Precancerous neoplastic cells can move through the pancreatic ductal system
Open accessAbstract
Most adult carcinomas develop from noninvasive precursor lesions, a progression that is supported by genetic analysis. However, the evolutionary and genetic relationships among co-existing lesions are unclear. Here we analysed the somatic variants of pancreatic cancers and precursor lesions sampled from distinct regions of the same pancreas. After inferring evolutionary relationships, we found that the ancestral cell had initiated and clonally expanded to form one or more lesions, and that subsequent driver gene mutations eventually led to invasive pancreatic cancer. We estimate that this multi-step progression generally spans many years. These new data reframe the step-wise progression model of pancreatic cancer by illustrating that independent, high-grade pancreatic precursor lesions observed in a single pancreas often represent a single neoplasm that has colonized the ductal system, accumulating spatial and genetic divergence over time.
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Recent phylogenetic analyses of precursor lesions from patients with established cancer confirmed the stepwise progression model and accumulation of genetic alterations from PanINs to PDAC.
“Recent phylogenetic analyses of precursor lesions from the pancreata of patients with established cancer have confirmed the stepwise progression model and accumulation of genetic alterations in the transition from PanINs to PDAC postulated using more rudimentary techniques26.”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [26]
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Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
A genetic model for colorectal tumorigenesis
Fearon, E. R., & Vogelstein, B. (1990) · Cell · doi:10.1016/0092-8674(90)90186-i · Cited by 12,132 · see citing works
Self-citationA framework for variation discovery and genotyping using next-generation DNA sequencing data
DePristo, M. A., Banks, E., Poplin, R. E., Garimella, K. V., Maguire, J., Hartl, C., Philippakis, A., del Angel, G., Rivas, M. A., Hanna, M., et al. (2011) · Nature Genetics · doi:10.1038/ng.806 · Cited by 11,216 · see citing works
Signatures of mutational processes in human cancer
Initiative, A. P. C. G., Alexandrov, L. B., ICGC Breast Cancer Consortium, ICGC MMML-Seq Consortium, PedBrain, I., Nik-Zainal, S., Wedge, D. C., Aparicio, S. A. J. R., Behjati, S., Biankin, A. V., et al. (2013) · Nature · doi:10.1038/nature12477 · Cited by 9,660 · see citing works
Vogelstein, B., Papadopoulos, N., Velculescu, V. E., Zhou, S., Diaz, L. A., & Kinzler, K. W. (2013) · Science · doi:10.1126/science.1235122 · Cited by 7,863 · see citing works
Self-citationSpencer, P. M., Cameron, J. L., & Lin, L. (2000) · Cited by 7,202 · see citing works
Mutational heterogeneity in cancer and the search for new cancer-associated genes
Lawrence, M. S., Stojanov, P., Polak, P., Kryukov, G. V., Cibulskis, K., Sivachenko, A., Carter, S. L., Stewart, C., Mermel, C. H., Roberts, S. A., et al. (2013) · Nature · doi:10.1038/nature12213 · Cited by 5,461 · see citing works
Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples
Cibulskis, K., Lawrence, M. S., Carter, S. L., Sivachenko, A., Jaffe, D. B., Sougnez, C. L., Gabriel, S., Meyerson, M. M., Lander, E. S., & Getz, G. A. (2013) · Nature Biotechnology · doi:10.1038/nbt.2514 · Cited by 4,838 · 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
Self-citationGenomic 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
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
Self-citationDistant metastasis occurs late during the genetic evolution of pancreatic cancer
Yachida, S., Jones, S., Bozic, I., Antal, T., Leary, R., Fu, B., Kamiyama, M., Hruban, R. H., Eshleman, J. R., Nowak, M. A., et al. (2010) · Nature · doi:10.1038/nature09515 · Cited by 2,502 · see citing works
Self-citationDELLY: structural variant discovery by integrated paired-end and split-read analysis
Rausch, T., Zichner, T., Schlattl, A., Stütz, A. M., Beneš, V., & Korbel, J. O. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts378 · Cited by 2,384 · see citing works
Pancreatic 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
Self-citationIntegrated 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
Self-citationDeciphering Signatures of Mutational Processes Operative in Human Cancer
Alexandrov, L. B., Nik‐Zainal, S., Wedge, D. C., Campbell, P. J., & Stratton, M. R. (2013) · Cell Reports · doi:10.1016/j.celrep.2012.12.008 · Cited by 1,277 · see citing works
Shen, R., & Seshan, V. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw520 · Cited by 1,263 · 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
Hruban, R. H., Takaori, K., Klimstra, D. S., Adsay, N. V., Albores-Saavedra, J., Biankin, A. V., Biankin, S. A., Compton, C., Fukushima, N., Furukawa, T., et al. (2004) · American Journal of Surgical Pathology · doi:10.1097/01.pas.0000126675.59108.80 · Cited by 1,091 · see citing works
Self-citationProgression model for pancreatic cancer.
