PreprintCited by 533Pancreatic and Hepatic Oncology ResearchCancer Genomics and DiagnosticsCholangiocarcinoma and Gallbladder Cancer Studies

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Genetics and biology of pancreatic ductal adenocarcinoma

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Ying, Haoqiang, Dey, Prasenjit, Yao, Wantong, Kimmelman, Alec C., Draetta, Giulio F., Maitra, Anirban, DePinho, Ronald A.·2016·Genes & Development

DOI 10.1101/gad.275776.115

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Abstract

With 5-year survival rates remaining constant at 6% and rising incidences associated with an epidemic in obesity and metabolic syndrome, pancreatic ductal adenocarcinoma (PDAC) is on track to become the second most common cause of cancer-related deaths by 2030. The high mortality rate of PDAC stems primarily from the lack of early diagnosis and ineffective treatment for advanced tumors. During the past decade, the comprehensive atlas of genomic alterations, the prominence of specific pathways, the preclinical validation of such emerging targets, sophisticated preclinical model systems, and the molecular classification of PDAC into specific disease subtypes have all converged to illuminate drug discovery programs with clearer clinical path hypotheses. A deeper understanding of cancer cell biology, particularly altered cancer cell metabolism and impaired DNA repair processes, is providing novel therapeutic strategies that show strong preclinical activity. Elucidation of tumor biology principles, most notably a deeper understanding of the complexity of immune regulation in the tumor microenvironment, has provided an exciting framework to reawaken the immune system to attack PDAC cancer cells. While the long road of translation lies ahead, the path to meaningful clinical progress has never been clearer to improve PDAC patient survival.

