, A., Visekruna, A., & Lauth, M. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2105367118 · Cited by 93 · 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
Tuft Cells Inhibit Pancreatic Tumorigenesis in Mice by Producing Prostaglandin D2
DelGiorno, K. E., Chung, C., Vavinskaya, V., Maurer, H. C., Novak, S. W., Lytle, N. K., Ma, Z., Giraddi, R. R., Wang, D., Fang, L., et al. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.07.037 · Cited by 85 · see citing works
Self-citationCheung, P. F., Yang, J., Fang, R., Borgers, A., Krengel, K., Stoffel, A., Althoff, K., Yip, C. W., Siu, E. H.-L., Ng, L. W. C., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-27088-9 · Cited by 84 · see citing works
Coordinated single-cell tumor microenvironment dynamics reinforce pancreatic cancer subtype
Oh, K., Yoo, Y. J., Torre-Healy, L. A., Rao, M., Fassler, D., Wang, P., Caponegro, M. D., Gao, M., Kim, J., Sasson, A. R., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40895-6 · Cited by 83 · see citing works
Dijk, F., Veenstra, V. L., Soer, E. C., Dings, M. P. G., Zhao, L., Halfwerk, J. B. G., Hooijer, G. K. J., Damhofer, H., Marzano, M., Steins, A., et al. (2020) · Scientific Reports · doi:10.1038/s41598-019-56826-9 · Cited by 81 · see citing works
Martens, S., Lefesvre, P., Nicolle, R., Biankin, A. V., Puleo, F., Laethem, J. V., & Rooman, I. (2019) · Annals of Oncology · doi:10.1093/annonc/mdz181 · Cited by 78 · see citing works
Clinical Impact of Molecular Subtyping of Pancreatic Cancer
Zhou, X., Hu, K., Bailey, P. J., Springfeld, C., Roth, S., Kurilov, R., Brors, B., Gress, T. M., Buchholz, M., An, J., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.743908 · Cited by 78 · see citing works
Metastasis in Pancreatic Ductal Adenocarcinoma: Current Standing and Methodologies
Pereira, M. A., & Chio, I. I. C. (2019) · Genes · doi:10.3390/genes11010006 · Cited by 75 · see citing works
The m6A-Related mRNA Signature Predicts the Prognosis of Pancreatic Cancer Patients
Meng, Z., Yuan, Q., Zhao, J., Wang, B., Li, S., Offringa, R., Jin, X., & Wu, H. (2020) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2020.04.011 · Cited by 72 · see citing works
Boelaars, K., Rodríguez, E., Huinen, Z. R., Liu, C., Wang, D., Springer, B. O., Olesek, K., Kruijssen, L. J. W., van Ee, T., Lindijer, D., et al. (2024) · Communications Biology · doi:10.1038/s42003-024-06087-8 · Cited by 72 · see citing works
Alternative polyadenylation drives oncogenic gene expression in pancreatic ductal adenocarcinomaPreprint
Venkat, S., Tisdale, A. A., Schwarz, J. R., Alahmari, A. A., Maurer, H. C., Olive, K. P., Eng, K. H., & Feigin, M. E. (2020) · Genome Research · doi:10.1101/gr.257550.119 · Cited by 72 · see citing works
Self-citationMechanisms of PDAC subtype heterogeneity and therapy response
Espinet, E., Klein, L., Puré, E., & Singh, S. K. (2022) · Trends in cancer · doi:10.1016/j.trecan.2022.08.005 · Cited by 70 · see citing works
Microdissected pancreatic cancer proteomes reveal tumor heterogeneity and therapeutic targets
Large, T. Y. S. L., Mantini, G., Meijer, L. L., Pham, T. V., Funel, N., van Grieken, N. C. T., Kok, B., Knol, J. C., van Laarhoven, H. W. M., Piersma, S. R., et al. (2020) · JCI Insight · doi:10.1172/jci.insight.138290 · Cited by 62 · see citing works
Somerville, T. D. D., Xu, Y., Wu, X., Maia-Silva, D., Hur, S. K., de Almeida, L. M. N., Preall, J. B., Koo, P. K., & Vakoc, C. R. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1921484117 · Cited by 60 · see citing works
The vascular landscape of human cancer
Kahn, B., Lucas, A., Alur, R. G., Wengyn, M. D., Schwartz, G. W., Li, J., Sun, K., Maurer, H. C., Olive, K. P., Faryabi, R. B., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci136655 · Cited by 54 · see citing works
