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Distant metastasis occurs late during the genetic evolution of pancreatic cancer
Open accessAbstract
Metastasis, the dissemination and growth of neoplastic cells in an organ distinct from that in which they originated, is the most common cause of death in cancer patients. This is particularly true for pancreatic cancers, where most patients are diagnosed with metastatic disease and few show a sustained response to chemotherapy or radiation therapy. Whether the dismal prognosis of patients with pancreatic cancer compared to patients with other types of cancer is a result of late diagnosis or early dissemination of disease to distant organs is not known. Here we rely on data generated by sequencing the genomes of seven pancreatic cancer metastases to evaluate the clonal relationships among primary and metastatic cancers. We find that clonal populations that give rise to distant metastases are represented within the primary carcinoma, but these clones are genetically evolved from the original parental, non-metastatic clone. Thus, genetic heterogeneity of metastases reflects that within the primary carcinoma. A quantitative analysis of the timing of the genetic evolution of pancreatic cancer was performed, indicating at least a decade between the occurrence of the initiating mutation and the birth of the parental, non-metastatic founder cell. At least five more years are required for the acquisition of metastatic ability and patients die an average of two years thereafter. These data provide novel insights into the genetic features underlying pancreatic cancer progression and define a broad time window of opportunity for early detection to prevent deaths from metastatic disease.
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“modeling studies performed on the mutational data have estimated that the timeline of multistep progression to invasive neoplasia in the pancreas likely spans multiple years and provides a theoretically wide window of opportunity for early detection27.”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [27]
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“Pancreatic tumours are highly heterogeneous, both within and between individuals.66,67”
From Early detection of pancreatic cancer (2020) · cites this paper as [67]
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“It is now appreciated that most clinically relevant solid tumors are highly heterogeneous at the phenotypic, physiologic, and genomic levels (13–15) and that they continue to evolve over time.”
From Radiomics: Images Are More than Pictures, They Are Data (2016) · cites this paper as [13]
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Cites
Spencer, P. M., Cameron, J. L., & Lin, L. (2000) · Cited by 7,202
Genetic instabilities in human cancers
Lengauer, C., Kinzler, K. W., & Vogelstein, B. (1998) · Nature · doi:10.1038/25292 · Cited by 4,168
Self-citationCore 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
Self-citationOlive, 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
Self-citationMetastasis: from dissemination to organ-specific colonization
Nguyen, D. X., Bos, P. D., & Massagué, J. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2622 · Cited by 2,716
Isaacson, P. G., Doǧan, A., Price, S. K., & Spencer, J. (1989) · The American Journal of Surgical Pathology · doi:10.1097/00000478-198912000-00004 · Cited by 1,913
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 827
Self-citationAdvanced pancreatic carcinoma: current treatment and future challenges
Stathis, A., & Moore, M. J. (2010) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2009.236 · Cited by 791
Signatures of mutation and selection in the cancer genome
Bignell, G. R., Greenman, C. D., Davies, H., Butler, A. P., Edkins, S., Andrews, J. M., Buck, G., Chen, L., Beare, D., Latimer, C., et al. (2010) · Nature · doi:10.1038/nature08768 · Cited by 707
Self-citationMaitra, A., & Hruban, R. H. (2008) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev.pathmechdis.3.121806.154305 · Cited by 707
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The Spectrum of Achalasia: Lessons From Studies of Pathophysiology and High-Resolution Manometry
Kahrilas, P. J., & Boeckxstaens, G. E. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.08.038 · Cited by 236
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 227
Obesity and pancreatic cancer: Overview of epidemiologic evidence and biologic mechanisms
Bracci, P. M. (2011) · Molecular Carcinogenesis · doi:10.1002/mc.20778 · Cited by 235