Hruban, R. H., Goggins, M., Parsons, J., & Kern, S. E. (2000) · PubMed · Cited by 872 · see citing works
Self-citationBasturk, O., Hong, S.-M., Wood, L. D., Adsay, N. V., Albores-Saavedra, J., Biankin, A. V., Brosens, L. A. A., Fukushima, N., Goggins, M., Hruban, R. H., et al. (2015) · American Journal of Surgical Pathology · doi:10.1097/pas.0000000000000533 · Cited by 864 · see citing works
Self-citationŞanlı, Ö., Dobruch, J. T., Knowles, M. A., Burger, M., Mehrdad Alemozaffar, A., Nielsen, M. E., & Lotan, Y. (2017) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2017.22 · Cited by 819 · see citing works
Comparative lesion sequencing provides insights into tumor evolution
Jones, S., Chen, W.-D. D., Parmigiani, G., Diehl, F., Beerenwinkel, N., Tibor Antal, A., Traulsen, A., Nowak, M. A., Siegel, C., Velculescu, V. E., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712345105 · Cited by 817 · see citing works
Self-citationDavoli, T., Xu, A. W., Mengwasser, K. E., Sack, L. M., Yoon, J. C., Park, P. J., & Elledge, S. J. (2013) · Cell · doi:10.1016/j.cell.2013.10.011 · Cited by 815 · see citing works
Chang, M. T., Asthana, S., Gao, S. P., Lee, B. H., Chapman, J. S., Kandoth, C., Gao, J., Socci, N. D., Solit, D. B., Olshen, A. B., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3391 · Cited by 808 · see citing works
Presence of Somatic Mutations in Most Early-Stage Pancreatic Intraepithelial Neoplasia
Kanda, M., Matthaei, H., Wu, J., Hong, S., Yu, J., Borges, M., Hruban, R. H., Maitra, A., Kinzler, K., Vogelstein, B., et al. (2012) · Gastroenterology · doi:10.1053/j.gastro.2011.12.042 · Cited by 741 · see citing works
Self-citationIntra-tumour diversification in colorectal cancer at the single-cell level
Roerink, S. F., Sasaki, N., Lee-Six, H., Young, M. D., Alexandrov, L. B., Behjati, S., Mitchell, T. J., Großmann, S., Lightfoot, H. W., Egan, D. A., et al. (2018) · Nature · doi:10.1038/s41586-018-0024-3 · Cited by 547 · see citing works
A renewed model of pancreatic cancer evolution based on genomic rearrangement patterns
Notta, F., Chan-Seng-Yue, M., Lemire, M., Li, Y., Wilson, G. W., Connor, A. A., Denroche, R. E., Liang, S.-B., Brown, A. M. K., Kim, J. C., et al. (2016) · Nature · doi:10.1038/nature19823 · Cited by 528 · see citing works
Pancreatic cancer biology and genetics from an evolutionary perspective
Makohon-Moore, A. P., & Iacobuzio–Donahue, C. A. (2016) · Nature reviews. Cancer · doi:10.1038/nrc.2016.66 · Cited by 430 · see citing works
Self-citationTomasetti, C., Vogelstein, B., & Parmigiani, G. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221068110 · Cited by 414 · see citing works
Self-citationMakohon-Moore, A. P., Zhang, M., Reiter, J. G., Bozic, I., Allen, B., Kundu, D., Chatterjee, K., Wong, F., Jiao, Y., Kohutek, Z. A., et al. (2017) · Nature Genetics · doi:10.1038/ng.3764 · Cited by 403 · see citing works
Evaluating the evaluation of cancer driver genes
Tokheim, C. J., Papadopoulos, N., Kinzler, K. W., Vogelstein, B., & Karchin, R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616440113 · Cited by 374 · see citing works
Self-citationTelomere Shortening Is Nearly Universal in Pancreatic Intraepithelial Neoplasia
van Heek, N. T., Meeker, A. K., Kern, S. E., Yeo, C. J., Lillemoe, K. D., Cameron, J. L., Offerhaus, G. J. A., Hicks, J. L., Wilentz, R. E., Goggins, M. G., et al. (2002) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)64432-x · Cited by 363 · see citing works
Self-citationWhole Genome Sequencing Defines the Genetic Heterogeneity of Familial Pancreatic Cancer
Roberts, N. J., Norris, A. L., Petersen, G. M., Bondy, M. L., Brand, R., Gallinger, S., Kurtz, R. C., Olson, S. H., Rustgi, A. K., Schwartz, A. G., et al. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0402 · Cited by 361 · see citing works
Self-citationThe Path to Cancer — Three Strikes and You're Out
