Pancreatic Cancer

Maitra, Anirban; Hruban, Ralph H.

doi:10.1146/annurev.pathmechdis.3.121806.154305

Cited by 717Pancreatic and Hepatic Oncology ResearchCancer Genomics and DiagnosticsPancreatitis Pathology and Treatment

Pancreatic Cancer

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Maitra, Anirban, Hruban, Ralph H.·2008·Annual Review of Pathology: Mechanisms of Disease

DOI 10.1146/annurev.pathmechdis.3.121806.154305PMC PMC2666336

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Abstract

The past two decades have witnessed an explosion in our understanding of pancreatic cancer, and it is now clear that pancreatic cancer is a disease of inherited (germ-line) and somatic gene mutations. The genes mutated in pancreatic cancer include KRAS2, p16/CDKN2A, TP53, and SMAD4/DPC4, and these are accompanied by a substantial compendium of genomic and transcriptomic alterations that facilitate cell cycle deregulation, cell survival, invasion, and metastases. Pancreatic cancers do not arise de novo, and three distinct precursor lesions have been identified. Experimental models of pancreatic cancer have been developed in genetically engineered mice, which recapitulate the multistep progression of the cognate human disease. Although the putative cell of origin for pancreatic cancer remains elusive, minor populations of cells with stem-like properties have been identified that appear responsible for tumor initiation, metastases, and resistance of pancreatic cancer to conventional therapies.

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Pancreatic cancer commonly features mutations in key genes KRAS, p16/CDKN2A, TP53 and SMAD4/DPC4.
“Pancreatic cancer commonly features mutations in key genes, such as KRAS, p16/CDKN2A, TP53 and SMAD4/DPC4 [3,4,5] (Table 1).”
From Significance of TP53, CDKN2A, SMAD4 and KRAS in Pancreatic Cancer (2024) · cites this paper as [3]
Somatic CDKN2A loss is common in pancreatic cancer.
“Germline CDKN2A mutation is associated with an increased risk of melanoma and pancreatic cancer, and somatic CDKN2A loss is common in pancreatic cancer49–51.”
From Impact of KRAS mutations and co-mutations on clinical outcomes in pancreatic ductal adenocarcinoma (2024) · cites this paper as [50]
Germline CDKN2A mutation is associated with an increased risk of melanoma and pancreatic cancer.
“Germline CDKN2A mutation is associated with an increased risk of melanoma and pancreatic cancer, and somatic CDKN2A loss is common in pancreatic cancer49–51.”
From Impact of KRAS mutations and co-mutations on clinical outcomes in pancreatic ductal adenocarcinoma (2024) · cites this paper as [50]

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Sahin, F., Maitra, A., Argani, P., Sato, N., Maehara, N., Montgomery, E. A., Goggins, M., Hruban, R. H., & Su, G. H. (2003) · Modern Pathology · doi:10.1097/01.mp.0000075645.97329.86 · Cited by 118 · see citing works
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Haber, D. A., Bell, D. W., Sordella, R., Kwak, E. L., Godin-Heymann, N., Sharma, S. V., Lynch, T. J., & Settleman, J. E. (2005) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2005.70.043 · Cited by 116 · see citing works
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Zhou, W., Sokoll, L. J., Bruzek, D. J., Zhang, L., Velculescu, V. E., Goldin, S. B., Hruban, R. H., Kern, S. E., Hamilton, S. R., Chan, D. W., et al. (1998) · PubMed · Cited by 115 · see citing works
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McCarthy, D. M., Maitra, A., Argani, P., Rader, A. E., Faigel, D. O., van Heek, N. T., Hruban, R. H., & Wilentz, R. E. (2003) · Applied immunohistochemistry & molecular morphology · doi:10.1097/00129039-200309000-00006 · Cited by 110 · see citing works
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Chen, R., Pan, S., Cooke, K., Moyes, K. W., Bronner, M. P., Goodlett, D. R., Aebersold, R. H., & Brentnall, T. A. (2006) · Pancreas · doi:10.1097/01.mpa.0000240615.20474.fd · Cited by 105 · see citing works
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Leach, S. (2005) · Journal of Clinical Gastroenterology · doi:10.1097/01.mcg.0000155547.83901.a3 · Cited by 43 · see citing works
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Point mutations of protein kinases and individualised cancer therapy
Davies, M. A., Hennessy, B. T., & Mills, G. B. (2006) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.7.16.2243 · Cited by 33 · see citing works
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Treatment of Metastatic Pancreatic Cancer
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Pancreatic carcinoma in carriers of a specific 19 base pair deletion of CDKN2A/p16 (p16-leiden).
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Telomerase as a new target for pancreatic cancer treatment
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MicroRNAs Linked to Pancreatic CancerMicroRNAs Linked to Pancreatic Cancer
Hampton, T. (2007) · JAMA · doi:10.1001/jama.297.9.937 · Cited by 11 · see citing works
What's new in pancreatic cancer treatment pipeline?
Hoff, D. D. V. (2006) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2005.11.009 · Cited by 11 · see citing works