Heemskerk, B., Kvistborg, P., & Schumacher, T. N. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.333 · Cited by 239
Fast and scalable inference of multi-sample cancer lineages
Popic, V., Salari, R., Hajirasouliha, I., Kashef-Haghighi, D., West, R. B., & Batzoglou, S. (2015) · Genome biology · doi:10.1186/s13059-015-0647-8 · Cited by 231
Gut microbial profile analysis by MiSeq sequencing of pancreatic carcinoma patients in China
Ren, Z., Jiang, J., Xie, H., Li, A., Lu, H., Xu, S., Zhou, L., Zhang, H., Cui, G., Chen, X., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.18820 · Cited by 240
Links between mutant p53 and genomic instability
Hanel, W., & Moll, U. M. (2012) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23400 · Cited by 216
Hori, S. S., & Gambhir, S. S. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3003110 · Cited by 228
Time to progression of pancreatic ductal adenocarcinoma from low-to-high tumour stages
Yu, J., Blackford, A. L., dal Molin, M., Wolfgang, C. L., & Goggins, M. (2015) · Gut · doi:10.1136/gutjnl-2014-308653 · Cited by 224
Power of metabolomics in diagnosis and biomarker discovery of hepatocellular carcinoma
Wang, X., Zhang, A., & Sun, H. J. (2012) · Hepatology · doi:10.1002/hep.26130 · Cited by 223
Tumor immunosurveillance in human cancers
Mlecnik, B., Bindea, G., Pagès, F., & Galon, J. (2011) · Cancer and Metastasis Reviews · doi:10.1007/s10555-011-9270-7 · Cited by 231
Hiley, C. T., de Bruin, E. C., McGranahan, N., & Swanton, C. (2014) · Genome biology · doi:10.1186/s13059-014-0453-8 · Cited by 233
Single-cell DNA sequencing reveals a late-dissemination model in metastatic colorectal cancerPreprint
Leung, M. L., Davis, A., Gao, R., Casasent, T. D., Wang, Y., Sei, E., Vilar, E., Maru, D. M., Kopetz, S., & Navin, N. E. (2017) · Genome Research · doi:10.1101/gr.209973.116 · Cited by 220
Early Diagnosis of Pancreatic Cancer: Challenges and New Developments
Kaur, S., Baine, M. J., Jain, M., Sasson, A. R., & Batra, S. K. (2012) · Biomarkers in Medicine · doi:10.2217/bmm.12.69 · Cited by 221
Mroz, E. A., Tward, A. D., Pickering, C. R., Myers, J. N., Ferris, R. L., & Rocco, J. W. (2013) · Cancer · doi:10.1002/cncr.28150 · Cited by 227
Cellular Potts Modeling of Tumor Growth, Tumor Invasion, and Tumor Evolution
Szabó, A., & Merks, R. M. H. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00087 · Cited by 221
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 226
Advanced-stage pancreatic cancer: therapy options
Werner, J., Combs, S. E., Springfeld, C., Hartwig, W., Hackert, T., & Büchler, M. W. (2013) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2013.66 · Cited by 220
Pancreatic Cancer Metabolism: Breaking It Down to Build It Back Up
Perera, R. M., & Bardeesy, N. M. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0671 · Cited by 218
Eckert, M. A., Pan, S., Hernandez, K. M., Loth, R. M., Andrade, J., Volchenboum, S. L., Faber, P. W., MONTAG, A. G., Lastra, R. R., Peter, M. E., et al. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-0607 · Cited by 212
Acute Pancreatitis and Pancreatic Cancer Risk: A Nationwide Matched-Cohort Study in Denmark
Kirkegård, J., Cronin-Fenton, D. P., Heide‐Jørgensen, U., & Mortensen, F. V. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.02.011 · Cited by 219
MicroRNAs in Pancreatic Cancer: biomarkers, prognostic, and therapeutic modulators
Daoud, A. Z., Mulholland, E. J., Cole, G., & McCarthy, H. O. (2019) · BMC Cancer · doi:10.1186/s12885-019-6284-y · Cited by 238
Integrative Survival-Based Molecular Profiling of Human Pancreatic Cancer
Donahue, T. R., Tran, L. M., Hill, R., Li, Y., Kovochich, A., Calvopina, J. H., Patel, S. G., Wu, N., Hindoyan, A. A., Farrell, J. J., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-1539 · Cited by 212
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 227
Lowery, M. A., Jordan, E., Baştürk, O., Ptashkin, R. N., Zehir, A., Berger, M. F., Leach, T., Herbst, B. T., Askan, G., Maynard, H., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-0899 · Cited by 212
Self-citationAn 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 213
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
Self-citationMetastatic progression of breast cancer: insights from 50 years of autopsies
Cummings, M. C., Simpson, P. T., Reid, L., Jayanthan, J., Skerman, J., Song, S., Reed, A. E. M., Kutasovic, J. R., Morey, A. L., Marquart, L., et al. (2013) · The Journal of Pathology · doi:10.1002/path.4288 · Cited by 210
Early detection of pancreatic cancer: Where are we now and where are we going?