Vogelstein, B., & Kinzler, K. W. (2015) · New England Journal of Medicine · doi:10.1056/nejmp1508811 · Cited by 324 · see citing works
Self-citationMurphy, S. J., Hart, S. N., Lima, J. F., Kipp, B. R., Klebig, M. L., Winters, J. L., Szabo, C., Zhang, L., Eckloff, B. W., Petersen, G. M., et al. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.07.049 · Cited by 199 · see citing works
ABRA: improved coding indel detection via assembly-based realignment
Mose, L. E., Wilkerson, M. D., Hayes, D. N., Perou, C. M., & Parker, J. S. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu376 · Cited by 174 · see citing works
Reconstructing metastatic seeding patterns of human cancers
Reiter, J. G., Makohon-Moore, A. P., Gerold, J. M., Božić, I., Chatterjee, K., Iacobuzio–Donahue, C. A., Vogelstein, B., & Nowak, M. A. (2017) · Nature Communications · doi:10.1038/ncomms14114 · Cited by 170 · see citing works
Self-citationHosoda, W., Chianchiano, P. E., Griffin, J. F., Pittman, M. E., Brosens, L. A. A., Noë, M., Yu, J., Shindo, K., Suenaga, M., Rezaee, N., et al. (2017) · The Journal of Pathology · doi:10.1002/path.4884 · Cited by 158 · see citing works
Self-citationPea, A., Yu, J., Rezaee, N., Luchini, C., He, J. P., Molin, M. D., Griffin, J. F., Fedor, H. L., Fesharakizadeh, S., Salvia, R., et al. (2016) · Annals of Surgery · doi:10.1097/sla.0000000000001817 · Cited by 132 · see citing works
Self-citationKlein, W. M., Hruban, R. H., Klein–Szanto, A. J., & Wilentz, R. E. (2002) · Modern Pathology · doi:10.1038/modpathol.3880544 · Cited by 131 · see citing works
Self-citationThe time of occurrence of liver metastasis in carcinoma of the pancreas
Amikura, K., Kobari, M., & Matsuno, S. (1995) · International Journal of Pancreatology · doi:10.1007/bf02788531 · Cited by 96 · see citing works
Matsuda, Y., Furukawa, T., Yachida, S., Nishimura, M., Seki, A., Nonaka, K., Aida, J., Takubo, K., Ishiwata, T., Kimura, W., et al. (2017) · Pancreas · doi:10.1097/mpa.0000000000000786 · Cited by 89 · see citing works
Self-citationBranching Process Models of Cancer
Durrett, R. T. (2015) · Springer eBooks · doi:10.1007/978-3-319-16065-8_1 · Cited by 57 · see citing works
Intraductal Spread of Pancreatic Cancer
Yamasaki, S., Suda, K., Nobukawa, B., & Sonoue, H. (2002) · Pancreatology · doi:10.1159/000065089 · Cited by 40 · see citing works
Pancreatic carcinogenesis — several small steps or one giant leap?
Reiter, J. G., & Iacobuzio–Donahue, C. A. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.190 · Cited by 20 · see citing works
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Pancreatic Cancer: Pathogenesis, Screening, Diagnosis, and Treatment
Wood, L. D., Canto, M. I., Jaffee, E. M., & Simeone, D. M. (2022) · Gastroenterology · doi:10.1053/j.gastro.2022.03.056 · Cited by 875 · see citing works
Goggins, M., Overbeek, K. A., Brand, R., Syngal, S., Del Chiaro, M., Bartsch, D. K., Bassi, C., Carrato, A., Farrell, J., Fishman, E. K., et al. (2020) · Gut · doi:10.1136/gutjnl-2019-319352 · Cited by 659 · see citing works
Self-citationPancreatic cancer evolution and heterogeneity: integrating omics and clinical data
Connor, A. A., & Gallinger, S. (2022) · Nature Reviews Cancer · doi:10.1038/s41568-021-00418-1 · Cited by 369 · see citing works
Cancer overdiagnosis: a biological challenge and clinical dilemma
Srivastava, S., Koay, E. J., Borowsky, A. D., Marzo, A. M. D., Ghosh, S., Wagner, P. D., & Kramer, B. S. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0142-8 · Cited by 339 · 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
Connor, A. A., Denroche, R. E., Jang, G. H., Lemire, M., Zhang, A. X. W., Chan‐Seng‐Yue, M., Wilson, G. W., Grant, R. C., Merico, D., Lungu, I. M., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2018.12.010 · Cited by 231 · see citing works
Schlesinger, Y., Yosefov-Levi, O., Kolodkin‐Gal, D., Granit, R. Z., Peters, L., Kalifa, R., Lei, X., Nasereddin, A., Shiff, I., Amran, O., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18207-z · Cited by 219 · see citing works