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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
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Pancreatic cancer
Hidalgo, M. (2010) · New England Journal of Medicine · doi:10.1056/nejmra0901557 · Cited by 2,570 · see citing works
Distant 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
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HMGB1 in health and disease
Kang, R., Chen, R., Zhang, Q., Hou, W., Wu, S., Cao, L., Huang, J., Yu, Y., Fan, X.-G., Yan, Z., et al. (2014) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2014.05.001 · Cited by 956 · see citing works
Early Detection of Pancreatic Cancer: Opportunities and Challenges
Singhi, A. D., Koay, E. J., Chari, S. T., & Maitra, A. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.01.259 · Cited by 841 · see citing works
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TGF-β signaling in health and disease
Massagué, J., & Sheppard, D. (2023) · Cell · doi:10.1016/j.cell.2023.07.036 · Cited by 890 · see citing works
Exomic Sequencing Identifies PALB2 as a Pancreatic Cancer Susceptibility Gene
Jones, S., Hruban, R. H., Kamiyama, M., Borges, M., Zhang, X., Parsons, D. W., Lin, J. C.-H., Palmisano, E., Brune, K., Jaffee, E. M., et al. (2009) · Science · doi:10.1126/science.1171202 · Cited by 826 · see citing works
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Advanced 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 · see citing works
Epidemiology of pancreatic cancer: an overview
Raimondi, S., Maisonneuve, P., & Lowenfels, A. B. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.177 · Cited by 742 · see citing works
Oncogenic Kras-induced GM-CSF production promotes the development of pancreatic neoplasia
Pylayeva-Gupta, Y., Lee, K. E., Hajdu, C. H., Miller, G., & Bar-Sagi, D. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.04.024 · Cited by 721 · see citing works
Pancreatic Ductal Adenocarcinoma: Current and Evolving Therapies
Adamska, A., Domenichini, A., & Falasca, M. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18071338 · Cited by 612 · see citing works
MicroRNAs in Plasma of Pancreatic Ductal Adenocarcinoma Patients as Novel Blood-Based Biomarkers of Disease
Wang, J., Chen, J., Chang, P., Leblanc, A. B., Li, D., Abbruzzesse, J. L., Frazier, M. L., Killary, A. M., & Sen, S. (2009) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-09-0094 · Cited by 560 · see citing works
Genetics and biology of pancreatic ductal adenocarcinoma
Ying, H., Dey, P., Yao, W., Kimmelman, A. C., Draetta, G. F., Maitra, A., & DePinho, R. A. (2016) · Genes & Development · doi:10.1101/gad.275776.115 · Cited by 527 · see citing works
Fabrication of gold nanoparticles for targeted therapy in pancreatic cancer
Patra, C. R., Bhattacharya, R., Mukhopadhyay, D., & Mukherjee, P. (2009) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.11.007 · Cited by 464 · see citing works
The Causes and Consequences of Polyploidy in Normal Development and Cancer
Davoli, T., & de Lange, T. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154234 · Cited by 432 · see citing works
EGF Receptor Signaling Is Essential for K-Ras Oncogene-Driven Pancreatic Ductal Adenocarcinoma
Navas, C., Hernández-Porras, I., Schuhmacher, A. J., Sibilia, M., Guerra, C., & Barbacid, M. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.08.001 · Cited by 391 · see citing works
Combined inhibition of BET family proteins and histone deacetylases as a potential epigenetics-based therapy for pancreatic ductal adenocarcinoma
Mazur, P., Herner, A., Mello, S., Wirth, M., Hausmann, S., Sánchez-Rivera, F. J., Lofgren, S. M., Kuschma, T., Hahn, S., Vangala, D., et al. (2015) · Nature Medicine · doi:10.1038/nm.3952 · Cited by 378 · see citing works
Tumor-stromal crosstalk in pancreatic cancer and tissue fibrosis
Thomas, D., & Radhakrishnan, P. (2019) · Molecular Cancer · doi:10.1186/s12943-018-0927-5 · Cited by 399 · see citing works
Notch and Kras reprogram pancreatic acinar cells to ductal intraepithelial neoplasia
Jean–Paul De La, O., Emerson, L. L., Goodman, J. L., Froebe, S. C., Illum, B. E., Curtis, A. B., & Murtaugh, L. C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810111105 · Cited by 396 · see citing works
Notch as a tumour suppressor
Nowell, C. S., & Radtke, F. (2017) · Nature reviews. Cancer · doi:10.1038/nrc.2016.145 · Cited by 371 · see citing works