Zhou, B., Xu, J., Cheng, Y., Gao, J., Hu, S., Wang, L., & Zhan, H. (2017) · International Journal of Cancer · doi:10.1002/ijc.30670 · Cited by 218
Neoantigen quality predicts immunoediting in survivors of pancreatic cancer
Łuksza, M., Sethna, Z. M., Rojas, L. A., Lihm, J., Bravi, B., Elhanati, Y., Soares, K. C., Amisaki, M., Dobrin, A., Hoyos, D., et al. (2022) · Nature · doi:10.1038/s41586-022-04735-9 · Cited by 209
Self-citationSynthetic biomarkers: a twenty-first century path to early cancer detection
Kwong, G. A., Ghosh, S., Gamboa, L., Patriotis, C., Srivastava, S., & Bhatia, S. N. (2021) · Nature reviews. Cancer · doi:10.1038/s41568-021-00389-3 · Cited by 218
Gibson, W. J., Høivik, E. A., Halle, M. K., Taylor-Weiner, A. N., Cherniack, A. D., Berg, A., Holst, F., Zack, T. I., Werner, H. M. J., Staby, K. M., et al. (2016) · Nature Genetics · doi:10.1038/ng.3602 · Cited by 211
Deng, S.-J., Chen, H.-Y., Zeng, Y., Deng, S., Zhu, S., Zeng, Z., He, C., Liu, M., Huang, K., Zhong, J., et al. (2018) · Oncogene · doi:10.1038/s41388-018-0382-1 · Cited by 206
A Critical Analysis of the Clinical Use of Incretin-Based Therapies
Nauck, M. A. (2013) · Diabetes Care · doi:10.2337/dc12-2504 · Cited by 205
Do Circulating Tumor Cells, Exosomes, and Circulating Tumor Nucleic Acids Have Clinical Utility?
Gold, B., Cankovic, M., Furtado, L. V., Meier, F. A., & Gocke, C. D. (2015) · Journal of Molecular Diagnostics · doi:10.1016/j.jmoldx.2015.02.001 · Cited by 215
Boursi, B., Finkelman, B., Giantonio, B. J., Haynes, K., Rustgi, A. K., Rhim, A. D., Mamtani, R., & Yang, Y.-X. (2017) · Gastroenterology · doi:10.1053/j.gastro.2016.11.046 · Cited by 202
Floor, S. L., van Staveren, W. C. G., Larsimont, D., Dumont, J. E., & Maenhaut, C. (2011) · Oncogene · doi:10.1038/onc.2011.184 · Cited by 209
Kloosterman, W. P., Hoogstraat, M., Paling, O., Tavakoli-Yaraki, M., Renkens, I., Vermaat, J. S., van Roosmalen, M. J., van Lieshout, S., Nijman, I. J., Roessingh, W., et al. (2011) · Genome Biology · doi:10.1186/gb-2011-12-10-r103 · Cited by 204
Identification of a three-biomarker panel in urine for early detection of pancreatic adenocarcinoma
Radon, T. P., Massat, N. J., Jones, R., Alrawashdeh, W., Dumartin, L., Ennis, D., Duffy, S. W., Kocher, H. M., Pereira, S. P., Guarner (posthumous), L., et al. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-2467 · Cited by 203
Scalable whole-genome single-cell library preparation without preamplification
Zahn, H., Steif, A., Laks, E., Eirew, P. D., VanInsberghe, M. A., Shah, S. P., Aparicio, S. A. J. R., & Hansen, C. L. (2017) · Nature Methods · doi:10.1038/nmeth.4140 · Cited by 199
Lussier, Y. A., Khodarev, N. N., Regan, K., Corbin, K. S., Li, H., Ganai, S., Khan, S. A., Gnerlich, J. L., Darga, T. E., Fan, H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050141 · Cited by 201
Reshaping the Tumor Stroma for Treatment of Pancreatic Cancer