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Autophagy in malignant transformation and cancer progression
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Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma
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Vitamin D Receptor-Mediated Stromal Reprogramming Suppresses Pancreatitis and Enhances Pancreatic Cancer Therapy
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Recruitment of P-TEFb for Stimulation of Transcriptional Elongation by the Bromodomain Protein Brd4
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Low-Dose Irradiation Programs Macrophage Differentiation to an iNOS+/M1 Phenotype that Orchestrates Effective T Cell Immunotherapy
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Cancer-Associated Stromal Fibroblasts Promote Pancreatic Tumor Progression
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Granzyme B and Perforin Are Important for Regulatory T Cell-Mediated Suppression of Tumor Clearance
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Whole-exome sequencing of pancreatic cancer defines genetic diversity and therapeutic targets
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“Correspondingly, PDACs harboring DDRmutations exhibit increased overall mutational burden and genomic instability (Waddell et al. 2015; Witkiewicz et al. 2015) and poorer prognosis (Witkiewicz et al. 2015).”
Influential
Nutrient-sensing mechanisms and pathways
Efeyan, A., Comb, W. C., & Sabatini, D. M. (2015) · Nature · doi:10.1038/nature14190 · Cited by 1,110
c-Myc Is a Universal Amplifier of Expressed Genes in Lymphocytes and Embryonic Stem Cells
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An Illustrated Consensus on the Classification of Pancreatic Intraepithelial Neoplasia and Intraductal Papillary Mucinous Neoplasms
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Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy
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Identification of Double-stranded Genomic DNA Spanning All Chromosomes with Mutated KRAS and p53 DNA in the Serum Exosomes of Patients with Pancreatic Cancer
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Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma
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“This mutation is a key initiator, as evidenced by its presence in PanIN lesions (Kanda et al. 2012; Murphy et al. 2013) and the production of PanIN lesions in oncogenic Kras-drivenGEMMs (Hezel et al. 2006; Perez-Mancera et al. 2012a).”
Influential
Links between metabolism and cancerPreprint
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Brick by brick: metabolism and tumor cell growth
DeBerardinis, R. J., Sayed, N., Ditsworth, D., & Thompson, C. B. (2008) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2008.02.003 · Cited by 1,018
The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors
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“The Pdx1 and Ptf1-p48 promoters are active in the common progenitors of all pancreatic cell types with relatively restricted expression outside of the pancreas (Pdx1 is also expressed in the developing duodenum and stomach, and Ptf1-p48 is expressed in the cerebellum) (Kawaguchi et al. 2002; Gu et al. 2003).”
Dynamics of the immune reaction to pancreatic cancer from inception to invasion
Clark, C. E., Hingorani, S. R., Mick, R., Combs, C., Tuveson, D. A., & Vonderheide, R. H. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0175 · Cited by 990
Targeting Tumor-Infiltrating Macrophages Decreases Tumor-Initiating Cells, Relieves Immunosuppression, and Improves Chemotherapeutic Responses
Mitchem, J. B., Brennan, D. J., Knolhoff, B. L., Belt, B. A., Zhu, Y., Sanford, D. E., Belaygorod, L., Carpenter, D. H., Collins, L. I., Piwnica-Worms, D. R., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-2731 · Cited by 964
Myeloid-Derived Suppressor Cells Inhibit T-Cell Activation by Depleting Cystine and Cysteine
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Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer
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“Clinical trials involving GVAX (allogeneic pancreatic cancer cells modified to express GM-CSF) alone and/or in combination with CRS207 (live attenuated Listeria monocytogenes expressing mesothelin) have shown positive outcomes and generated excitement among the immunotherapy community.”
Influential
Cutting Edge: Contact-Mediated Suppression by CD4+CD25+ Regulatory Cells Involves a Granzyme B-Dependent, Perforin-Independent Mechanism
Gondek, D. C., Lu, L., Quezada, S. A., Sakaguchi, S., & Noelle, R. J. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.4.1783 · Cited by 943
Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies
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Glucose Deprivation Contributes to the Development of KRAS Pathway Mutations in Tumor Cells
Yun, J., Rago, C., Cheong, I., Pagliarini, R., Angenendt, P., Rajagopalan, H., Schmidt, K., Willson, J. K. V., Markowitz, S., Zhou, S., et al. (2009) · Science · doi:10.1126/science.1174229 · Cited by 914
Treatment of Metastatic Melanoma with Autologous CD4+ T Cells against NY-ESO-1
Hunder, N. N. H., Wallen, H. D., Cao, J., Hendricks, D. W., Reilly, J. Z., Rodmyre, R. M., Jungbluth, A. A., Gnjatic, S., Thompson, J. A., & Yee, C. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0800251 · Cited by 904
Human pancreatic cancer tumors are nutrient poor and tumor cells actively scavenge extracellular protein
Kamphorst, J. J., Nofal, M., Commisso, C., Hackett, S. R., Lu, W., Grabocka, E., Vander Heiden, M. G., Miller, G., Drebin, J. A., Bar-Sagi, D., et al. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-2211 · Cited by 893