Inflammation, Autophagy, and Obesity: Common Features in the Pathogenesis of Pancreatitis and Pancreatic Cancer
Gukovsky, I., Li, N., Todoric, J., Gukovskaya, A. S., & Karin, M. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.02.007 · Cited by 346 · see citing works
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Oberstein, P. E., & Olive, K. P. (2013) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x13478680 · Cited by 334 · see citing works
Hyaluronan, fluid pressure, and stromal resistance in pancreas cancer
Provenzano, P. P., & Hingorani, S. R. (2013) · British Journal of Cancer · doi:10.1038/bjc.2012.569 · Cited by 326 · see citing works
Repression of the miR-143/145 cluster by oncogenic Ras initiates a tumor-promoting feed-forward pathwayPreprint
Kent, O. A., Chivukula, R. R., Mullendore, M. E., Wentzel, E. A., Feldmann, G., Lee, K. H., Liu, S., Leach, S. D., Maitra, A., & Mendell, J. T. (2010) · Genes & Development · doi:10.1101/gad.1950610 · Cited by 310 · see citing works
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Mutant KRAS is a druggable target for pancreatic cancer
Zorde Khvalevsky, E., Gabai, R., Rachmut, I. H., Horwitz, E., Brunschwig, Z., Orbach, A., Shemi, A., Golan, T., Domb, A. J., Yavin, E., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314307110 · Cited by 295 · see citing works
A Critical Analysis of the Clinical Use of Incretin-Based Therapies
Butler, P. C., Elashoff, M., Elashoff, R., & Gale, E. A. M. (2013) · Diabetes Care · doi:10.2337/dc12-2713 · Cited by 296 · see citing works
Restitution of Tumor Suppressor MicroRNAs Using a Systemic Nanovector Inhibits Pancreatic Cancer Growth in Mice
Pramanik, D., Campbell, N. R., Karikari, C. A., Chivukula, R. R., Kent, O. A., Mendell, J. T., & Maitra, A. (2011) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-11-0152 · Cited by 295 · see citing works
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Detection of early pancreatic ductal adenocarcinoma with thrombospondin-2 and CA19-9 blood markers
Kim, J., Bamlet, W. R., Oberg, A. L., Chaffee, K. G., Donahue, G., Cao, X.-J., Chari, S., Garcia, B. A., Petersen, G. M., & Zaret, K. S. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aah5583 · Cited by 269 · see citing works
The Pathology and Genetics of Metastatic Pancreatic Cancer
Yachida, S., & Iacobuzio–Donahue, C. A. (2009) · Archives of Pathology & Laboratory Medicine · doi:10.5858/133.3.413 · Cited by 269 · see citing works
Circulating tumor DNA as an early cancer detection tool
Campos-Carrillo, A., Weitzel, J. N., Sahoo, P., Rockne, R. C., Mokhnatkin, J. V., Murtaza, M., Gray, S. W., Goetz, L. H., Goel, A., Schork, N. J., et al. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107458 · Cited by 252 · see citing works
Mesenchymal lineage heterogeneity underlies nonredundant functions of pancreatic cancer-associated fibroblasts
Helms, E. J., Berry, M. W., Chaw, R. C., DuFort, C. C., Sun, D., Onate, M. K., Oon, C., Bhattacharyya, S., Sanford-Crane, H., Horton, W., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-0601 · Cited by 238 · see citing works
Molecular Pathogenesis of Pancreatic Cancer
Grant, T. J., Hua, K., & Singh, A. (2016) · Progress in Molecular Biology and Translational Science · doi:10.1016/bs.pmbts.2016.09.008 · Cited by 237 · see citing works
Immunohistochemically Detected Expression of 3 Major Genes (CDKN2A/p16, TP53, and SMAD4/DPC4) Strongly Predicts Survival in Patients With Resectable Pancreatic Cancer
Oshima, M., Okano, K., Muraki, S., Haba, R., Maeba, T., Suzuki, Y., & Yachida, S. (2013) · Annals of Surgery · doi:10.1097/sla.0b013e3182827a65 · Cited by 236 · see citing works
Resveratrol, a multitargeted agent, can enhance antitumor activity of gemcitabine in vitro and in orthotopic mouse model of human pancreatic cancer
Harikumar, K. B., Kunnumakkara, A. B., Sethi, G., Diagaradjane, P., Anand, P., Pandey, M. K., Gelovani, J. G., Krishnan, S., Guha, S., & Aggarwal, B. B. (2010) · International Journal of Cancer · doi:10.1002/ijc.25041 · Cited by 232 · see citing works
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 213 · see citing works
Systemic Administration of Polymeric Nanoparticle-Encapsulated Curcumin (NanoCurc) Blocks Tumor Growth and Metastases in Preclinical Models of Pancreatic Cancer