Vennin, C., Murphy, K. J., Morton, J. P., Cox, T. R., Pajic, M., & Timpson, P. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.11.280 · Cited by 207
Genomic heterogeneity in bladder cancer: challenges and possible solutions to improve outcomes
Meeks, J. J., Al‐Ahmadie, H. A., Faltas, B. M., Taylor, J. A., Flaig, T. W., DeGraff, D. J., Christensen, E., Woolbright, B. L., McConkey, D. J., & Dyrskjøt, L. (2020) · Nature Reviews Urology · doi:10.1038/s41585-020-0304-1 · Cited by 207
Hypoxia-inducible factors: a central link between inflammation and cancer
Triner, D., & Shah, Y. M. (2016) · Journal of Clinical Investigation · doi:10.1172/jci84430 · Cited by 199
Future medical applications of single-cell sequencing in cancer
Navin, N. E., & Hicks, J. B. (2011) · Genome Medicine · doi:10.1186/gm247 · Cited by 200
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Biswas, A., & Acharyya, S. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-0251-4 · Cited by 199
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Sicard, F., Gayral, M., Lulka, H., Buscail, L., & Cordelier, P. (2013) · Molecular Therapy · doi:10.1038/mt.2013.35 · Cited by 217
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Kanji, Z. S., & Gallinger, S. (2013) · Canadian Medical Association Journal · doi:10.1503/cmaj.121368 · Cited by 196
New biomarkers and targets in pancreatic cancer and their application to treatment
Costello, E., Greenhalf, W., & Neoptolemos, J. P. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.119 · Cited by 192
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El-Sayes, N., Vito, A., & Mossman, K. L. (2021) · Cancers · doi:10.3390/cancers13040806 · Cited by 208
Marquardt, J. U., Galle, P. R., & Teufel, A. (2011) · Journal of Hepatology · doi:10.1016/j.jhep.2011.07.007 · Cited by 194
Cystic precursors to invasive pancreatic cancer
Matthaei, H., Schulick, R. D., Hruban, R. H., & Maitra, A. (2011) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2011.2 · Cited by 193
Self-citationMolecular and cellular heterogeneity: the hallmark of glioblastoma
Aum, D. J., Kim, D. H., Beaumont, T., Leuthardt, E. C., Dunn, G. P., & Kim, A. H. (2014) · Neurosurgical FOCUS · doi:10.3171/2014.9.focus14521 · Cited by 200
Phylogenetic analyses of melanoma reveal complex patterns of metastatic dissemination
Sanborn, Z., Chung, J., Purdom, E. A., Wang, N. J., Kakavand, H., Wilmott, J. S., Butler, T. M., Thompson, J. F., Mann, G. J., Haydu, L. E., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508074112 · Cited by 186
Clinical utility of circulating tumor DNA for molecular assessment in pancreatic cancer
Takai, E., Totoki, Y., Nakamura, H. K., Morizane, C., Nara, S., Hama, N., Suzuki, M., Furukawa, E., Kato, M., Hayashi, H., et al. (2015) · Scientific Reports · doi:10.1038/srep18425 · Cited by 196