Clinical Significance and Therapeutic Potential of the Programmed Death-1 Ligand/Programmed Death-1 Pathway in Human Pancreatic Cancer
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A Revised Classification System and Recommendations From the Baltimore Consensus Meeting for Neoplastic Precursor Lesions in the Pancreas
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Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer
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Modelling Myc inhibition as a cancer therapy
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A Gene Expression Signature Associated with “K-Ras Addiction” Reveals Regulators of EMT and Tumor Cell Survival
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T Helper 17 Cells Promote Cytotoxic T Cell Activation in Tumor Immunity
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Tumor-Derived Lactate Modifies Antitumor Immune Response: Effect on Myeloid-Derived Suppressor Cells and NK Cells
Husain, Z., Huang, Y., Seth, P., & Sukhatme, V. P. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202702 · Cited by 827
Exomic Sequencing Identifies PALB2 as a Pancreatic Cancer Susceptibility Gene
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“Germline mutations of some DDR genes, such as BRCA1, BRCA2, PALB2, ATM, MLH1, MSH2, and MSH6, have been linked to an increased predisposition to PDAC (Goggins et al. 1996; Thompson et al. 2002; Jones et al. 2009; Roberts et al. 2012; Grant et al. 2015; Holter et al. 2015).”
Oncogenic BRAF Regulates Oxidative Metabolism via PGC1α and MITF
Haq, R., Shoag, J., Andreu-Perez, P., Yokoyama, S., Edelman, H., Rowe, G. C., Frederick, D. T., Hurley, A. D., Nellore, A., Kung, A. L., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.02.003 · Cited by 818
Transcriptional control of autophagy-lysosome function drives pancreatic cancer metabolism
Perera, R. M., Stoykova, S., Nicolay, B. N., Ross, K. N., Fitamant, J., Boukhali, M., Lengrand, J., Deshpande, V., Selig, M. K., Ferrone, C. R., et al. (2015) · Nature · doi:10.1038/nature14587 · Cited by 799
Demethylation of H3K27 Regulates Polycomb Recruitment and H2A Ubiquitination
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Biochemical and Structural Analysis of Common Cancer-Associated KRAS Mutations
Hunter, J. C., Manandhar, A., Carrasco, M. A., Gurbani, D., Gondi, S., & Westover, K. D. (2015) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-15-0203 · Cited by 786
Recurrent GNAS Mutations Define an Unexpected Pathway for Pancreatic Cyst Development
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International Cancer of the Pancreas Screening (CAPS) Consortium summit on the management of patients with increased risk for familial pancreatic cancer
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Stromal biology and therapy in pancreatic cancer
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Myeloid suppressor cells in cancer: Recruitment, phenotype, properties, and mechanisms of immune suppression
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Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice
Collins, M. A., Bednar, F., Zhang, Y., Brisset, J.-C., Galbán, S., Galbán, C. J., Rakshit, S., Flannagan, K. S., Adsay, N. V., & Pasca di Magliano, M. (2012) · Journal of Clinical Investigation · doi:10.1172/jci59227 · Cited by 770
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 752
Molecular Mechanisms of Resistance to Cetuximab and Panitumumab in Colorectal Cancer
Bardelli, A., & Siena, S. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.24.6116 · Cited by 746
KRAS and YAP1 Converge to Regulate EMT and Tumor Survival
Shao, D. D., Xue, W., Krall, E. B., Bhutkar, A., Piccioni, F., Wang, X., Schinzel, A. C., Sood, S., Rosenbluh, J., Kim, J. W., et al. (2014) · Cell · doi:10.1016/j.cell.2014.06.004 · Cited by 744
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
Induction of Membrane Ruffling and Fluid-Phase Pinocytosis in Quiescent Fibroblasts by ras Proteins
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Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes
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Hypoxic and Ras-transformed cells support growth by scavenging unsaturated fatty acids from lysophospholipids
Kamphorst, J. J., Cross, J. R., Fan, J., de Stanchina, E., Mathew, R., White, E. P., Thompson, C. B., & Rabinowitz, J. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307237110 · Cited by 726
MYC/PGC-1α Balance Determines the Metabolic Phenotype and Plasticity of Pancreatic Cancer Stem Cells
Sancho, P., Burgos-Ramos, E., Tavera, A., Bou Kheir, T., Jagust, P., Schoenhals, M., Barneda, D., Sellers, K., Campos-Olivas, R., Graña, O., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.08.015 · Cited by 722
Metabolic Reprogramming of Immune Cells in Cancer Progression
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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 · cited 2×
“…PI3K inhibitors can attenuate the release of G-CSF and improve survival in an orthotopic allograft mouse model established by injecting primary ductal epithelial cells (PDECs) isolated from aGEMMof PDAC into the pancreata of syngeneic C57Bl/6 mice (Cox and Olive 2012; Pylayeva-Gupta et al. 2012).”
Intratumor T helper type 2 cell infiltrate correlates with cancer-associated fibroblast thymic stromal lymphopoietin production and reduced survival in pancreatic cancer
Monte, L. B. D., Reni, M., Tassi, E., Clavenna, D., Papa, I., Recalde, H. R., Braga, M., Carlo, V. D., Doglioni, C., & Protti, M. P. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20101876 · Cited by 721
Yap1 Activation Enables Bypass of Oncogenic Kras Addiction in Pancreatic Cancer