Self-citationHyeon, D. Y., Nam, D., Han, Y., Kim, D. K., Kim, G., Kim, D., Bae, J., Back, S., Mun, D., Madar, I. H., et al. (2022) · Nature Cancer · doi:10.1038/s43018-022-00479-7 · Cited by 54 · 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
Clinical functional proteomics of intercellular signalling in pancreatic cancer
Huang, P., Gao, W., Fu, C., Wang, M., Li, Y., Chu, B., He, A., Li, Y., Deng, X., Zhang, Y., et al. (2024) · Nature · doi:10.1038/s41586-024-08225-y · Cited by 51 · see citing works
Hosen, S. M. Z., Uddin, M. N., Xu, Z., Buckley, B. J., Perera, C. J., Pang, T., Mekapogu, A. R., Moni, M. A., Notta, F., Gallinger, S., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1060957 · Cited by 50 · see citing works
The Role of the Microbiome in Pancreatic Cancer
Miyabayashi, K., Ijichi, H., & Fujishiro, M. (2022) · Cancers · doi:10.3390/cancers14184479 · Cited by 45 · see citing works
Laser Capture Proteomics: spatial tissue molecular profiling from the bench to personalized medicine
Liotta, L. A., Pappalardo, P. A., Carpino, A., Haymond, A. N., Howard, M., Espina, V. A., Wulfkuhle, J., & Petricoin, E. F. (2021) · Expert Review of Proteomics · doi:10.1080/14789450.2021.1984886 · Cited by 42 · see citing works
Nicolle, R., Bachet, J., Harlé, A., Iovanna, J., Hammel, P. R., Rebours, V., Turpin, A., Abdelghani, M. B., Wei, A. C.-C., Mitry, E., et al. (2023) · Journal of Clinical Oncology · doi:10.1200/jco.22.02668 · Cited by 40 · see citing works
Molecular and Metabolic Subtypes Correspondence for Pancreatic Ductal Adenocarcinoma Classification
Espiau-Romera, P., Courtois, S., Parejo-Alonso, B., & Sancho, P. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9124128 · Cited by 38 · see citing works
Genomic Heterogeneity of Pancreatic Ductal Adenocarcinoma and Its Clinical Impact
Gutiérrez, M. L., Muñoz‐Bellvís, L., & Órfão, A. (2021) · Cancers · doi:10.3390/cancers13174451 · Cited by 38 · see citing works
Murphy, K. J., Chambers, C. R., Herrmann, D., Timpson, P., & Pereira, B. (2021) · Cancers · doi:10.3390/cancers13143481 · Cited by 38 · see citing works
Secretome of Stromal Cancer-Associated Fibroblasts (CAFs): Relevance in Cancer
Mishra, D., & Banerjee, D. (2023) · Cells · doi:10.3390/cells12040628 · Cited by 36 · see citing works
Combinatorial Gli activity directs immune infiltration and tumor growth in pancreatic cancer
Scales, M. K., Velez-Delgado, A., Steele, N. G., Schrader, H. E., Stabnick, A. M., Yan, W., Mercado-Soto, N. M., Nwosu, Z., Johnson, C. N., Zhang, Y.-Q., et al. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1010315 · Cited by 28 · see citing works
Self-citationSwietlik, J. J., Bärthel, S., Falcomatà, C., Fink, D., Sinha, A., Cheng, J., Ebner, S., Landgraf, P., Dieterich, D. C., Daub, H., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38171-8 · Cited by 36 · see citing works
Dissecting FGF Signalling to Target Cellular Crosstalk in Pancreatic Cancer
Carter, E. P., Coetzee, A. S., Bort, E. T., Wang, Q., Kocher, H. M., & Grose, R. P. (2021) · Cells · doi:10.3390/cells10040847 · Cited by 33 · see citing works
A mucus production programme promotes classical pancreatic ductal adenocarcinoma
Tonelli, C., Yordanov, G. N., Hao, Y., Deschênes, A., Hinds, J., Belleau, P., Klingbeil, O., Brosnan, E., Doshi, A., Park, Y., et al. (2024) · Gut · doi:10.1136/gutjnl-2023-329839 · Cited by 34 · see citing works
Samain, R., Brunel, A., Douché, T., Fanjul, M., Cassant‐Sourdy, S., Rochotte, J., Cros, J. F., Neuzillet, C., Raffenne, J., Duluc, C., et al. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.01.008 · Cited by 32 · see citing works
de Oliveira, G., Freire, P. P., Cury, S. S., de Moraes, D., Oliveira, J. S., Dal‐Pai‐Silva, M., Reis, P. P., & Carvalho, R. F. (2020) · Cancers · doi:10.3390/cancers12030716 · Cited by 32 · see citing works