An analysis of genetic heterogeneity in untreated cancers
Reiter, J. G., Baretti, M., Gerold, J. M., Makohon-Moore, A. P., DAUD, A. I., Iacobuzio–Donahue, C. A., Azad, N. S., Kinzler, K. W., Nowak, M. A., & Vogelstein, B. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0185-x · Cited by 208 · see citing works
Self-citationThe pancreatic cancer genome revisited
Hayashi, A., Hong, J., & Iacobuzio-Donahue, C. A. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00463-z · Cited by 211 · see citing works
Self-citationA mathematical model of ctDNA shedding predicts tumor detection size
Avanzini, S., Kurtz, D. M., Chabon, J. J., Moding, E. J., Hori, S. S., Gambhir, S. S., Alizadeh, A. A., Diehn, M., & Reiter, J. G. (2020) · Science Advances · doi:10.1126/sciadv.abc4308 · Cited by 214 · see citing works
Self-citation3D genomic mapping reveals multifocality of human pancreatic precancers
Braxton, A. M., Kiemen, A. L., Grahn, M. P., Forjaz, A., Parksong, J., Babu, J. M., Lai, J., Zheng, L., Niknafs, N., Jiang, L., et al. (2024) · Nature · doi:10.1038/s41586-024-07359-3 · Cited by 158 · see citing works
Self-citationGenomic characterization of malignant progression in neoplastic pancreatic cysts
Noë, M., Niknafs, N., Fischer, C. G., Hackeng, W. M., Guthrie, V. B., Hosoda, W., Debeljak, M., Papp, E., Adleff, V., White, J. R., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17917-8 · Cited by 144 · see citing works
Self-citationBarriga, F. M., Tsanov, K. M., Ho, Y.-J., Sohail, N., Zhang, A., Baslan, T., Wuest, A. N., Del Priore, I., Meškauskaitė, B., Livshits, G., et al. (2022) · Nature Cancer · doi:10.1038/s43018-022-00443-5 · Cited by 125 · see citing works
Self-citationRecent insights into the biology of pancreatic cancer
Yao, W., Maitra, A., & Ying, H. (2020) · EBioMedicine · doi:10.1016/j.ebiom.2020.102655 · Cited by 125 · 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
Self-citationThe Evolutionary Origins of Recurrent Pancreatic Cancer
Sakamoto, H., Attiyeh, M. A., Gerold, J. M., Makohon-Moore, A. P., Hayashi, A., Hong, J., Kappagantula, R. L., Zhang, L., Melchor, J. P., Reiter, J. G., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-1508 · Cited by 118 · see citing works
Self-citationWhy is pancreatic cancer so deadly? The pathologist's view
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Nobre, A. R., Dalla, E., Yang, J., Huang, X., Wullkopf, L., Risson, E., Razghandi, P., Anton, M. L., Zheng, W., Seoane, J. A., et al. (2022) · Nature Cancer · doi:10.1038/s43018-022-00424-8 · Cited by 97 · see citing works
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Wood, L. D., Yurgelun, M. B., & Goggins, M. G. (2019) · Gastroenterology · doi:10.1053/j.gastro.2018.12.039 · Cited by 91 · see citing works
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Iacobuzio–Donahue, C. A., Michael, C., Baez, P., Kappagantula, R. L., Hooper, J. E., & Hollman, T. J. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0199-4 · Cited by 89 · see citing works
Self-citationJavadrashid, D., Baghbanzadeh, A., Derakhshani, A., Leone, P., Silvestris, N., Racanelli, V., Solimando, A. G., & Baradaran, B. (2021) · Biomedicines · doi:10.3390/biomedicines9040373 · Cited by 88 · see citing works
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Skaro, M. F., Nanda, N., Gauthier, C. D., Felsenstein, M., Jiang, Z., Qiu, M., Shindo, K., Yu, J., Hutchings, D., Javed, A. A., et al. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.01.254 · Cited by 65 · see citing works
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Lippman, S. M., Abate-Shen, C. T., Maresso, K. C., Colditz, G. A., Dannenberg, A. J., Davidson, N. E., Disis, M. L., DuBois, R. N., Szabo, E. M., Giuliano, A. R., et al. (2018) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-18-0421 · Cited by 47 · see citing works