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“…importantly, while multiple mechanisms leading to resistance to KRAS inactivation have been identified in various experimental models, these KRAS-bypass pancreatic tumors exhibit expression signatures reminiscent of a subset of human PDACs; namely, the quasimesenchymal subtype (Kapoor et al. 2014).”
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PGC1α Expression Defines a Subset of Human Melanoma Tumors with Increased Mitochondrial Capacity and Resistance to Oxidative Stress
Vazquez, F., Lim, J.-H., Chim, H., Bhalla, K., Girnun, G., Pierce, K., Clish, C. B., Granter, S. R., Widlund, H. R., Spiegelman, B. M., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2012.11.020 · Cited by 715
Blood-Based Analyses of Cancer: Circulating Tumor Cells and Circulating Tumor DNA
Haber, D. A., & Velculescu, V. E. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-1014 · Cited by 710
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Maitra, A., & Hruban, R. H. (2008) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev.pathmechdis.3.121806.154305 · Cited by 707
Identification of Sox9-dependent acinar-to-ductal reprogramming as the principal mechanism for initiation of pancreatic ductal adenocarcinoma
Kopp, J. L., von Figura, G., Mayes, E., Liu, F.-F., Dubois, C. L., Morris, J. P., Pan, F. C., Akiyama, H., Wright, C. V. E., Jensen, K., et al. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.10.025 · Cited by 697
Preclinical Mouse Cancer Models: A Maze of Opportunities and Challenges
Day, C.-P., Merlino, G., & Van Dyke, T. (2015) · Cell · doi:10.1016/j.cell.2015.08.068 · Cited by 676
Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer
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Whole-exome sequencing of neoplastic cysts of the pancreas reveals recurrent mutations in components of ubiquitin-dependent pathways
Wu, J., Jiao, Y., Molin, M. D., Maitra, A., de Wilde, R. F., Wood, L. D., Eshleman, J. R., Goggins, M., Wolfgang, C. L., Canto, M. I., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118046108 · Cited by 652
Germline BRCA2 gene mutations in patients with apparently sporadic pancreatic carcinomas.
Goggins, M., Schutte, M. E. M., Lü, J., Moskaluk, C. A., Weinstein, C. L., Petersen, G. M., Yeo, C. J., Jackson, C. E., Lynch, H. T., Hruban, R. H., et al. (1996) · PubMed · Cited by 642
Safety and Survival With GVAX Pancreas Prime and Listeria Monocytogenes –Expressing Mesothelin (CRS-207) Boost Vaccines for Metastatic Pancreatic Cancer
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Non-cell-autonomous driving of tumour growth supports sub-clonal heterogeneity
Marusyk, A., Tabassum, D. P., Altrock, P. M., Almendro, V., Michor, F., & Polyák, K. (2014) · Nature · doi:10.1038/nature13556 · Cited by 606
FoxO transcription factors in the maintenance of cellular homeostasis during aging
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Binding of Ras to Phosphoinositide 3-Kinase p110α Is Required for Ras- Driven Tumorigenesis in Mice
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The dynamic nature of autophagy in cancerPreprint
Kimmelman, A. C. (2011) · Genes & Development · doi:10.1101/gad.17558811 · Cited by 599
KRAS, Hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma
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Small molecule inhibition of the KRAS–PDEδ interaction impairs oncogenic KRAS signalling
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Autophagy suppresses progression of K-ras-induced lung tumors to oncocytomas and maintains lipid homeostasis
Guo, J. Y., Karsli-Uzunbas, G., Mathew, R., Aisner, S. C., Kamphorst, J. J., Strohecker, A. M., Chen, G., Price, S., Lu, W., Teng, X., et al. (2013) · Genes & Development · doi:10.1101/gad.219642.113 · Cited by 589
Both p16 Ink4a and the p19 Arf -p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse
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Authors: Ying, H., Dey, P., Yao, W., Kimmelman, A. C., Draetta, G. F., Maitra, A., & DePinho, R. A.
Affiliations: The University of Texas MD Anderson Cancer Center (US)
Dana-Farber Cancer Institute (US)
ORCID: Ying, Haoqiang
Dey, Prasenjit
Yao, Wantong
Kimmelman, Alec C.
Draetta, Giulio F.
Maitra, Anirban
DePinho, Ronald A.
Venue: Genes & Development
Publisher: Cold Spring Harbor Laboratory
Published: 2016-02-15
Volume: 30
Issue: 4
Pages: 355-385
ISSN: 0890-9369 (ISSN-L)
1549-5477
DOI: 10.1101/gad.275776.115
OpenAlex: W4295846302
Cited by: 527
References: 392
Citations by year: 2026: 20 · 2025: 33 · 2024: 44 · 2023: 68 · 2022: 56 · 2021: 75 · 2020: 57 · 2019: 48 · 2018: 51 · 2017: 59 · 2016: 16
Type: posted content
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc
Locations: Genes & Development (publishedVersion, cc-by-nc)
HighWire Press Open Archive (submittedVersion)
Funders: Sheikh Ahmed Center for Pancreatic Cancer Research
Pancreatic Cancer Moon Shot at the University of Texas MD Anderson Cancer Center
University of Texas Star Award (W81XWH-14-1-0429)
Department of Defense (U01DK108328, U01CA196403)
Odyssey Fellowship (Anne Eastland Spears Fellowship in GI Cancer Research)
University of Texas MD Anderson Cancer Center (RSG-13-298-01-TBG)
American Cancer Society (R01GM095567, R01CA157490, R01CA188048)
National Institutes of Health (14-90-25-DRAE, P01CA117969)
American Association for Cancer Research (W81XWH-11-1-0418)
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 › Cholangiocarcinoma and Gallbladder Cancer Studies
Keywords: pancreatic ductal adenocarcinoma, cancer genomics, molecular classification, cancer metabolism, DNA repair, tumor microenvironment, cancer immunotherapy, drug discovery, obesity, metabolic syndrome, preclinical models

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Genetics and biology of pancreatic ductal adenocarcinoma

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