Cellular metabolism in pancreatic cancer as a tool for prognosis and treatment (Review)
Zuzčák, M., & Trnka, J. (2022) · International Journal of Oncology · doi:10.3892/ijo.2022.5383 · Cited by 33 · see citing works
Gene Targeting in Disease Networks
Weighill, D. A., Guebila, M. B., Glass, K., Platig, J., Yeh, J. J., & Quackenbush, J. F. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.649942 · Cited by 30 · see citing works
Suurmeijer, J. A., Soer, E. C., Dings, M. P. G., Kim, Y., Strijker, M., Bonsing, B. A., Brosens, L. A. A., Busch, O. R., Groen, J. V., Halfwerk, J. B. G., et al. (2022) · British journal of surgery · doi:10.1093/bjs/znac272 · Cited by 30 · see citing works
Morphological Heterogeneity in Pancreatic Cancer Reflects Structural and Functional Divergence
Sántha, P., Lenggenhager, D. M., Finstadsveen, A. V., Dorg, L. T., Tøndel, K., Amrutkar, M., Gladhaug, I. P., & Verbeke, C. S. (2021) · Cancers · doi:10.3390/cancers13040895 · Cited by 30 · see citing works
Ramu, I., Buchholz, S. M., Patzak, M. S., Goetze, R. G., Singh, S. K., Richards, F. M., Jodrell, D. I., Sipos, B., Ströbel, P., Ellenrieder, V., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.09.024 · Cited by 29 · see citing works
GPCRs in pancreatic adenocarcinoma: Contributors to tumour biology and novel therapeutic targets
Sriram, K., Salmerón, C., Wiley, S. Z., & Insel, P. A. (2020) · British Journal of Pharmacology · doi:10.1111/bph.15028 · Cited by 29 · see citing works
Miyabayashi, K., Nakagawa, H., & Koike, K. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.682872 · Cited by 28 · see citing works
Pancreatic Organoids for Regenerative Medicine and Cancer Research
Casamitjana, J., Espinet, E., & Rovira, M. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.886153 · Cited by 28 · see citing works
ROR2 Regulates Cellular Plasticity in Pancreatic Neoplasia and Adenocarcinoma
Benitz, S., Steep, A., Nasser, M. M., Preall, J. B., Mahajan, U. M., McQuithey, H., Loveless, I. M., Davis, E. T., Wen, H.-J., Long, D. W., et al. (2024) · Cancer Discovery · doi:10.1158/2159-8290.cd-24-0137 · Cited by 27 · see citing works
Birnbaum, D. J., Begg, S. K. S., Finetti, P., Vanderburg, C. R., Kulkarni, A. S., Neyaz, A., Hank, T. P., Tai, E. C., Deshpande, V., Bertucci, F., et al. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-1039 · Cited by 27 · see citing works
A Tumor Microenvironment Model of Pancreatic Cancer to Elucidate Responses toward Immunotherapy
Kast, V., Nadernezhad, A., Pette, D., Gabrielyan, A., Fusenig, M., Honselmann, K. C., Stange, D. E., Werner, C., & Loessner, D. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202201907 · Cited by 25 · see citing works
Torre-Healy, L. A., Kawalerski, R. R., Oh, K., Chrastecka, L., Peng, X. L., Aguirre, A. J., Rashid, N. U., Yeh, J. J., & Moffitt, R. A. (2023) · Communications Biology · doi:10.1038/s42003-023-04461-6 · Cited by 25 · see citing works
Pervasiveness of HLA allele-specific expression loss across tumor types
Filip, I., Wang, A., Kravets, O., Orenbuch, R., Zhao, J., Perea-Chamblee, T. E., Manji, G. A., de Maturana, E. L., Malats, N., Olive, K. P., et al. (2023) · Genome Medicine · doi:10.1186/s13073-023-01154-x · Cited by 24 · see citing works
Self-citationJiang, Z., Zheng, X., Li, M., & Liu, M. (2023) · Frontiers of Medicine · doi:10.1007/s11684-023-1050-6 · Cited by 24 · see citing works
The Gut Microbiome and Pancreatic Cancer Development and Treatment
Attebury, H., & Daley, D. (2023) · The Cancer Journal · doi:10.1097/ppo.0000000000000647 · Cited by 23 · see citing works
Drivers of Gene Expression Dysregulation in Pancreatic Cancer
Venkat, S., Alahmari, A. A., & Feigin, M. E. (2021) · Trends in cancer · doi:10.1016/j.trecan.2021.01.008 · Cited by 22 · see citing works