Self-citationOutcomes with FOLFIRINOX for borderline resectable and locally unresectable pancreatic cancer
Boone, B. A., Steve, J., Krasinskas, A. M., Zureikat, A. H., Lembersky, B. C., Gibson, M. K., Stoller, R. G., Zeh, H. J., & Bahary, N. (2013) · Journal of Surgical Oncology · doi:10.1002/jso.23392 · Cited by 191
Understanding Metastasis in Pancreatic Cancer: A Call for New Clinical Approaches
Tuveson, D. A., & Neoptolemos, J. P. (2012) · Cell · doi:10.1016/j.cell.2011.12.021 · Cited by 188
Biologic Challenges in the Detection of Circulating Tumor Cells
Joosse, S. A., & Pantel, K. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-3422 · Cited by 188
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Yachida, S., Wood, L. D., Suzuki, M., Takai, E., Totoki, Y., Kato, M., Luchini, C., Arai, Y., Nakamura, H. K., Hama, N., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2015.12.012 · Cited by 183
Self-citationEvolution of platinum resistance in high-grade serous ovarian cancer
Cooke, S. L., & Brenton, J. D. (2011) · The Lancet Oncology · doi:10.1016/s1470-2045(11)70123-1 · Cited by 213
Evolution and dynamics of pancreatic cancer progression
Yachida, S., & Iacobuzio–Donahue, C. A. (2013) · Oncogene · doi:10.1038/onc.2013.29 · Cited by 185
Self-citationExtracranial Oligometastases: A Subset of Metastases Curable With Stereotactic Radiotherapy
Corbin, K. S., Hellmän, S., & Weichselbaum, R. R. (2013) · Journal of Clinical Oncology · doi:10.1200/jco.2012.45.9651 · Cited by 185
Evolution of the cancer genome
Podlaha, O., Riester, M., De, S., & Michor, F. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.01.003 · Cited by 188
Palma, M. D., & Hanahan, D. (2012) · Molecular Oncology · doi:10.1016/j.molonc.2012.01.011 · Cited by 188
Boone, B. A., Steve, J., Zenati, M. S., Hogg, M. E., Singhi, A. D., Bartlett, D. L., Zureikat, A. H., Bahary, N., & Zeh, H. J. (2014) · Annals of Surgical Oncology · doi:10.1245/s10434-014-3842-z · Cited by 182
Czerniak, B. A., Dinney, C. P., & McConkey, D. J. (2016) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-012513-104703 · Cited by 182
Update on the management of pancreatic cancer: Surgery is not enough
Ansari, D., Gustafsson, A., & Andersson, R. E. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i11.3157 · Cited by 188
Dormant tumour cells, their niches and the influence of immunity
Goddard, E. T., Božić, I., Riddell, S. R., & Ghajar, C. M. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0214-0 · Cited by 180
Brown, D. N., Smeets, D., Székely, B., Larsimont, D., Szász, A. M., Adnet, P.-Y., Rothé, F., Rouas, G., Nagy, Z., Faragó, Z., et al. (2017) · Nature Communications · doi:10.1038/ncomms14944 · Cited by 183
Jayatilaka, H., Tyle, P., Chen, J. J., Kwak, M., Ju, J., Kim, H. J., Lee, J. S. H., Wu, P.-H., Gilkes, D. M., Fan, R., et al. (2017) · Nature Communications · doi:10.1038/ncomms15584 · Cited by 177
What does physics have to do with cancer?