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Rozengurt, E., & Eibl, G. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02499-y · Cited by 47 · see citing works
Singh, K., Pruski, M. A., Bland, R., Younes, M., Guha, S., Thosani, N. C., Maitra, A., Cash, B. D., McAllister, F. M., Logsdon, C. D., et al. (2020) · Laboratory Investigation · doi:10.1038/s41374-020-00490-5 · Cited by 44 · see citing works
Paracrine and cell autonomous signalling in pancreatic cancer progression and metastasis
Thomas, S. K., Lee, J., & Beatty, G. L. (2020) · EBioMedicine · doi:10.1016/j.ebiom.2020.102662 · Cited by 42 · see citing works
Sagami, R., Yamao, K., Nakahodo, J., Minami, R., Tsurusaki, M., Murakami, K., & Amano, Y. (2021) · Cancers · doi:10.3390/cancers13050945 · Cited by 43 · see citing works
Nagai, K., Mizukami, Y., Omori, Y., Kin, T., Yane, K., Takahashi, K., Ono, Y., Sugitani, A., Karasaki, H., Shinohara, T., et al. (2019) · Modern Pathology · doi:10.1038/s41379-019-0405-7 · Cited by 33 · see citing works
Rozengurt, E., & Eibl, G. (2021) · Cancers · doi:10.3390/cancers13205126 · Cited by 30 · see citing works
Mentis, A. A., Grivas, P. D., Dardiotis, E., Romas, N. A., & Papavassiliou, A. G. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03529-4 · Cited by 29 · see citing works
Pedro, B. A., & Wood, L. D. (2025) · Journal of Clinical Investigation · doi:10.1172/jci191937 · Cited by 29 · see citing works
Milan, M., Diaferia, G. R., & Natoli, G. (2021) · The EMBO Journal · doi:10.15252/embj.2020107206 · Cited by 27 · see citing works
Diagnostic Bioliquid Markers for Pancreatic Cancer: What We Have vs. What We Need
Liou, G., & Byrd, C. J. (2023) · Cancers · doi:10.3390/cancers15092446 · Cited by 25 · see citing works
Jiang, Z., Zheng, X., Li, M., & Liu, M. (2023) · Frontiers of Medicine · doi:10.1007/s11684-023-1050-6 · Cited by 24 · see citing works
Ren, Y., Huang, S., Dai, C., Xie, D., Zheng, L. Z., Xie, H., Zheng, H., She, Y., Zhou, F., Wang, Y., et al. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00288 · Cited by 25 · see citing works
Udgata, S., Takenaka, N., Bamlet, W. R., Oberg, A. L., Yee, S. S., Carpenter, E. L., Herman, D. S., Kim, J., Petersen, G. M., & Zaret, K. S. (2020) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-20-0403 · Cited by 24 · see citing works
Mathematical Modeling to Address Challenges in Pancreatic Cancer
Dogra, P., Ruiz-Ramírez, J., Peláez, M. J., Wang, Z., Vittorio Cristini, C., Parasher, G., & Rawat, M. (2020) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026620666200101095641 · Cited by 20 · see citing works
Omori, Y., Furukawa, T., Scarpa, A., & Luchini, C. (2023) · Journal of Clinical Pathology · doi:10.1136/jcp-2023-209012 · Cited by 19 · see citing works
The biology of pancreatic cancer morphology
McDonald, O. G. (2021) · Pathology · doi:10.1016/j.pathol.2021.09.012 · Cited by 18 · see citing works
Early Detection in a Mouse Model of Pancreatic Cancer by Imaging DNA Damage Response Signaling
Knight, J. C., Torres, J. B., Goldin, R. D., Mosley, M. J., Dias, G., Bravo, L. C., Kersemans, V., Allen, P. D., Mukherjee, S., Smart, S., et al. (2019) · Journal of Nuclear Medicine · doi:10.2967/jnumed.119.234708 · Cited by 18 · see citing works
Fujikura, K., Hutchings, D., Braxton, A. M., Zhu, Q., Laheru, D. A., Hruban, R. H., Thompson, E. D., & Wood, L. D. (2020) · Modern Pathology · doi:10.1038/s41379-020-0572-6 · Cited by 18 · see citing works
Self-citationPancreatic cancer pathology viewed in the light of evolution
Noë, M., Hong, S., Wood, L. D., Thompson, E. D., Roberts, N. J., Goggins, M., Klein, A. P., Eshleman, J. R., Kern, S. E., & Hruban, R. H. (2021) · Cancer and Metastasis Reviews · doi:10.1007/s10555-020-09953-z · Cited by 17 · see citing works
Self-citationFujita, Y., Matsuda, S., Sasaki, Y., Masugi, Y., Kitago, M., Yagi, H., Abe, Y., Shinoda, M., Tokino, T., Sakamoto, M., et al. (2019) · Cancer Science · doi:10.1111/cas.14268 · Cited by 17 · see citing works