Bisht, S., Mizuma, M., Feldmann, G., Ottenhof, N. A., Hong, S., Pramanik, D., Chenna, V., Karikari, C. A., Sharma, R. B., Goggins, M., et al. (2010) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-10-0172 · Cited by 216 · see citing works
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Cellular Histone Modification Patterns Predict Prognosis and Treatment Response in Resectable Pancreatic Adenocarcinoma: Results From RTOG 9704
Manuyakorn, A., Paulus, R., Farrell, J. J., Dawson, N. A., Tze, S., Cheung-Lau, G. C., Hines, O. J., Reber, H. A., Seligson, D. B., Horvath, S., et al. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.24.5639 · Cited by 216 · see citing works
Advances in diagnosis, treatment and palliation of pancreatic carcinoma: 1990-2010
Sharma, C. (2011) · World Journal of Gastroenterology · doi:10.3748/wjg.v17.i7.867 · Cited by 214 · see citing works
Genetics of Biliary Tract Cancers and Emerging Targeted Therapies
Hezel, A. F., Deshpande, V., & Zhu, A. X. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.27.4787 · Cited by 210 · see citing works
MicroRNA Molecular Profiles Associated with Diagnosis, Clinicopathologic Criteria, and Overall Survival in Patients with Resectable Pancreatic Ductal Adenocarcinoma
Jamieson, N. B., Morran, D. C., Morton, J. P., Ali, A., Dickson, E. J., Carter, C. R., Sansom, O. J., Evans, T. R. J., McKay, C. J., & Oien, K. A. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-0679 · Cited by 209 · see citing works
The Axl receptor tyrosine kinase confers an adverse prognostic influence in pancreatic cancer and represents a new therapeutic target
Koorstra, J.-B. M., Karikari, C. A., Feldmann, G., Bisht, S., Rojas, P. L., Offerhaus, G. J. A., Alvarez, H., & Maitra, A. (2009) · Cancer Biology & Therapy · doi:10.4161/cbt.8.7.7923 · Cited by 208 · see citing works
Self-citation
Metabolic reprogramming of pancreatic cancer mediated by CDK4/6 inhibition elicits unique vulnerabilities
Franco, J., Balaji, U., Freinkman, E., Witkiewicz, A. K., & Knudsen, E. S. (2016) · Cell Reports · doi:10.1016/j.celrep.2015.12.094 · Cited by 199 · see citing works
Biochemical role of the collagen-rich tumour microenvironment in pancreatic cancer progression
Shields, M. A., Dangi-Garimella, S. Y., Redig, A. J., & Munshi, H. G. (2011) · Biochemical Journal · doi:10.1042/bj20111240 · Cited by 203 · see citing works
Beyond just a tight fortress: contribution of stroma to epithelial-mesenchymal transition in pancreatic cancer
Bulle, A. S., & Lim, K. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00341-1 · Cited by 203 · see citing works
Inhibition of sonic hedgehog pathway and pluripotency maintaining factors regulate human pancreatic cancer stem cell characteristics
Tang, S., Fu, J., Nall, D., Rodova, M., Shankar, S., & Srivastava, R. K. (2011) · International Journal of Cancer · doi:10.1002/ijc.26323 · Cited by 203 · 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
Pancreatic cancer cell/fibroblast co-culture induces M2 like macrophages that influence therapeutic response in a 3D model
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Authors: Maitra, A., & Hruban, R. H.
Affiliations: Johns Hopkins University (US)
ORCID: Maitra, Anirban
Hruban, Ralph H.
Venue: Annual Review of Pathology: Mechanisms of Disease
Publisher: Annual Reviews
Published: 2008-02-01
Volume: 3
Issue: 1
Pages: 157-188
ISSN: 1553-4006 (ISSN-L)
1553-4014
DOI: 10.1146/annurev.pathmechdis.3.121806.154305
PMC: PMC2666336
OpenAlex: W4211122150
Cited by: 707
References: 185
Citations by year: 2026: 16 · 2025: 10 · 2024: 31 · 2023: 29 · 2022: 55 · 2021: 46 · 2020: 46 · 2019: 39 · 2018: 43 · 2017: 42 · 2016: 41 · 2015: 53 · 2014: 59 · 2013: 48 · 2012: 32
FWCI: 3.60
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Annual Review of Pathology Mechanisms of Disease (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (R01CA113669, P50CA062924)
Topics: Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Health Sciences › Medicine › Surgery › Pancreatitis Pathology and Treatment
Keywords: pancreatic cancer, germline mutations, somatic mutations, KRAS2, CDKN2A, TP53, genetic alterations, transcriptomic alterations, cell cycle dysregulation, metastasis, precursor lesions, genetically engineered mouse models, tumor progression, cancer stem cells, treatment resistance
MeSH terms: Animals, Disease Models, Animal, Humans, Pancreatic Neoplasms, Mice

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