Michor, F., Liphardt, J., Mauro Ferrari, B., & Widom, J. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3092 · Cited by 184
Emerging strategies for treating metastasis
Esposito, M., Ganesan, S., & Kang, Y. (2021) · Nature Cancer · doi:10.1038/s43018-021-00181-0 · Cited by 175
From human genome to cancer genome: The first decadePreprint
Wheeler, D. A., & Wang, L. (2013) · Genome Research · doi:10.1101/gr.157602.113 · Cited by 183
Genetic and Phenotypic Diversity in Breast Tumor Metastases
Almendro, V., Kim, H. J., Cheng, Y.-K., Gönen, M., Itzkovitz, S., Argani, P., van Oudenaarden, A., Sukumar, S. V., Michor, F., & Polyák, K. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-2357-t · Cited by 176
What We Have Learned About Pancreatic Cancer From Mouse Models
Pérez-Mancera, P. A., Guerra, C. E., Barbacid, M., & Tuveson, D. A. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.03.002 · Cited by 178
Roth, A. J. L., Ding, J., Morin, R. D., Crisan, A., Ha, G., Giuliany, R., Bashashati, A., Hirst, M., Turashvili, G., Oloumi, A., et al. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts053 · Cited by 173
Emerging roles of the CXCL12/CXCR4 axis in pancreatic cancer progression and therapy
Sleightholm, R. L., Neilsen, B. K., Li, J., Steele, M. M., Singh, R. K., Hollingsworth, M. A., & Oupický, D. (2017) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.05.012 · Cited by 171
Circulating tumour cells as a biomarker for diagnosis and staging in pancreatic cancer
Ankeny, J. S., Court, C. M., Hou, S., Li, Q., Song, M., Wu, D., Chen, J., Lee, T., Lin, M., Sho, S., et al. (2016) · British Journal of Cancer · doi:10.1038/bjc.2016.121 · Cited by 171
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 169
Self-citationCancer research: past, present and future
Cao, Y., DePinho, R. A., Ernst, M., & Vousden, K. H. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3138 · Cited by 170
The acinar differentiation determinant PTF1A inhibits initiation of pancreatic ductal adenocarcinoma
Krah, N. M., De La O, J.-P., Swift, G. H., Hoang, C. Q., Willet, S. G., Chen Pan, F., Cash, G. M., Bronner, M. P., Wright, C. V., MacDonald, R. J., et al. (2015) · eLife · doi:10.7554/elife.07125 · Cited by 166
Yu, J., Sadakari, Y., Shindo, K., Suenaga, M., Brant, A., Almario, J. A. N., Borges, M., Barkley, T., Fesharakizadeh, S., Ford, M., et al. (2017) · Gut · doi:10.1136/gutjnl-2015-311166 · Cited by 164
Self-citationMeasuring cancer evolution from the genome
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Self-citation
Metadata
- Authors
- Yachida, S., Jones, S., Bozic, I., Antal, T., Leary, R., Fu, B., Kamiyama, M., Hruban, R. H., Eshleman, J. R., Nowak, M. A., Velculescu, V. E., Kinzler, K. W., Vogelstein, B., & Iacobuzio-Donahue, C. A.
- Affiliations
- Johns Hopkins University (US)
- Howard Hughes Medical Institute (US)
- Harvard University (US)
- ORCID
- Venue
- Nature
- Published
- 2010-10
- Volume
- 467
- Issue
- 7319
- Pages
- 1114-1117
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3148940
- OpenAlex
- W2169895148
- Cited by
- 2,502
- References
- 24
- Citations by year
- 2026: 73 · 2025: 84 · 2024: 76 · 2023: 105 · 2022: 122 · 2021: 165 · 2020: 157 · 2019: 147 · 2018: 176 · 2017: 218 · 2016: 208 · 2015: 237 · 2014: 224 · 2013: 182 · 2012: 197
- FWCI
- 50.92
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (5r01ca121113-15)
- U.S. Public Health Service (A62924)
- National Cancer Institute (R01CA140599, CA 57345, R01-CA121113, CA-121113, CA43460, K08CA106610, R37CA043460, R01CA057345, CA106610, P50CA062924, R37CA057345)
- National Institute of General Medical Sciences (R01GM078986, GM078986)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- pancreatic cancer, distant metastasis, clonal evolution, tumor subclones, chromosomal rearrangements, genomic instability, early detection, tumor heterogeneity, therapeutic target
- MeSH terms
- Adenocarcinoma, Autopsy, Clone Cells, DNA Mutational Analysis, Humans, Liver Neoplasms, Lung Neoplasms, Models, Biological, Mutation, Neoplasm Metastasis, Pancreas, Pancreatic Neoplasms, Peritoneal Neoplasms, Time Factors, Disease Progression, Cell Lineage, Evolution, Molecular, Early Detection of Cancer
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