MicroRNA-sensitive oncolytic measles virus for chemovirotherapy of pancreatic cancer
Singh, H. M., Leber, M. F., Bossow, S., Engeland, C. E., Dessila, J., Grossardt, C., Zaoui, K., Bell, J. C., Jäger, D., Kalle, C. V., et al. (2021) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2021.04.015 · Cited by 22 · see citing works
Targeting the Stroma in the Management of Pancreatic Cancer
Edwards, P., Kang, B. W., & Chau, I. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.691185 · Cited by 22 · see citing works
Laise, P., Turunen, M. M., Garcia, A. C., Tomassoni, L., Maurer, H. C., Elyada, E., Schmierer, B., Worley, J., Kesner, J. S., Tan, X., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.27.357269 · Cited by 21 · see citing works
Self-citationFAK promotes stromal PD-L2 expression associated with poor survival in pancreatic cancer
Davidson, C., Taggart, D., Sims, A. H., Lonergan, D. W., Canel, M., & Serrels, A. (2022) · British Journal of Cancer · doi:10.1038/s41416-022-01966-5 · Cited by 20 · see citing works
Tamagawa, H., Fujii, M., Togasaki, K., Seino, T., Kawasaki, S., Takano, A., Toshimitsu, K., Takahashi, S., Ohta, Y., Matano, M., et al. (2024) · Nature Cell Biology · doi:10.1038/s41556-024-01498-5 · Cited by 20 · see citing works
Cannon, A. C., Thompson, C. M., Maurer, H. C., Atri, P., Bhatia, R., West, S. C., Ghersi, D., Olive, K. P., Sushil Kumar, K., & Batra, S. K. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-1359 · Cited by 20 · see citing works
Self-citationSchreyer, D., Neoptolemos, J. P., Barry, S. T., & Bailey, P. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.795735 · Cited by 19 · see citing works
Serum levels of iCAF ‐derived osteoglycin predict favorable outcome in pancreatic cancer
Dings, M. P. G., Manoukian, P., Waasdorp, C., Quik, J. S. E., Strijker, M., Lodestijn, S. C., van Neerven, S. M., Moreno, L. F., de Oliveira, R. L., Bonsing, B. A., et al. (2022) · International Journal of Cancer · doi:10.1002/ijc.34276 · Cited by 18 · see citing works
Laser Capture Microdissection: A Gear for Pancreatic Cancer Research
Rao, B. H., Souček, P., & Hlaváč, V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232314566 · Cited by 19 · see citing works
Transcriptomic subtyping of gastrointestinal malignancies
de Back, T. R., van Hooff, S. R., Sommeijer, D. W., & Vermeulen, L. (2024) · Trends in cancer · doi:10.1016/j.trecan.2024.06.007 · Cited by 17 · see citing works
Krebs, N., Klein, L., Wegwitz, F., Espinet, E., Maurer, H. C., Tu, M., Penz, F., Küffer, S., Xu, X., Bohnenberger, H., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.154475 · Cited by 16 · see citing works
A tangled tale of molecular subtypes in pancreatic cancer
Singh, S. K., Hasselluhn, M. C., & Neeße, A. (2019) · Gut · doi:10.1136/gutjnl-2018-318086 · Cited by 16 · see citing works
Purinergic GPCR-integrin interactions drive pancreatic cancer cell invasion
Bort, E. T., Joseph, M. D., Wang, Q., Carter, E. P., Roth, N. J., Gibson, J., Samadi, A., Kocher, H. M., Simoncelli, S., McCormick, P. J., et al. (2023) · eLife · doi:10.7554/elife.86971 · Cited by 15 · see citing works
Alfarano, G., Audano, M., Chiaro, P. D., Balestrieri, C., Milan, M., Polletti, S., Spaggiari, P., Zerbi, A., Diaferia, G. R., Mitro, N., et al. (2022) · Gut · doi:10.1136/gutjnl-2021-325811 · Cited by 15 · see citing works
Lowe, M. E., Andersen, D. K., Caprioli, R. M., Choudhary, J., Cruz-Monserrate, Z., Dasyam, A. K., Forsmark, C. E., Gorelick, F. S., Gray, J. W., Haupt, M., et al. (2019) · Pancreas · doi:10.1097/mpa.0000000000001412 · Cited by 15 · see citing works
Self-citationGlapiński, F., Zając, W., Fudalej, M. M., Deptała, A., Czerw, A. I., Sygit, K., Kozłowski, R., & Badowska-Kozakiewicz, A. M. (2025) · Cancers · doi:10.3390/cancers17101599 · Cited by 14 · see citing works