Organotypic Culture of Acinar Cells for the Study of Pancreatic Cancer Initiation
Carrer, A., & Paoli, C. (2020) · Cancers · doi:10.3390/cancers12092606 · Cited by 16 · see citing works
Ma, J., Fu, S., Tan, J., Han, Y., Chen, Y., Deng, X., Shen, H., Zeng, S., Peng, Y., & Cai, C. (2025) · Advanced Science · doi:10.1002/advs.202502714 · Cited by 17 · see citing works
Cobo, I., Iglesias, M., Flández, M., Verbeke, C., Pozo, N., Llorente, M., Lawlor, R., Luchini, C., Rusev, B., Scarpa, A., et al. (2020) · Journal of Pathology · doi:10.1002/path.5570 · Cited by 12 · see citing works
Koopmann, B. D. M., Dunnewind, N., van Duuren, L. A., Lansdorp‐Vogelaar, I., Naber, S. K., Cahen, D. L., Bruno, M. J., & de Kok, I. M. C. M. (2023) · Gastroenterology · doi:10.1053/j.gastro.2023.08.027 · Cited by 15 · see citing works
Cell Dissemination in Pancreatic Cancer
Kim, J. (2022) · Cells · doi:10.3390/cells11223683 · Cited by 17 · see citing works
Koopmann, B. D. M., Omidvari, A., Lansdorp‐Vogelaar, I., Cahen, D. L., Bruno, M. J., & de Kok, I. M. C. M. (2022) · International Journal of Cancer · doi:10.1002/ijc.34379 · Cited by 14 · see citing works
Turner, K. M., Wilson, G. C., Patel, S. H., & Ahmad, S. A. (2023) · Annals of Surgical Oncology · doi:10.1245/s10434-023-14585-y · Cited by 14 · see citing works
Spadafora, V. K., Pryce, B. R., Oles, A. R., Talbert, E. E., Romeo, M. J., Vaena, S. G., Berto, S., Ostrowski, M. C., Wang, J., & D, D. C. G. (2024) · BMC Cancer · doi:10.1186/s12885-024-12104-0 · Cited by 14 · see citing works
Novel strategy for oncogenic alteration-induced lipid metabolism reprogramming in pancreatic cancer
Guo, D., Ye, L., Wu, W., Yu, X., & Jin, K. (2023) · Acta Biochimica et Biophysica Sinica · doi:10.3724/abbs.2023045 · Cited by 13 · see citing works
Identification and analysis of pancreatic intraepithelial neoplasia: opportunities and challenges
Pian, L.-L., Song, M.-H., Wang, T., Qi, L., Peng, T.-L., & Xie, K.-P. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1401829 · Cited by 14 · see citing works
Kim, J., Ekstrom, T. J., Yang, W., Donahue, G., Grygoryev, D., Ngo, T. T. M., Muschler, J. L., Morgan, T. K., & Zaret, K. S. (2021) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-21-0483 · Cited by 10 · see citing works
Sereni, E., Luchini, C., Salvia, R., & Pea, A. (2019) · Chinese Clinical Oncology · doi:10.21037/cco.2019.04.03 · Cited by 10 · see citing works
Can we predict the progression of premalignant pancreatic cystic tumors to ductal adenocarcinoma?
Chidambaram, S., Kawka, M., Gall, T., Cunningham, D., & Jiao, L. R. (2022) · Future Oncology · doi:10.2217/fon-2021-1545 · Cited by 9 · see citing works
Circulating Cell-Free Nucleic Acids as Biomarkers for Diagnosis and Prognosis of Pancreatic Cancer
Marin, A. M., Sanchuki, H. B. S., Namur, G. N., Uno, M., Zanette, D. L., & Aoki, M. N. (2023) · Biomedicines · doi:10.3390/biomedicines11041069 · Cited by 9 · see citing works
Post‐mortem tissue donation programs as platforms to accelerate cancer research
Dankner, M., Issa‐Chergui, B., & Bouganim, N. (2020) · The Journal of Pathology Clinical Research · doi:10.1002/cjp2.159 · Cited by 9 · see citing works
Tissue structure accelerates evolution: premalignant sweeps precede neutral expansionPreprint
West, J., Schenck, R. O., Gatenbee, C., Robertson‐Tessi, M., & Anderson, A. R. A. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/542019 · Cited by 9 · see citing works
Transcriptomic Plasticity Is a Hallmark of Metastatic Pancreatic Cancer
Jiménez-Sánchez, A., Persad, S., Hayashi, A., Umeda, S., Sharma, R., Xie, Y., Mehta, A., Park, W., Masilionis, I., Chu, T., et al. (2025) · Cancer Research · doi:10.1158/0008-5472.can-25-1117 · Cited by 8 · see citing works
Self-citationKiemen, A. L., Wu, P.-H., Braxton, A. M., Cornish, T. C., Hruban, R. H., Wood, L. D., Wirtz, D., & Zwicker, D. (2024) · Science Advances · doi:10.1126/sciadv.ado5103 · Cited by 8 · see citing works