Dong, M., Tang, R., Wang, W., Xu, J., Liu, J., Liang, C., Hua, J., Meng, Q., Yu, X., Zhang, B., et al. (2023) · Translational Oncology · doi:10.1016/j.tranon.2023.101692 · Cited by 13 · see citing works
Opposing roles for ADAMTS2 and ADAMTS14 in myofibroblast differentiation and function
Carter, E. P., Yoneten, K. K., Gavara, N., Tyler, E. J., Gauthier, V., Murray, E. R., ten Dijke, P., Cameron, A. J. M., Pearce, O. M. T., & Grose, R. P. (2023) · The Journal of Pathology · doi:10.1002/path.6214 · Cited by 13 · see citing works
Naso, J. R., Topham, J. T., Karasinska, J. M., Lee, M. K. C., Kalloger, S. E., Wong, H., Nelson, J., Moore, R. A., Mungall, A. J. J., Jones, S. J. M., et al. (2020) · Cancer Medicine · doi:10.1002/cam4.3695 · Cited by 13 · see citing works
Melzer, M. K., Breunig, M., Arnold, F., Wezel, F., Azoitei, A., Roger, É., Krüger, J., Merkle, J., Schütte, L. D., Resheq, Y. J., et al. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202102345 · Cited by 13 · see citing works
Hajkarim, M. C., May, M. S., Amin, A. D., Jamison, J. K. R., Tagore, S., D’Souza, E. K., Caprio, L., Walsh, Z. H., Fan, J. L., Zhang, M., et al. (2025) · Nature Genetics · doi:10.1038/s41588-025-02345-5 · Cited by 12 · see citing works
Self-citationPathology and Molecular Characteristics of Pancreatic Cancer
Kearney, J. F., Adsay, V. N., & Yeh, J. J. (2021) · Surgical Oncology Clinics of North America · doi:10.1016/j.soc.2021.06.003 · Cited by 12 · see citing works
Heterogeneity in Pancreatic Cancer Fibroblasts—TGFβ as a Master Regulator?
Watt, D. M., & Morton, J. P. (2021) · Cancers · doi:10.3390/cancers13194984 · Cited by 12 · see citing works
Ohara, Y., Liu, H., Moreno, P., Suzuki, S., & Hussain, S. P. (2025) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2025.108946 · Cited by 11 · see citing works
Monkman, J. H., Thompson, E. W., & Nagaraj, S. H. (2019) · Cancers · doi:10.3390/cancers11111745 · Cited by 11 · see citing works
Eicosanoids in the Pancreatic Tumor Microenvironment—A Multicellular, Multifaceted Progression
Gubbala, V. B., Jytosana, N., Trinh, V. Q., Maurer, H. C., Naeem, R. F., Lytle, N. K., Ma, Z., Zhao, S., Lin, W., Han, H., et al. (2022) · Gastro Hep Advances · doi:10.1016/j.gastha.2022.02.007 · Cited by 11 · see citing works
Self-citation
- Authors
- Maurer, C., Holmstrom, S. R., He, J., Laise, P., Su, T., Ahmed, A., Hibshoosh, H., Chabot, J. A., Oberstein, P. E., Sepulveda, A. R., Genkinger, J. M., Zhang, J., Iuga, A. C., Bansal, M., Califano, A., & Olive, K. P.
- Affiliations
- Columbia University Irving Medical Center (US)
- NYU Langone Health (US)
- University of California San Diego (US)
- Psychogenics (United States) (US)
- Corresponding author
- Califano, Andrea
- ORCID
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2019-01-18
- Volume
- 68
- Issue
- 6
- Pages
- 1034-1043
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- PMC
- PMC6509007
- OpenAlex
- W2910033560
- Cited by
- 216
- References
- 27
- Citations by year
- 2026: 15 · 2025: 27 · 2024: 30 · 2023: 22 · 2022: 36 · 2021: 43 · 2020: 27 · 2019: 16
- FWCI
- 12.85
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Gut (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene expression and cancer classification
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Keywords
- pancreatic ductal adenocarcinoma, tumor stroma, molecular subtypes, stromal gene expression, extracellular matrix, antitumor immunity
- MeSH terms
- Adenocarcinoma, Computer Simulation, Extracellular Matrix, Humans, Pancreatic Neoplasms, Sensitivity and Specificity, Gene Expression Regulation, Neoplastic, Case-Control Studies, Gene Expression Profiling, Carcinoma, Pancreatic Ductal, Microdissection
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