Self-citationBraxton, A. M., Kiemen, A. L., Grahn, M. P., Forjaz, A., Babu, J. M., Zheng, L., Jiang, L., Cheng, H., Song, Q., Reichel, R., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.27.525553 · Cited by 8 · see citing works
Self-citationRuiz, C. F., Ge, X., McDonnell, R., Agabiti, S. S., McQuaid, D. C., Tang, A., Kharwa, M., Goodell, J., Saavedra-Peña, R. D. M., Wing, A., et al. (2026) · Cancer Discovery · doi:10.1158/2159-8290.cd-25-0734 · Cited by 7 · see citing works
Min, J., Schweizer, L., Zonderland, G., Selvanesan, B. C., Thomsen, J. H., Oldenburg, L., Bae, S.-W., Kim, B., Hernandez, S. D., Jez, G., et al. (2026) · Cancer Discovery · doi:10.1158/2159-8290.cd-25-1119 · Cited by 9 · see citing works
Gimotty, P. A., Till, J. E., Udgata, S., Takenaka, N., Yee, S. S., Lariviere, M. J., O’Hara, M. H., Reiss, K. A., O'Dwyer, P. J., Katona, B. W., et al. (2021) · Oncotarget · doi:10.18632/oncotarget.28099 · Cited by 7 · see citing works
Is the Early Detection of Pancreatic Cancer Possible? It Is Good News, Bad News
Hruban, R. H. (2019) · Pancreas · doi:10.1097/mpa.0000000000001299 · Cited by 7 · see citing works
Self-citationClonal analysis of metachronous double biliary tract cancers
Omori, Y., Aoki, S., Ono, Y., Kokumai, T., Yoshimachi, S., Sato, H., Kusaka, A., Iseki, M., Douchi, D., Miura, T., et al. (2024) · The Journal of Pathology · doi:10.1002/path.6265 · Cited by 6 · see citing works
Cancer metabolism challenges genomic instability and clonal evolution as therapeutic targets
Takeda, Y., Chijimatsu, R., Ofusa, K., Kobayashi, S., Doki, Y., Eguchi, H., & Ishii, H. (2022) · Cancer Science · doi:10.1111/cas.15279 · Cited by 5 · see citing works
Yang, S., Chen, T., Cui, M., & Hu, Y. N. (2025) · International Journal of Surgery · doi:10.1097/js9.0000000000002814 · Cited by 6 · see citing works
Genomic evolution of pancreatic cancer at single-cell resolution
Zhang, H., Sashittal, P., Karnoub, E.-R. R., Jakatdar, A., Umeda, S., Hong, J., Noronha, A. M., Cardenas, A., Erakky, A., McIntyre, C. A., et al. (2026) · Nature Genetics · doi:10.1038/s41588-025-02468-9 · Cited by 5 · see citing works
Self-citationHa, C. S. R., Müller‐Nurasyid, M., Petrera, A., Hauck, S. M., Marini, F., Bartsch, D. K., Slater, E. P., & Strauch, K. (2023) · PLoS ONE · doi:10.1371/journal.pone.0280399 · Cited by 5 · see citing works
Takeda, Y., Matsumoto, K., Onoyama, T., Yamashita, T., Koda, H., Hamamoto, W., Sakamoto, Y., Shimosaka, T., Kawahara, S., Seki, Y., et al. (2023) · Diagnostics · doi:10.3390/diagnostics13091536 · Cited by 4 · see citing works
A conserved re-epithelialization program underlies malignancy in pancreatic ductal adenocarcinoma
Zhuo, M., Li, Y., Zhang, Y., Yang, C. R., Zou, D., Xu, W., Han, J., Wang, S., Deng, H., Pan, X., et al. (2026) · Cancer Cell · doi:10.1016/j.ccell.2026.03.021 · Cited by 3 · see citing works
Tachibana, S., Mizukami, Y., Ono, Y., Sugiyama, Y., Okada, T., Kitazaki, A., Sasajima, J., Tominaga, M., Sakamoto, J., Kimura, K., et al. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00728 · Cited by 3 · see citing works
Clinical Relevance of Cancerization of Ducts in Resected Pancreatic Ductal Adenocarcinoma
Kinny‐Köster, B., Ahmad, Y., Pflüger, M. J., Habib, J. R., Fujikura, K., Hutchings, D., Cameron, J. L., Shubert, C. R., Lafaro, K. J., Burkhart, R. A., et al. (2024) · Pancreas · doi:10.1097/mpa.0000000000002326 · Cited by 3 · see citing works
Self-citationAnandi, L., V, Garcia, J., Ros, M., Janská, L., Liu, J., & Carmona‐Fontaine, C. (2024) · Life Science Alliance · doi:10.26508/lsa.202403053 · Cited by 2 · see citing works
Yuan, Q., Chen, J., Luo, P., liu, K., Guo, F., Xu, Y., Tong, M., Xiang, H., & Shang, D. (2026) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-026-03712-8 · Cited by 2 · see citing works
Is it time to reconsider the principles of pancreatic cancer surgery?
Barreto, S. G., & Sirohi, B. (2018) · Pancreatology · doi:10.1016/j.pan.2018.12.003 · Cited by 2 · see citing works
A war on many fronts: cross disciplinary approaches for novel cancer treatment strategies
Herrera, A. D. P., & Ferrall‐Fairbanks, M. C. (2024) · Frontiers in Genetics · doi:10.3389/fgene.2024.1383676 · Cited by 2 · see citing works
Emerging and extensive clonal evolution in the pancreas
Makohon-Moore, A. P. (2024) · Trends in cancer · doi:10.1016/j.trecan.2024.06.011 · Cited by 2 · see citing works
Self-citationOkada, T., Mizukami, Y., Hayashi, A., Kawabata, H., Sato, H., Kawamoto, T., Goto, T., Taniue, K., Ono, Y., Karasaki, H., et al. (2020) · Suizo · doi:10.2958/suizo.35.302 · Cited by 2 · see citing works
Skip to the end: metastasis before tumorigenesis
Nobre, A. R., & Boire, A. A. (2022) · Nature Genetics · doi:10.1038/s41588-022-01228-3 · Cited by 1 · see citing works
Evidence that extra copies of chromosome 1q play a role in the early phases of pancreatic neoplasia
Douville, C. B., Parksong, J., Molin, M. D., Graham, S., Greipp, P. T., Knudson, R. A., Curtis, S. D., Wang, Y., Dobbyn, L., Popoli, M., et al. (2026) · Science Advances · doi:10.1126/sciadv.adx7501 · Cited by 1 · see citing works
Self-citationEarly cellular plasticity promotes progression and dissemination in pancreatic adenocarcinoma
Innamorati, G., Malpeli, G., Giacomello, L., Salvia, R., & Wilkie, T. M. (2026) · Cancer and Metastasis Reviews · doi:10.1007/s10555-026-10326-1 · Cited by 1 · see citing works
Wang, Y., Zhang, Y., Wang, X., Zhao, W., Li, Q., Zhou, M., Liu, Y., Yi, X., He, J. I., Li, Y. P., et al. (2026) · Molecular Cancer · doi:10.1186/s12943-026-02712-8 · Cited by 1 · see citing works
Remnant Pancreatic Cancer After Surgical Resection for Pancreatic Cancer
Miyasaka, Y., & Nakamura, M. (2022) · Springer eBooks · doi:10.1007/978-981-19-0063-1_54 · Cited by 1 · see citing works
Palliative treatment of pancreatic cancer
Tseimakh, A. E., Lazarev, A. F., & Shoykhet, Y. N. (2023) · Russian Journal of Oncology · doi:10.17816/onco115222 · Cited by 1 · see citing works
Giordano, G., Cipolletta, G., Mellone, A., Puopolo, G., Coppola, L., Santis, E. D., Forte, N. R., Napolitano, F., Caruso, F. P., Parente, P., et al. (2024) · Pancreatology · doi:10.1016/j.pan.2024.06.010 · Cited by 1 · see citing works
Chen, R., Sugiyama, A., Kataoka, N., Sugimoto, M., Yokoyama, S., Fukuda, A., Takaishi, S., & Seno, H. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00316 · Cited by 1 · see citing works
Schäfer, H., Traulsen, A., & Sebens, S. (2019) · HepatoBiliary Surgery and Nutrition · doi:10.21037/hbsn.2019.06.03 · Cited by 1 · see citing works
Chromosome 9p21.3 Coordinates Cell Intrinsic and Extrinsic Tumor SuppressionPreprint
Barriga, F. M., Tsanov, K. M., Ho, Y.-J., Sohail, N., Zhang, A. X. W., Baslan, T., Wuest, A. N., Priore, I. S. D., Meškauskaitė, B., Livshits, G., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.22.504793 · Cited by 1 · see citing works
Self-citation
- Authors
- Makohon-Moore, A. P., Matsukuma, K., Zhang, M., Reiter, J. G., Gerold, J. M., Jiao, Y., Sikkema, L., Attiyeh, M. A., Yachida, S., Sandone, C., Hruban, R. H., Klimstra, D. S., Papadopoulos, N., Nowak, M. A., Kinzler, K. W., Vogelstein, B., & Iacobuzio-Donahue, C. A.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- University of California, Davis (US)
- Johns Hopkins University (US)
- Harvard University (US)
- The University of Osaka (JP)
- Howard Hughes Medical Institute (US)
- ORCID
- Venue
- Nature
- Published
- 2018-09
- Volume
- 561
- Issue
- 7722
- Pages
- 201-205
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC6342205
- OpenAlex
- W2888908131
- Cited by
- 120
- References
- 47
- Citations by year
- 2026: 13 · 2025: 7 · 2024: 14 · 2023: 17 · 2022: 13 · 2021: 13 · 2020: 20 · 2019: 19 · 2018: 3
- FWCI
- 4.15
- Type
- journal article
- Language
- en
- Open access
- green
- pure.amsterdamumc.nl
- Licence
- other-oa
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (acceptedVersion, other-oa)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Lustgarten Foundation
- Virginia and D.K. Ludwig Fund for Cancer Research
- Rolfe Pancreatic Cancer Foundation
- Austrian Science Fund (J 3996)
- National Institutes of Health (CA062924)
- National Cancer Institute (T32CA067751, T32CA160001, F31CA180682, P50CA062924, P30CA008748)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Keywords
- pancreatic cancer, pancreatic precursor lesions, somatic mutations, clonal evolution, tumor progression, pancreatic ductal system, tumor heterogeneity, driver mutations
- MeSH terms
- Exome Sequencing, Humans, Models, Biological, Neoplasm Invasiveness, Pancreatic Ducts, Pancreatic Neoplasms, Precancerous Conditions, Time Factors, Mutagenesis, Disease Progression, Cell Lineage, Evolution, Molecular, Polymorphism, Single Nucleotide, Carcinoma, Pancreatic Ductal, INDEL Mutation
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